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The structure of the conus arteriosus of the sturgeon (Acipenser naccarii) heart: II. The myocardium, the subepicardium, and the conus-aorta transition
Abstract
Sturgeons constitute a family of living "fossil" fish whose heart is related to that of other ancient fish and the elasmobranches. We have undertaken a systematic study of the structure of the sturgeon heart aimed at unraveling the relationship between the heart structure and the adaptive evolutionary changes. In a related paper, data were presented on the conus valves and the subendocardium. Here, the structure of the conus myocardium, the subepicardial tissue, and the conus-aorta transition were studied by conventional light, transmission, and scanning electron microscopy. In addition, actin localization by fluorescent phalloidin was used. The conus myocardium is organized into bundles whose spatial organization changes along the conus length. The variable orientation of the myocardial cell bundles may be effective in emptying the conus lumen during contraction and in preventing reflux of blood. Myocardial cell bundles are separated by loose connective tissue that contains collagen and elastin fibers, vessels, and extremely flat cells separating the cell bundles and enclosing blood vessels and collagen fibers. The ultrastructure of the myocardial cells was found to be very similar to that of other fish groups, suggesting that it is largely conservative. The subepicardium is characterized by the presence of nodular structures that contain lympho-hemopoietic (thymus-like) tissue in the young sturgeons and a large number of lymphocytes after the sturgeons reach sexual maturity. This tissue is likely implicated in the establishment and maintenance of the immune responses. The intrapericardial ventral aorta shows a middle layer of circumferentially oriented cells and internal and external layers with cells oriented longitudinally. Elastin fibers completely surround each smooth muscle cell, and the spaces between the different layers are occupied by randomly arranged collagen bundles. The intrapericardial segment of the ventral aorta is a true transitional segment whose structural characteristics are different from those of both the conus subendocardium and the rest of the ventral aorta.
... In adult teleosts, haematopoietic organs comprise head kidney and trunk kidney, as well as spleen, thymus, liver and intestinal mucosa (Zapata et al. 2006). Sturgeon, however, possess additional haematopoietic pericardial tissue and haematopoietic meningeal tissue in cartilaginous skull capsules, located above the medulla oblongata and the anterior notochord (F€ ange 1986;Lange et al. 2000;Icardo et al. 2002;Gradil et al. 2014b;Liu et al. 2017b). ...
... The subepicardium of the sturgeon heart contains nodular structures, separated by connective or adipose tissue. In young specimens, it contains thymus-like lympho-haematopoietic cells (F€ ange 1986;Lange et al. 2000;Icardo et al. 2002). Icardo et al. (2002) suggest the subepicardium to establish and maintain the immune responses in sturgeon. ...
... In young specimens, it contains thymus-like lympho-haematopoietic cells (F€ ange 1986;Lange et al. 2000;Icardo et al. 2002). Icardo et al. (2002) suggest the subepicardium to establish and maintain the immune responses in sturgeon. This structure is changing with age, losing distinct organization with sexual maturity. ...
Sturgeon immunity is relevant for basic evolutionary and applied research, including caviar-and meat-producing aquaculture, protection of wild sturgeons and their re-introduction through conservation aquaculture. Starting from a comprehensive overview of immune organs, we discuss pathways of innate and adaptive immune systems in a vertebrate phylogenetic and genomic context. The thymus as a key organ of adaptive immunity in sturgeons requires future molecular studies. Likewise, data on immune functions of sturgeon-specific pericardial and meningeal tissues are largely missing. Integrating immunological and endo-crine functions, the sturgeon head kidney resembles that of teleosts. Recently identified pattern recognition receptors in sturgeon require research on downstream regulation. We review first acipenseriform data on Toll-like receptors (TLRs), type I transmembrane glycoproteins expressed in membranes and endo-somes, initiating inflammation and host defence by molecular pattern-induced activation. Retinoic acid-inducible gene-I-like (RIG-like) receptors of sturgeons present RNA and key sensors of virus infections in most cell types. Sturgeons and teleosts share major components of the adaptive immune system, including B cells, immunoglobulins, major histocompatibility complex and the adaptive cellular response by T cells. The ontogeny of the sturgeon innate and onset of adaptive immune genes in different organs remain understudied. In a genomics perspective , our new data on 100 key immune genes exemplify a multitude of evolutionary trajectories after the sturgeon-specific genome duplication, where some single-copy genes contrast with many duplications, allowing tissue specialization, sub-functionalization or both. Our preliminary conclusion should be tested by future evolutionary bioinformatics, involving all >1000 immunity genes. This knowledge update about the acipenseriform immune system identifies several important research gaps and presents a basis for future applications.
... Recent studies also indicate a complex situation in basal species. Chondrichthyans (Durán et al., 2008), chondrosteans (Durán et al., 2014;Icardo et al., 2002a), and holosteans (Grimes et al., 2010) display a discrete arterial-like segment, the bulbus arteriosus, interposed between the conus and the ventral aorta. It should be underscored that only a small number of species have been examined, but in all the cases, a conus and a bulbus can be recognized within the pericardial cavity. ...
... A compact layer is observed in all elasmobranchs (Figs. 3A and 7A), in sturgeons (Icardo et al., 2002a), in the holostean Amia calva (unpublished observation), and in many teleost species (Figs. 3B and 8), especially the Clupeidae, Salmonidae, Anguillidae, Carangidae, and Scombridae families (see Santer and Greer Walker, 1980). ...
... The dimensions of the cylinder are not regular, being thicker in the middle. This occurs, at least, in rays (Fig. 3A), sturgeons (Icardo et al., 2002a) and bichirs (Fig. 2B). The wall of the conus is organized into layers. ...
This chapter covers morphological aspects of the fish heart. It starts with the recognition of the existence of six heart components that are present during embryonic development, and in the adult, and that are anatomically arranged in sequence: sinus venosus, atrium, atrioventricular canal, ventricle, conus arteriosus, and bulbus arteriosus. The anatomy and structure of all the cardiac components are then described and compared between the different fish groups. Data from the basal Cyclostomata, chondrichthyans, basal Osteichthyes, and more advanced teleosts are included and analyzed. Then, data on blood supply to the heart, nerves, and localization of the heart pacemaker are discussed. A separate section at the end of the chapter is committed to the lungfish heart. Lungfishes share many anatomical and functional characteristics with both freshwater fish and amphibians, and the lungfish heart shows some unique and very peculiar characteristics. The enormous diversification of morphological characteristics of the fish heart is emphasized throughout this chapter.
... The out fl ow tract (OFT) is the morphological division of the heart located between the ventricle and the beginning of the dorsal aorta. In most primitive fi sh, the OFT is formed by two segments: a proximal, muscular, conus arteriosus, and a distal, arterial-like, bulbus arteriosus (Icardo et al. 2002(Icardo et al. , 2005aDurán et al. 2008 ;Grimes and Kirby 2009 ) . The anatomical composition of the OFT in several other ancient fi sh, like hag fi shes and lampreys, is unclear, but most uncertainties appear to derive from partial observations (Parsons 1930 ;Yamauchi 1980 ) . ...
... This is surprising, but it is not an isolated feature in fi sh. The subepicardium of the sturgeon contains thymus-like tissue (Icardo et al. 2002 ) which has been implicated in the The out fl ow tract, the ventricle (V), and the atrioventricular (AV) regions are exposed. The bulbus (B) shows well-marked longitudinal ridges. ...
... The lea fl ets present a thick luminal fi brosa, which probably bears most of the stress generated by the back fl ow of blood (Icardo et al. 2003 ;Icardo 2006 ) . This is a feature shared with other fi sh groups (Sans-Coma et al. 1995 ;Icardo et al. 2002 ) , but it is opposite to the situation observed in mammals, where the fi brosa is located on the parietal side of the lea fl et. Differences in extracellular matrix composition have been described in the conus valves of several teleost species (Greer Walker et al. 1985 ;Raso 1993 ;Icardo et al. 2003 ) . ...
This chapter addresses the morphology of the teleost heart. The heart of this fish group is being used as a model organ to study numerous genetic and epigenetic mechanisms of great biological importance. Full understanding of the developmental and phylogenetic implications of these mechanisms requires a precise knowledge of the final organ anatomy. However, a comprehensive review focused on the morphological aspects of the teleost heart is still lacking. The anatomy and structure of the heart outflow, the ventricle, and the venous pole of the teleost heart are reviewed here. Anatomical descriptions are linked, when appropriate, to evolutionary and functional considerations. Rather than being focused on any particular species, this manuscript intends to reflect the enormous morphological diversity of the teleost heart, put the focus on controversial issues, and addresses matters of general morpho-functional significance.
... Internally, it progressively adopts an arterial-like organization (Fig. 8.3c and d). In the adult heart, this segment shows organized layers of smooth muscle cells, collagen and elastin (Icardo et al., 2002b). Since the organization of these layers is different on each side of the pericardial attachment, the distal OFT portion has recently been termed the transitional segment (Icardo et al., 2002b), suggesting a different origin from the rest of the ventral aorta, or bulbus arteriosus (Guerrero et al., 2004), by homology with the teleost bulbus. ...
... In the adult heart, this segment shows organized layers of smooth muscle cells, collagen and elastin (Icardo et al., 2002b). Since the organization of these layers is different on each side of the pericardial attachment, the distal OFT portion has recently been termed the transitional segment (Icardo et al., 2002b), suggesting a different origin from the rest of the ventral aorta, or bulbus arteriosus (Guerrero et al., 2004), by homology with the teleost bulbus. The early changes observed in the distal OFT have been suggested to represent a phenotypic transformation, from a myocardial to a smooth muscle-like phenotype (Guerrero et al., 2004). ...
... Another interesting feature of the subepicardium is the presence, in the conus and in the ventricle, of nodular structures that contain lympho-hemopoietic, thymus-like tissue (Icardo et al., 2002b). It is precisely the presence of these nodes, and that of the surrounding adipose tissue, that gives to the heart surface a cobblestone appearance (Fig. 8.2d). ...
We review the anatomic development of the sturgeon’s (Acipenser naccarii) heart. Attention has been focussed on the main developmental events that take place during the embryonic and early post-hatching
periods. The study examines identification of the early heart tube, cardiac loop formation, and the transformation of the
tubular heart into a multi-chambered organ in a temporal sequence. Also included are the development of the heart valves and
that of the epicardium. Many of these processes have been followed into adulthood to illustrate the maturation of the different
structures with age. On the whole, sturgeon heart formation appears to share many developmental mechanisms with other vertebrates.
This indicates the conservation of the mechanisms along the phyletic scale. The development of the A. naccarii heart appears to be a very slow process in relation both to other sturgeon species and to other fish classes. This should
allow detailed investigation of specific morphologic events. Many of the developmental changes experienced by the heart could
well prove useful in establishing the chronology of both embryonic and juvenile specimens.
... Recent studies also indicate a complex situation in basal species. Chondrichthyans (Durán et al., 2008), chondrosteans (Durán et al., 2014;Icardo et al., 2002a), and holosteans (Grimes et al., 2010) display a discrete arterial-like segment, the bulbus arteriosus, interposed between the conus and the ventral aorta. It should be underscored that only a small number of species have been examined, but in all the cases, a conus and a bulbus can be recognized within the pericardial cavity. ...
... A compact layer is observed in all elasmobranchs (Figs. 3A and 7A), in sturgeons (Icardo et al., 2002a), in the holostean Amia calva (unpublished observation), and in many teleost species (Figs. 3B and 8), especially the Clupeidae, Salmonidae, Anguillidae, Carangidae, and Scombridae families (see Santer and Greer Walker, 1980). ...
... The dimensions of the cylinder are not regular, being thicker in the middle. This occurs, at least, in rays (Fig. 3A), sturgeons (Icardo et al., 2002a) and bichirs (Fig. 2B). The wall of the conus is organized into layers. ...
The subject of heart development has attracted the interest of many embryologists over the last two centuries. As a result, the main morphologic features of the developmental anatomy of the heart are already well established. Although there are still some controversial points, and there is probably much descriptive work yet to be done, emphasis is currently being placed on developmental mechanisms rather than simply on descriptive facts. The availability of new techniques and the overall advances in biological research are placing heart embryology in a new perspective. Today, we do not simply ask whether one or another embryonic structure arises further right or further left; instead, we are studying how cells, tissues, and their microenvironment interrelate at the several levels of biological organization (from the gene upwards) so as to give rise to a mature organ with a distinct shape and well-established functions.
This paper attempts to review some of the basic aspects of the developmental anatomy of the heart. Descriptive embryology is used here as a tool. Emphasis is placed on developmental mechanisms, and on the present knowledge of how these mechanisms are related to the structural development of the heart.
... In addition, a distinct intima-like layer is located between the inner elastica and the smooth muscle cells. These structural differences between the two aortic portions indicate that the intrapericardial segment constitutes a transitional segment, the embryonic origin of which might differ from that of the extrapericardial ventral aorta (Icardo et al., 2002b). ...
... The distal component displays a nonmyocardial character and, presumably, transforms into the transitional (or intermediate) segment, intercalated between the conus arteriosus and the ventral aorta, as described by Icardo et al. (2002a,b) in adult sturgeons. The present data on the formation of this transitional segment supports the notion of Icardo et al. (2002b) that its morphogenetic origin diverges from that of the ventral aorta, a fact which may explain the structural differences between them in the adult heart (see Icardo et al., 2002a,b). ...
... From the preceding data we conclude that a true bulbus arteriosus exists in primitive actinopterygian fishes, i.e., the sturgeons; it corresponds to the secondarily nonmyocardial, distal portion of the cardiac OFT that Icardo et al. (2002b) referred to by using the term "intrapericardial transitional segment". Moreover, we presume that a bulbus arteriosus also exists in the elasmobranchs. ...
Previous work showed that in the adult sturgeon an intrapericardial, nonmyocardial segment is interposed between the conus arteriosus of the heart and the ventral aorta. The present report illustrates the ontogeny of this intermediate segment in Acipenser naccarii. The sample studied consisted of 178 alevins between 1 and 24 days posthatching. They were examined using light and electron microscopy. Our observations indicate that the entire cardiac outflow tract displays a myocardial character during early development. Between the fourth and sixth days posthatching, the distal portion of the cardiac outflow tract undergoes a phenotypical transition, from a myocardial to a smooth muscle-like phenotype. The length of this region with regard to the whole outflow tract increases only moderately during subsequent developmental stages, becoming more and more cellularized. The cells soon organize into a pattern that resembles that of the arterial wall. Elastin appears at this site by the seventh day posthatching. Therefore, two distinct components, proximal and distal, can be recognized from the fourth day posthatching in the cardiac outflow tract of A. naccarii. The proximal component is the conus arteriosus, characterized by its myocardial nature and the presence of endocardial cushions. The distal component transforms into the intrapericardial, nonmyocardial segment mentioned above, which is unequivocally of cardiac origin. We propose to designate this segment the "bulbus arteriosus" because it is morphogenetically equivalent to the bulbus arteriosus of teleosts. The present findings, together with data from the literature, point to the possibility that cells from the cardiac neural crest are involved in the phenotypical transition that takes place at the distal portion of the cardiac outflow tract, resulting in the appearance of the bulbus arteriosus. Moreover, they suggest that the cardiac outflow tract came to be formed by a bulbus arteriosus and a conus arteriosus from an early period of the vertebrate evolutionary story. Finally, we hypothesize that the embryonic truncus of birds and mammals is homologous to the bulbus arteriosus of fish.
... The conus shows a relatively thick layer of compact myocardium and is endowed with several rows of valves. The OFT of the primitive actinopterygians such as the polypteriforms (Parsons, 1930), holosteans (Parsons, 1930;Bertin, 1958), and chondrosteans (Parsons, 1930;Icardo et al., 2002aIcardo et al., , 2002b also presents a distinct conus arteriosus. The same is true for coelacanths (Anthony et al., 1965) and for lungfishes (Robertson, 1914;Icardo et al., 2005). ...
... Near this boundary, the OFT wall was formed by an elastic tissue similar to that of the aorta. The presence of a comparable segment has been reported in the holostean Amia calva (Parsons, 1930), in chondrosteans (Icardo et al., 2002b;Guerrero et al., 2004), and in lungfishes (Bugge, 1961;Icardo et al., 2005). A similar segment has not been found in other ancient fish (coelacanths), or its existence has been denied (Polypterus, chondrosteans, and most of the holosteans). ...
... However, the nature of some of these affirmations should be put under closer scrutiny. As stated above, chondrosteans have a distinct arteriallike segment included within the pericardial cavity (Icardo et al., 2002b;Guerrero et al., 2004), although the existence of this segment was unrecognized in early reports (Parsons, 1930). On the other hand, the configuration of the OFT in the most primitive chordates, hagfishes and lampreys, is unclear. ...
The heart outflow tract (OFT) of primitive fish is formed by two portions: a proximal conus arteriosus and a distal bulbus arteriosus. The OFT of modern teleosts is considered to be formed by a single component, the bulbus, the conus having been lost through evolution. This article challenges the concept of the disappearance of the conus arteriosus in the teleost heart. A total of 28 teleost species belonging to 19 families and 10 orders were analyzed. The hearts were divided into two large groups: those having entirely trabeculated ventricles, and those possessing a compacta. In the hearts having entirely trabeculated ventricles, the conus arteriosus appears as a distinct segment interposed between the ventricle and the bulbus arteriosus, being formed by compact vascularized myocardium. However, the conus of several species lacks vessels. In these cases, the conus presents large intercellular spaces bounded by collagen. In the hearts possessing a ventricular compacta, the conus either appears as a muscular ring of variable length connecting the ventricle and the bulbus or forms a crown or ring of myocardium apposed to the ventricular base. In all the teleosts studied, the conus can be recognized as an anatomic entity different from the ventricle. Furthermore, the conus appears as a distinct heart segment in the developing fish. Therefore, the conus arteriosus has not been lost in evolution and constitutes a fundamental part of the teleost OFT. In all the species studied, the conus supports the OFT valves, which should properly be named conus valves.
... A distinct bulbus arteriosus was almost certainly located between them. The conus is usually more developed in size than the bulbus in chondrichthyans (Durán et al., 2008) and early actinopterygians such as the polypteriforms (Grimes and Kirby, 2009;Grimes et al., 2010;Durán et al., 2014), acipenseriforms (Icardo et al., 2002a(Icardo et al., , 2002bGuerrero et al., 2004;Grimes et al., 2010), lepisosteiforms (Grimes and Kirby, 2009;Grimes et al., 2010) and amiiforms (Boas, 1880;Senior, 1907aSenior, , 1907bSenior, , 1907cParsons, 1930;Grimes and Kirby, 2009;Grimes et al., 2010). A conspicuous conus coexists with a patent bulbus in species belonging to the ancient teleost genera Albula, Pterothrisus and Megalops (= Tarpon) (Stannius, 1846;Boas, 1880;Senior, 1907a,b,c). ...
... A conspicuous conus coexists with a patent bulbus in species belonging to the ancient teleost genera Albula, Pterothrisus and Megalops (= Tarpon) (Stannius, 1846;Boas, 1880;Senior, 1907a,b,c). In the teleosts, the bulbus has evolved into a well-developed compartment, splitting into a wide range of structural variants (Icardo et al., 1999a(Icardo et al., , 1999b(Icardo et al., , 2002a(Icardo et al., , 2002b, while the conus has undergone a remarkable reduction in size, though without disappearing (Icardo, 2006), as had been commonly assumed in classic work. In this context, it should be stressed that recent work has shown that the bulbus arteriosus of the extant teleosts exhibits a characteristic that makes it unique regarding other fish, namely the fact that its wall contains elastin b (Moriyama et al., 2016). ...
This study was designed to determine whether the outflow tract of the holocephalan heart is composed of a myocardial conus arteriosus and a non-myocardial bulbus arteriosus, as is the case in elasmobranchs. This is a key issue to verify the hypothesis that these two anatomical components existed from the onset of the jawed vertebrate radiation. The Holocephali are the sister group of the elasmobranchs, sharing with them a common, still unknown Palaeozoic ancestor. The sample examined herein consisted of hearts from individuals of four species, two of them belonging to the Chimaeridae and the other two to the Rhinochimaeridae. In all specimens, the cardiac outflow tract consisted of a conus arteriosus, with myocardium in its walls and two rows of valves at its luminal side, and an intrapericardial bulbus arteriosus shorter than the conus and devoid of valves. The bulbus, mainly composed of elastin and smooth musculature, was covered by the epicardium and crossed longitudinally by coronary artery trunks. These findings give added support to the viewpoint that the outflow tract of the primitive heart of the gnathostomes was not composed of a single component, but two, the conus and the bulbus. All rabbitfish (Chimaera monstrosa) examined had pigment cells over the surface of the heart. The degree of pigmentation, which varied widely between individuals, was particularly intense in the cardiac outflow tract. Pigment cells also occurred in the bulbus arteriosus of one of the two hearts of the straightnose rabbitfish (Rhinochimaera atlantica) included in the study. The cells containing pigment, presumably derived from the neural crest, were located in the subepicardium.
... The bulbus arteriosus is the dominant portion of the OFT in derived teleosts, and was considered to be an acquisition of this fish group (see Icardo, 2012). However, recent evidence indicates that in more basal osteichthyes and in chondrichthyes (Icardo et al., 2002;Dur an et al., 2008;Grimes et al., 2010), a distinct bulbus arteriosus, connecting the conus and the ventral aorta, is present within the pericardial cavity. ...
... In fact, they constitute a structural continuum. Where studied (Icardo et al., 2002), the histological organization of the ventral aorta and the bulbus differs significantly, existing a sharp modification at the boundary between the two structures. The asymmetry of the aorta-ventricle junction is intriguing, but we do not have any clear explanation for this feature. ...
We have studied the heart in three species of hagfish: Myxine glutinosa, Eptatretus stoutii, and Eptatretus cirrhatus and report about the morphology of the ventricle, the arterial connection and the ventral aorta. On the whole, the hagfish heart lacks outflow tract components, the ventricle and atrium adopt a dorso-caudal rather than a ventro-dorsal relationship, and the sinus venosus opens into the left side of the atrium. This may indicate a "defective" cardiac looping during embryogenesis. The ventral aorta is elongated in M. glutinosa and E. stoutii but sac-like in E. cirrhatus. The ventricles are entirely trabeculated. The myocytes show a low myofibrillar content and junctional complexes formed by fascia adherens and desmosomes. Gap junctions could not be demonstrated. Myocardial cells in M. glutinosa contain numerous lipid droplets. These droplets are less numerous in E. stoutii and practically absent in E. cirrhatus, suggesting different metabolic requirements. Other cell types present in the ventricle are chromaffin cells and granular leukocytes that contain rod-shaped granules. The ventricle-aorta connection is guarded by a bicuspid valve with left and right, pocket-like leaflets. The leaflets extend from the cranial end of the ventricle into the aorta but the junction is asymmetrical. This junction contains a ganglion-like structure in E. cirrhatus. The ventral aorta shows endothelial, media, and adventitial layers. The media contains smooth muscle cells surrounded by dense bands formed by tightly-packed extracellular filaments. In addition, a short number of elastic fibers are observed in M. glutinosa and E. stoutii. Cellular and extracellular elements are more loosely organized in the aorta of E. cirrhatus. The collagenous adventitia contains ganglion-like cells in the three species. In the absence of nerves, chromaffin and ganglion-like cells may control the activity of the myocardium and that of the aortic smooth muscle cells, respectively.
... Valve systems appear at the sinoatrial and atrioventricular junctions and in the conus arteriosus (Burggren et al., 1997). Recently, a systematic study of the structural characteristics of the adult outflow tract has been reported (Icardo et al., 2002a(Icardo et al., , 2002b. During the embryonic period, we have also studied the development of the bulbus portion of the outflow tract (Guerrero et al., 2004). ...
... All these features are summarized in Table 1. Other important developmental steps such as the compaction of the outer ventricular myocardium and the establishment of the ventricular vasculature (later than 45 dph), or the development of the complex subepicardium containing thymus-like nodes (later than 90 dph) (see Icardo et al., 2002b), are late events and, consequently, are not registered here. ...
This paper presents a sequential analysis of the development of the sturgeon (Acipenser naccarii) heart from the end of gastrulation to the early juvenile stages. At late neurulation, the heart appears as a straight, short tube located over the endoderm that forms the wall of the yolk sac, in front of the developing head. The heart axis is aligned with the axis of the developing head. Subsequently, the heart elongates and adopts a C-shape, and its axis becomes perpendicular to that of the head. Around the time of hatching, the heart loses the loop and appears as a mostly straight tube with the chambers arranged in a craniocaudal sequence: outflow tract, ventricle, atrium, and a small sinus venosus. During the first 4 days post-hatching (dph), the heart starts looping again, adopts a C-shape, and undergoes a counterclockwise movement that brings the atrium to the left of the outflow tract and the ventricle to a caudal position. Thus, a primary and a secondary cardiac loop occur in the sturgeon. Later, the atria come to occupy a middle position behind the outflow tract, and the sinus venosus shifts from a caudal to a dorsal position. A morphological arrangement similar to that found in adult sturgeons is attained in all specimens at days 7-9 dph. The external changes are accompanied by a series of internal modifications that include trabeculation (3-4 dph), development of endocardial cushions in the atrioventricular canal (4 dph) and in the conus arteriosus (3-4 dph), conus (22-24 dph) and atrioventricular (18-20 dph) valve formation, and development of the epicardium (4 dph) and the coronary vessels (10 dph). The main developmental features of the heart have been registered, and a basic body of information, which should be very useful in future developmental studies, has been established. Similarities and dissimilarities between the development of the sturgeon heart and that of other vertebrates are underscored.
... reported as an epicardial lympho-haematopoietic tissue by Icardo et al. (2002). This 295 nodular tissue has to be studied further to identify the cells responsible for the uptake and We conclude that there is neither a clear phylogenetic trend to explain anatomical 323 localization of SECs, nor any pattern in terms of habitat (salinity preferences). ...
... In basal actinopterygians, the conus arteriosus dominates the cardiac outflow, while in teleosts, it is the bulbus arteriosus that prevails, a notion that harks back to Gegenbaur (1866) and before. The conus arteriosus displays multiple fibrous valve rows, a character state that represents the general gnathostome condition, primitively retained in basal actinopterygian groups (Durán et al., 2008;Boas, 1880;Boas, 1901;Schib et al., 2002;Xavier-Neto et al., 2010;Parsons, 1929;Icardo et al., 2002a;Durán et al., 2014;Icardo et al., 2002b). The multiple conal valve rows of basal actinopterygians prevent backflow and protect the delicate gill vessels from the elevated pulsations generated by the ventricle (Satchell and Jones, 1967). ...
ELife digest
Modern research has majorly advanced our understanding of how the heart works, and has led to new therapies for cardiac diseases. However, little is known about how the heart has evolved throughout the history of animals with backbones – a group that is collectively referred to as vertebrates. This is partly because the heart is made from soft muscle tissue, which does not fossilize as often as harder tissues such as bones.
Even though fossils of soft tissues are rare, paleontologists have already unearthed fossils of other soft organs such as the stomach and umbilical cord. These discoveries suggested that there was hope of finding fossil hearts, and now Maldanis, Carvalho et al. have indeed discovered fossil hearts in two specimens of an extinct species of bony fish called Rhacolepis buccalis. These fish were alive over 113 million years ago during the Cretaceous period, in an area that is now modern-day Brazil.
Like all known vertebrates, these R. buccalis fossils have valves between the heart and the major artery that carries blood out of the heart. Such valves are vital because they prevent pumped blood from flowing back into the heart. However, oddly, R. buccalis fossils show five of these valves, which is more than any advanced bony fish that is alive today. Comparing this with the situation in other fish species suggests that vertebrate hearts gradually evolved to become progressively simpler.
This discovery shows that it is possible to study heart evolution with fossils. Maldanis, Carvalho et al. hope that their findings will stimulate researchers from all over the world to examine the fossils of well-preserved animals in search of clues to help reconstruct the major steps in the evolution of the vertebrate heart.
DOI: http://dx.doi.org/10.7554/eLife.14698.002
... The above mentioned findings are in agreement with the identification of lymphocytes, macrophages and dendriticelike cells in the bulbus arteriosus of T. bernacchii by electron microscopy [18]. In addition, Icardo et al. [25] have also reported a thymuselike tissue in the conus arteriosus of the sturgeon (Acipenser naccarii) containing lymphocytes, macrophages and granulocytes, which may be involved in their immune responses. The source of these immune cells in these heart chambers is unknown and further studies are required to investigate their origin. ...
The bulbus arteriosus is the most anterior chamber of the teleost heart. The present study aimed to establish the presence, and to provide semi–quantitative information on the abundance, of several immune and cell–cycle proteins in the bulbus arteriosus of healthy Atlantic salmon (Salmo salar L.). Using immunohistochemistry, lymphocyte–like cells were identified in the bulbus arteriosus using antibodies to CD3ε and MHC class II β. Few PCNA positive cells were identified in post–smolt fish as compared to moderate levels of staining in fresh water fry. Interestingly no staining was evident in adult fish (1–3 kg), thus there was a loss of cells expressing cell–cycle regulatory proteins with ontogeny/progressive life–history stages. Eosinophilic granulocytes (EGCs) were identified in the bulbus arteriosus using TNFα and HIF1α antibodies. Anti–caspase 3 immune–reaction identified a strong endothelial cytoplasmic staining in the bulbus arteriosus. Taken together, the immunolocalization of immune–related molecules (CD3, MHC class II and TNFα), cell–cycle regulatory proteins (PCNA and HIF1α) and apoptosis markers (TUNEL, caspase 3) suggest that the bulbus arteriosus may have an immune component within its functional repertoire.
... The proximal part, which should be termed conus arteriosus, is formed by compact, well-vascularized myocardium and supports the outflow tract valves. It is homologous to the conus present in chondrosteans, elasmobranches, and teleosts (Icardo et al., 2002b;Schib et al., 2002;Guerrero et al., 2004). It should be stressed that the conus is always formed of compact myocardium. ...
We report a morphologic study of the heart ventricle and outflow tract of the African lungfish Protopterus dolloi. The ventricle is saccular and appears attached to the anterior pericardial wall by a thick tendon. An incomplete septum divides the ventricle into two chambers. Both the free ventricular wall and the incomplete ventricular septum are entirely trabeculated. Only a thin rim of myocardium separates the trabecular system from the subepicardial space. The outflow tract consists of proximal, middle, and distal portions, separated by two flexures, proximal and distal. The proximal outflow tract portion is endowed with a layer of compact, well-vascularized myocardium. This portion is homologous to the conus arteriosus observed in the heart of most vertebrates. The middle and distal outflow tract portions are arterial-like, thus being homologous to the bulbus arteriosus. However, the separation between the muscular and arterial portions of the outflow tract is not complete in the lungfish. A thin layer of myocardium covers the arterial tissue, and a thin layer of elastic tissue underlies the conus myocardium. Two unequal ridges composed of loose connective tissue, the spiral and bulbar folds, run the length of the outflow tract. They form an incomplete division of the outflow tract, but fuse at the distal end. The two folds are covered by endocardium and contain collagen, elastin, and fibroblast-like cells. They appear to be homologous to the dextro-dorsal and sinistro-ventral ridges observed during the development of the avian and mammalian heart. Two to three rows of vestigial arterial-like valves appear in the dorsal and ventral aspects of the conus. These valves are unlikely to have a functional role. The possible functional significance of the “gubernaculum cordis,” the thick tendon extending between the anterior ventricular surface and the pericardium, is discussed. J. Morphol. © 2005 Wiley-Liss, Inc.
... The ventricles of active fish species have a morphologically distinct outer compact myocardium and an inner spongy myocardium. Although the relative proportion each layer contributes to total myocardial mass has been quantified in a number of species and described in great morphological detail (Santer et al., 1983; Tota et al., 1983; Icardo et al., 2002), there has been little comparison of their electrical properties. In the tunas (family Scombridae), the heart is relatively large and has a high proportion of compact myocardium (40–70%) that is morphologically distinct from the spongy myocardium (Agnisola & Tota, 1994). ...
Monophasic action potentials (MAPs) were recorded from the spongy and compact layers of the yellowfin tuna Thunnus albacares ventricle as stimulation frequency was increased. MAP duration decreased with increase in stimulation frequency in both the spongy and compact myocardial layers, but no significant difference in MAP duration was observed between the layers.
... However, whereas in the present study the existence of myofibroblasts has not been specifically addressed, the authors believe that in all cases presented the markers utilized are labeling primarily bona fide smooth muscle cells, because they comprise a limited population of cells at the myocardial-smooth muscle, arterial pole transition that are continuous with distal OFT cells known to possess a smooth muscle phenotype. For example, cells identified in the middle component of the OFT of some chondrichthyans generally constitute a relatively small subpopulation located at the myocardium-smooth muscle junction, whereas the myofibroblasts described in the aforementioned studies were in the context of tissue supporting the proximal valves (in the yellow spotted rayFHamlett et al. 1996) or in the ''conus valves and subendocardium'' (in the sturgeonFIcardo et al. 2002a), rather than in the ''conusaorta transition'' (Icardo et al. 2002b). Further, the myofibroblasts in previous studies were not identified by immunohistochemical techniques. ...
In chick and mouse embryogenesis, a population of cells described as the secondary heart field (SHF) adds both myocardium and smooth muscle to the developing cardiac outflow tract (OFT). Following this addition, at approximately HH stage 22 in chick embryos, for example, the SHF can be identified architecturally by an overlapping seam at the arterial pole, where beating myocardium forms a junction with the smooth muscle of the arterial system. Previously, using either immunohistochemistry or nitric oxide indicators such as diaminofluorescein 2-diacetate, we have shown that a similar overlapping architecture also exists in the arterial pole of zebrafish and some shark species. However, although recent work suggests that development of the zebrafish OFT may also proceed by addition of a SHF-like population of cells, the presence of a true SHF in zebrafish and in many other developmental biological models remains an open question. We performed a comprehensive morphological study of the OFT of a wide range of vertebrates. Our data suggest that all vertebrates possess three fundamental OFT components: a proximal myocardial component, a distal smooth muscle component, and a middle component that contains overlapping myocardium and smooth muscle surrounding and supporting the outflow valves. Because the middle OFT component of avians and mammals is derived from the SHF, our observations suggest that a SHF may be an evolutionarily conserved theme in vertebrate embryogenesis.
... At this point, it should be noted that, at stages 4-5 dph, the outflow tract is completed by the formation of a new segment, the intermediate (conus-aorta transition) segment (Icardo et al., 2002) or bulbus arteriosus (Guerrero et al., 2004), which is added to the cranial end of the heart, between the conus arteriosus and the ventral aorta. We could not find evidence for the progression of the epicardium into this segment (Fig. 5). ...
This article reports on the development of the epicardium in alevins of the sturgeon Acipenser naccarii, aged 4-25 days post-hatching (dph). Epicardial development starts at 4 dph with formation of the proepicardium (PE) that arises as a bilateral structure at the boundary between the sinus venosus and the duct of Cuvier. The PE later becomes a midline organ arising from the wall of the sinus venosus and ending at the junction between the liver, the sinus venosus and the transverse septum. This relative displacement appears related to venous reorganization at the caudal pole of the heart. The mode and time of epicardium formation is different in the various heart chambers. The conus epicardium develops through migration of a cohesive epithelium from the PE villi, and is completed through bleb-like aggregates detached from the PE. The ventricular epicardium develops a little later, and mostly through bleb-like aggregates. The bulbus epicardium appears to derive from the mesothelium located at the junction between the outflow tract and the pericardial cavity. Strikingly, formation of the epicardium of the atrium and the sinus venosus is a very late event occurring after the third month of development. Associated to the PE, a sino-ventricular ligament develops as a permanent connection. This ligament contains venous vessels that communicate the subepicardial coronary plexus and the sinus venosus, and carries part of the heart innervation. The development of the sturgeon epicardium shares many features with that of other vertebrate groups. This speaks in favour of conservative mechanisms across the evolutionary scale.
... These features are typical of fish and have been demonstrated in many species (Santer, 1985; Farrell & Jones, 1992; Icardo et al. 2005c), including the Australian lungfish (Chopin & Bennett, 1995). The present findings give further support to the idea that the myocardial structure is largely conservative (Santer, 1985; Icardo et al. 2002). The most curious feature observed here is the presence of large intracytoplasmic spaces devoid of organelles. ...
This paper reports on the structure and ultrastructure of the ventricular myocardium of the African lungfish Protopterus dolloi in freshwater (FW), in aestivation (AE), and after the AE period. The myocardium shows a conventional myofibrillar structure. All the myocytes contain large intracytoplasmic spaces occupied by a pale material that could contain glycosaminoglycans and/or glycogen, which may be used as food and water reservoirs. In FW, the myocytes in the trabeculae associated with the free ventricular wall show structural signs of low transcriptional and metabolic activity (heterochromatin, mitochondria of the dense type). These signs are partially reversed during the AE period (euchromatin, mitochondria with a light matrix), with a return to the FW appearance after arousal. The myocytes in the septum show, in FW conditions, nuclear polymorphism (heterochromatin, euchromatin), and two types (colliquative and coagulative) of necrosis. In AE, all the septal myocytes show euchromatin, and the number of necrotic cells increases greatly. Cell necrosis appears to be related to the septal architecture. After arousal, the septal myocytes exhibit a heterochromatin pattern, the number of necrotic cells decreases, cell debris accumulates under the endocardium, and phagocytosis takes place. Despite being a morphologic continuum, the trabeculae associated with the free ventricular wall appear to constitute a different compartment from that formed by the trabeculae in the ventricular septum. Paradoxically, AE appears to trigger an increase in transcriptional and synthetic myocardial activities, especially at the level of the ventricular septum. This activity may be involved in mechanisms of autocrine/paracrine regulation. Aestivation cannot be regarded as the result of a general depression of all cellular and organic activities. Rather, it is a much more complex state in which the interplay between upregulation and downregulation of diverse cell activities appears to play a fundamental role.
Rich fossil evidence suggests that many traits and functions related to terrestrial evolution were present long before the ancestor of lobe- and ray-finned fishes. Here, we present genome sequences of the bichir, paddlefish, bowfin, and alligator gar, covering all major early divergent lineages of ray-finned fishes. Our analyses show that these species exhibit many mosaic genomic features of lobe- and ray-finned fishes. In particular, many regulatory elements for limb development are present in these fishes, supporting the hypothesis that the relevant ancestral regulation networks emerged before the origin of tetrapods. Transcriptome analyses confirm the homology between the lung and swim bladder and reveal the presence of functional lung-related genes in early ray-finned fishes. Furthermore, we functionally validate the essential role of a jawed vertebrate highly conserved element for cardiovascular development. Our results imply the ancestors of jawed vertebrates already had the potential gene networks for cardio-respiratory systems supporting air breathing.
The evolution of the circulatory system from invertebrates to mammals has involved the passage from an open system to a closed in-parallel system via a closed in-series system, accompanying the increasing complexity and efficiency of life's biological functions. The archaic heart enables pulsatile motion waves of hemolymph in invertebrates, and the in-series circulation in fish occurs with only an endothelium, whereas mural smooth muscle cells appear later. The present review focuses on evolution of the circulatory system. In particular, we address how and why this evolution took place from a closed, flowing, longitudinal conductance at low pressure to a flowing, highly pressurized and bifurcating arterial compartment.The general teleonomy of the evolution of species is the differentiation of individual organ function, supported by specific fueling allowing and favoring partial metabolic autonomy. This was achieved via the establishment of an active contractile tone in resistance arteries, which permitted the regulation of blood supply to specific organ activities via its localized function-dependent inhibition. The resistance to viscous blood flow is the peripheral increase in frictional forces caused by the tonic change in arterial radius, which backscatter as systemic arterial blood pressure. Consequently, the arterial pressure gradient from blood to the adventitial interstitium generates the outward radial advective conductance of plasma solutes across the wall. This hemodynamic evolution was accompanied by important changes in arterial wall structure, supported by smooth muscle cell functional plasticity. These adaptive phenotypic shifts are due to epigenetic regulation, mainly related to mechanotransduction. These paradigms actively participate in cardio-arterial pathologies.
The cardiac outflow tract (OFT) in teleosts is composed of a proximal short conus arteriosus and a distal well-developed bulbus arteriosus located between the ventricle and ventral aorta. The role of these anatomical components includes structural connections, prevention of blood backflow and blood pressure control, which are related to their histological and histochemical compositions. A previous study in the heart of the Amazonian species Arapaima gigas reported an unusual OFT arrangement among teleosts that has been found only in members of Osteoglossiformes so far. Thus, considering the wide structural variability of the teleostean OFT, the present study focuses on identifying glycosaminoglycans types and describing the distribution of collagen, elastic and reticular fibers in the conus arteriosus, conal valves, and bulbus arteriosus of A. gigas. Hearts from A. gigas between 327 and 4040 g weight were used. Collagen fibers were concentrated in regions that were regularly exposed to stress, as elastic fibers showed a broad distribution in all anatomical segments. Several fibrous connections between the conal valve leaflets and the conus arteriosus were observed, possibly acting as the primary connection form. The functions of the connective fibers in the valve leaflets and the bulbus are supported by an extracellular matrix rich in non-sulfated glycosaminoglycans. The complex reticular fiber network in the compact myocardium of the conus and the smooth muscle of the bulbus wall suggests a relevant role in support contraction of both muscle types, and in attachment and mobility of the conal valve leaflets.
This chapter aims to explore the state of knowledge about the immune mechanisms in sturgeon with a focus on the Siberian sturgeon (Acipenser baerii), stress factors that can disrupt the immune system and the sources of stimulation. Studies conducted carried out for several decades on sturgeon suggest specificities of their immune system compared to other fish species: special organs (meningeal myeloid tissue, tissues surrounding the heart), particularity of cells and components of immunity (larger white blood cells, lack of myeloperoxidase in neutrophils that are classified as heterophils). Other features have also been shown, i.e. the slow development of organs of immunity, the rapid response to acute stress, but also the great capacity for recovery from stress, all of which give a particular character to the sturgeon in the family of farmed fishes. Stress factors that can influence the immune system of sturgeons have also been researched in the last decade, with strong certainties about the influence of temperature, oxygen levels, pathogens and the presence in water of chemical substances. More and more programs on the research of solutions to boost the immune system have been implemented in recent years, with proven stimulatory actions on immunity factors (vaccines, probiotics, prebiotics, symbiotics, certain vitamins polysaccharides, plants and their components) and more mixed results (proteins, amino acids and certain vitamins). However, it seems that one domain is much less explored: the correlation between the pathogen, the host immunity and its environment. Nevertheless, this correlation is essential in the choice of solutions, which can be proposed, in particular in the field of immunostimulation.
The outflow tract of the fish heart is the segment interposed between the ventricle and the ventral aorta. It holds the valves that prevent blood backflow from the gill vasculature to the ventricle. The anatomical composition, histological structure and evolutionary changes in the fish cardiac outflow tract have been under discussion for nearly two centuries and are still subject to debate. This paper offers a brief historical review of the main conceptions about the cardiac outflow tract components of chondrichthyans (cartilaginous fish) and actinopterygians (ray‐finned fish) which have been put forward since the beginning of the nineteenth century up to the current day. We focus on the evolutionary origin of the outflow tract components and the changes to which they have been subject in the major extant groups of chondrichthyans and actinopterygians. In addition, an attempt is made to infer the primitive anatomical design of the heart of the gnathostomes (jawed vertebrates). Finally, several areas of further investigation are suggested. Recent work on fish heart morphology has shown that the cardiac outflow tract of chondrichthyans does not consist exclusively of the myocardial conus arteriosus as classically thought. A conus arteriosus and a bulbus arteriosus, devoid of myocardium and mainly composed of elastin and smooth muscle, are usually present in cartilaginous and ray‐finned fish. This is consistent with the suggestion that both components coexisted from the onset of the gnathostome radiation. There is evidence that the conus arteriosus appeared in the agnathans. By contrast, the evolutionary origin of the bulbus is still unclear. It is almost certain that in all fish, both the conus and bulbus develop from the embryonic second heart field. We suggest herein that the primitive anatomical heart of the jawed vertebrates consisted of a sinus venosus containing the pacemaker tissue, an atrium possessing trabeculated myocardium, an atrioventricular region with compact myocardium which supported the atrioventricular valves, a ventricle composed of mixed myocardium, and an outflow tract consisting of a conus arteriosus, with compact myocardium in its wall and valves at its luminal side, and a non‐myocardial bulbus arteriosus that connected the conus with the ventral aorta. Chondrichthyans have retained this basic anatomical design of the heart. In actinopterygians, the heart has been subject to notable changes during evolution. Among them, the following two should be highlighted: (i) a decrease in size of the conus in combination with a remarkable development of the bulbus, especially in teleosts; and (ii) loss of the myocardial compact layer of the ventricle in many teleost species.
The outflow tract of the heart lies within the pericardial cavity and is the connecting vessel between the ventricle and ventral aorta in all jawed fishes. There is much diversity in the design of the outflow tract among fishes. All display one or even two clearly recognizable forms, a bulbus arteriosus with the wall highly modified for extreme elasticity and a conus arteriosus made up of myocardial muscle. A truncus arteriosus covered in cardiac epithelium, but lacking cardiac muscle in its walls, may occur in some fishes. There is a great amount of diversity in the specific designs, the shapes, and the materials that make up the outflow tract among fishes. For the bulbus, the anatomical form is tuned to maximize its function of providing a continuous flow of blood in the ventral aorta and beyond. The conus may play a minor role in smoothing blood flow but the presence of multiple valves in association with cardiac muscle suggests that the primary function of the conus is in stopping blood flow from the heart. The truncus only occurs in a few species and appears to help keep oxygenated and deoxygenated blood separated in lungfishes.
Sturgeons are primitive bony fishes and their hearts have structural features found in other primitive fishes. Sturgeons have a pericardioperitoneal canal (PPC), a one-way conduit into the peritoneum. A PPC also occurs in elasmobranchs (sharks and rays) and studies with that group demonstrate that pericardial pressure and pericardial fluid loss via the PPC affect stroke volume. A study of white sturgeon (Acipenser transmontanus) heart function was conducted to test for a comparable PPC and pericardial effects. White sturgeon-elasmobranch heart-function similarities include biphasic ventricular filling, a comparable operational pericardial pressure (−0.03 kPa), and a strongly negative pressure (−0.2 to −0.6 kPa) with complete pericardial fluid withdrawal. Differences include the white sturgeon's relatively smaller atrium and ventricle but a larger conus arteriosus. Although white sturgeon heart size is also smaller, its pericardial volume is disproportionately less (2.4 to 2.7 vs. 3.5 to 5.4 ml kg−1 in elasmobranchs), meaning it has less scope for increasing stroke volume upon PPC fluid release. These differences may reflect the phylogenetic progression from the less complex operation of the elasmobranch heart, which lacks sympathetic innervation and has a mechanically mediated (PPC) stroke volume, to the condition in the more derived bony fishes which have sympathetic and parasympathetic regulation of both stroke volume and heart rate.
It has been reported that in chondrichthyans the cardiac outflow tract is composed of the myocardial conus arteriosus, while in most teleosteans it consists of the nonmyocardial bulbus arteriosus. Classical studies already indicated that a conus and a bulbus coexist in several ancient actinopterygian and teleost groups. Recent work has shown that a cardiac outflow tract consisting of a conus and a bulbus is common to both cartilaginous and bony fishes. Nonetheless and despite their position at the base of the actinopterygian phylogenetic lineage, the anatomical arrangement of the cardiac outflow tract of the Polypteriformes remained uncertain. The present study of hearts from gray bichirs was intended to fill this gap. The cardiac outflow tract of the bichir consists of two main components, namely a very long conus arteriosus, furnished with valves, and a short, intrapericardial, arterial-like bulbus arteriosus, which differs from the ventral aorta because it is covered by epicardium, shows a slightly different spatial arrangement of the histological elements and is crossed by coronary arteries. Histomorphologically, the outflow tract consists of three longitudinal regions, distal, middle and proximal, an arrangement which has been suggested to be common to all vertebrates. The distal region corresponds to the bulbus, while the conus comprises the middle and proximal regions. The present findings reinforce the notion that the bulbus arteriosus of fish has played an essential role in vertebrate heart evolution as it is the precursor of the intrapericardial trunks of the aorta and pulmonary artery of birds and mammals.
This study was conducted to establish the efficient condition for stable derivation of heart-derived cell culture in Siberian sturgeon (Acipenser baerii). Three factors including isolation methods, cell densities in initial seeding, and basal media were evaluated for the derivation of heart-derived cell culture. As the results, enzymatic isolation was more efficient than mechanical isolation in both cell retrieval and further culture. Total 48 trials of culture employing low and middle cell densities of less than 5.5 × 10(4) cells/cm(2) in initial seeding did not induce cell survivals (0%, 0/48), but the trials in high cell density of more than 5.5 × 10(5) cells/cm(2) could induce cell survival and primary cell attachment on the plate (88.9%, 24 in 27 trials). When all initially attached cell populations were continuously cultured in two different media, only five cell populations that were enzymatically isolated and cultured under Leibovitz's L-15 medium could grow up to more than 40th subculture. Each cell population was stably cultured according to its own growth rate and all showed normal diploid DNA contents. Two morphologically different cell types that has an elongated shape or a round shape were identified in culture, which was subsequently identified that two cell types are considered as a fibroblast (an elongated shape) and a vascular endothelial cell (a round shape) on the basis of the results of gene and protein expression analysis. Additionally, the sufficient number of viable cells could be successfully retrieved after freezing and thawing from all five cell populations suggesting the feasibility of long-term cryopreservation of the cells. The data and cells obtained from this study will contribute to development of in vitro model for basic biological studies using sturgeon species.
The cardiovascular system is crucial by virtue of its role in transporting nutrients, respiratory gases, hormones, and waste products. This chapter focuses on circulatory form and function: the anatomy of the cardiovascular system, cardiac dynamics, and cardiovascular control. Studying circulatory control in any fish is particularly difficult because discrete circulations of specific organs are not easily accessible. Therefore, by necessity, most information on cardiovascular control in primitive fishes is limited largely to the control of cardiac output (Q), as well as control of blood flow through the gills, to air‐breathing organs, and the gastrointestinal tract. Unusual adaptations of primitive fishes that deviate from those piscine features common to elasmobranchs and teleosts are highlighted. The chapter starts with the most primitive fishes, the cyclostomes, and moves through the cardiovascular anatomy of the coelacanth to the cardiovascular anatomy and physiology of dipnoans, the forerunners to tetrapods. It then closes by covering the limited physiological information for Polypterids, gars, bowfins, and sturgeons. By comparing cardiovascular adaptations among these primitive fishes, this chapter examines the evolutionary roots and the evolutionary divergence of the piscine cardiovascular system.
A large number of congenital heart defects associated with mortality in humans are those that affect the cardiac outflow tract, and this provides a strong imperative to understand its development during embryogenesis. While there is wide phylogenetic variation in adult vertebrate heart morphology, recent work has demonstrated evolutionary conservation in the early processes of cardiogenesis, including that of the outflow tract. This, along with the utility and high reproductive potential of fish species such as Danio rerio, Oryzias latipes etc., suggests that fishes may provide ideal comparative biological models to facilitate a better understanding of this poorly understood region of the heart. In this review, the authors present the current understanding of both phylogeny and ontogeny of the cardiac outflow tract in fishes and examine how new molecular studies are informing the phylogenetic relationships and evolutionary trajectories that have been proposed. The authors also attempt to address some of the issues of nomenclature that confuse this area of research.
It has been generally assumed that the outflow tract of the chondrichthyan heart consists of the conus arteriosus, characterized by cardiac muscle in its walls. However, classical observations, neglected for many years, indicated that the distal component of the cardiac outflow tract of several elasmobranch species was composed of tissue resembling that of the ventral aorta. The present study was outlined to test the hypothesis that this intrapericardial, non-myocardial component might be homologous to the actinopterygian bulbus arteriosus. The material consisted of Atlantic catshark adults and embryos, which were examined by means of histochemical and immunohistochemical techniques for light and fluorescence microscopy. In this species, the distal component of the outflow tract differs histomorphologically from both the ventral aorta and the conus arteriosus; it is devoid of myocardium, is covered by epicardium and is crossed by the coronary arterial trunks. In the embryonic hearts examined, this distal component showed positive reactivity for 4,5-diaminofluorescein 2-diacetate (DAF-2DA), a fluorescent nitric oxide indicator. These findings, together with other observations in holocephals and several elasmobranch species, confirm that chondrichthyans possess a bulbus arteriosus interposed between the conus arteriosus and the ventral aorta. Therefore, the primitive heart of gnathostomates consists of five intrapericardial components, sinus venosus, atrium, ventricle, conus arteriosus and bulbus arteriosus, indicating that the bulbus arteriosus can no longer be regarded as an actinopterygian apomorphy. The DAF-2DA-positive reactivity of the chondrichthyan embryonic bulbus suggests that this structure is homologous to the base of the great arterial trunks of birds and mammals, which derives from the embryonic secondary heart field.
Myxobolus dogieli Bykhovskaya-Pavlovskaya & Bykhovski, 1940 is regarded as a site specific myxosporean, infecting the heart of cyprinid fish. During a survey of the myxosporean fauna of Lake Balaton fish, heart myxobolosis was found in the common bream, Abramis brama, with heavy infection of the ventricle and the bulbus arteriosus in some infected bream. Developing and mature plasmodia were mostly in the connective tissue of the subepicardium and subendocardium. Plasmodia developing in the subendocardium protruded into the lumen of the heart, while plasmodia developing in the subepicardium protruded over the epicardium forming large sausage-like outgrowths. Plasmodia with mature spores were found in the summer. The shape and size of the spores corresponded to those of the original description. Phylogenetic analysis based on the 18S rDNA sequence of M. dogieli showed that this species fit well in the genus Myxobolus. As no molecular data are available on spores from the type host, common carp, the species studied by us is temporarily designated as Myxobolus s.l. dogieli.
This paper reports on the presence of the conus arteriosus in the heart of the adult gilthead seabream, Sparus auratus (Perciformes, Teleostei). The junctional region between the single ventricle and the bulbus arteriosus has been studied by conventional light microscopy, and by scanning and transmission electron microscopy. In addition, fluorescent phalloidin and antibodies against the muscle myosin heavy chains, laminin and collagen type IV have been used. The conus arteriosus is a distinct muscular segment interposed between the ventricle and the bulbus arteriosus. It is clearly different from the bulbus arteriosus due to its myocardial nature. It can also be distinguished from the ventricular myocardium because: (1) it has a conus shape; (2) it is formed by compact, well-vascularized myocardium; (3) it is surrounded on its inner and outer faces by fibrous layers rich in collagen and elastin; (4) it constitutes the anatomical support of the so-termed conus valves; (5) it shows intense staining for laminin and type-IV collagen; and (6) the myocardial cells located close to the inner fibrous layer are helicoidally arranged. By contrast, the ventricular myocardium is highly trabecular, lacks a compacta, shows no vessels, and presents barely detectable amounts of laminin and collagen type IV. The presence of a distinct conus arteriosus in the heart of an evolutionary advanced teleost species indicates that the conus is not a vestigial segment from the evolutionary or embryological points of view. The characteristic spatial arrangement of the conus myocytes strongly suggests that the conus is implicated in the mechanical performance of the conus valves.
Sturgeons are primitive bony fishes and their hearts have structural features found in other primitive fishes. Sturgeons have a pericardioperitoneal canal (PPC), a one-way conduit into the peritoneum. A PPC also occurs in elasmobranchs (sharks and rays) and studies with that group demonstrate that pericardial pressure and pericardial fluid loss via the PPC affect stroke volume. A study of white sturgeon (Acipenser transmontanus) heart function was conducted to test for a comparable PPC and pericardial effects. White sturgeon-elasmobranch heart-function similarities include biphasic ventricular filling, a comparable operational pericardial pressure (-0.03 kPa), and a strongly negative pressure (-0.2 to -0.6 kPa) with complete pericardial fluid withdrawal. Differences include the white sturgeon's relatively smaller atrium and ventricle but a larger conus arteriosus. Although white sturgeon heart size is also smaller, its pericardial volume is disproportionately less (2.4 to 2.7 vs. 3.5 to 5.4 ml kg(-1) in elasmobranchs), meaning it has less scope for increasing stroke volume upon PPC fluid release. These differences may reflect the phylogenetic progression from the less complex operation of the elasmobranch heart, which lacks sympathetic innervation and has a mechanically mediated (PPC) stroke volume, to the condition in the more derived bony fishes which have sympathetic and parasympathetic regulation of both stroke volume and heart rate.
Acipenseriformes occupy a special place in the history of ideas concerning fish evolution, but in many respects, phylogenetic
studies of the group remain in their infancy. Even such basic questions as the monophyly of Acipenser (the largest genus) are unanswered. We define relationships based on comparative osteology, which allows us to incorporate
well-preserved fossils into analyses. Acipenseriformes has existed at least since the Lower Jurassic (approximately 200 MYBP),
and all fossil and recent taxa are from the Holarctic. Phylogenetic relationships among Paleozoic and Early Mesozoic actinopterygians
are problematic, but most workers agree that Acipenseriformes is monophyletic and derived from some component of ‘paleonisciform’
fishes. (‘Paleonisciformes’ is a grade of primitive non-neopterygian actinopterygians, sensu Gardiner 1993.) Taxa discussed
in comparison here are: †Cheirolepis, Polypterus, †Mimia. †Moythomasia, †Birgeria, †Saurichthys, Lepisosteus and Amia. We review generic diversity within the four nominal families of fossil and recent Acipenseriformes (†Chondrosteidae, †Peipiaosteidae,
Polyodontidae, and Acipenseridae), and provide a cladogram summarizing osteological characters for those four groups. Monophyly
of the two extant families is well-supported, but there are no comprehensive studies of all of the known species and specimens
of †Chondrosteidae and †Peipiaosteidae. As a result, sister-group relationships among †Chondrosteidae, †Peipiaosteidae, and
Acipenseroidei (= Polyodontidae + Acipenseridae)are unresolved. We discuss five features fundamental to the biology of acipenseriforms
that benefit from the availability of our new phylogenetic hypothesis: (1) specializations of jaws and operculum relevant
to jaw protrusion, feeding, and ram ventilation; (2) anadromy or potamodromy and demersal spawning; (3) paedomorphosis and
evolution of the group; (4) the biogeography of Asian and North American polyodontids and scaphirhynchines; and (5) the great
abundance of electroreceptive organs in the rostral and opercular regions. Finally, we summarize our nomenclatural recommendations.
The preparation of optically clear, thick sections of fragile embryonic tissues greatly aids the power of confocal scanning laser microscopy in imaging three-dimensional structures. We report here conditions for embedding, sectioning, and staining embryos in polyacrylamide gels for a variety of confocal imaging techniques. Infiltration of tissues in standard mixtures of 10-15% acrylamide monomer yields, upon polymerization, blocks that cut easily by vibratome between 50 and 1,000 microns. These conditions worked well for tissues previously stained or for staining gel sections with low molecular weight water-soluble fluorochromes (MW < 5 kD [e.g., propidium iodide, phalloidin]). For immunostaining of tissue after embedding and sectioning, the acrylamide concentration was reduced to 2-3% acrylamide to allow access of immunoglobulins to antigenic sites; such gels were supplemented with 1% agarose to facilitate sectioning and handling. Either method yielded abundant, optically clear, and easily handled sections for mounting and examination in water-miscible media.
This chapter discusses different aspects of the cardiac anatomy, morphology, and physiology of fish. The fish heart is a four-chambered organ contained within a pericardial sac. Together, the sinus venosus, atrium, ventricle, and either an elastic bulbus arteriosus, or a contractile conus arteriosus raise the potential and kinetic energy of the blood. The principal tissue component of the sinus wall is connective tissue with bounding inner endothelial and outer epicardial linings. The amount of cardiac muscle present in the sinus venosus varies considerably among species. The ventricle shows considerable species variability with respect to its relative mass, gross morphology, histology, and vascularity. The addition of inner fibers, either as a circular arrangement around the sac-like elasmobranch ventricle, or as coils around the vertices of the pyramidal teleost ventricle, is clearly a characteristic of fish that are more active and perhaps provides a mechanical advantage for developing higher blood pressures. The histological structure of the fish coronary artery is characterized by an external parenchyma surrounding a medial layer of vascular smooth muscle; an internal elastic lamina separates the media from the intima, which normally has a single layer of endothelial cells.
The sections in this article are:
Diversity of Vertebrate Cardiovascular Patterns
Vertebrate Origins and Driving Forces behind Cardiovascular Evolution
Cardiovascular Patterns in Vertebrates
Functional Properties of Vertebrate Hearts
Overview
Electrical Properties of Cardiac Cells
Excitation–Contraction Coupling
Mechanical Properties of Cardiac Muscle
Cardiac Output and Cardiac Performance
Coronary Circulations, Myocardial O 2 Consumption, and Myocardial O 2 Supply
Peripheral Circulation and Hemodynamics
Arterial Blood Pressure and Its Regulation
Blood Volume and Its Regulation
Cardiovascular Performance Under Special Conditions
Aerobic Exercise
Breath Holding and Diving
Reduced Metabolism
Digestive State
Responses to Gravity
Development of Cardiovascular Systems
Conclusions and Future Directions
Mechanistic Unknowns
Adaptive Unknowns
Integrative Unknowns
Developmental Unknowns
The liver of the adult cod (teleost, Gadus morhua macrocephalus) was observed with transmission and scanning electron microscopy. Hepatocytes of this animal are extremely large (about 50–70 m in diameter) and characterized by numerous large lipid droplets (5–15 m in diameter) showing fluorescence for vitamin A, though weaker than that of Ito cells. No Kupffer cells were recognized in the endothelial lining. Collagen fibrils are sparse in the perisinusoidal space, while Ito cells stretching their long cytoplasmic processes to the perisinusoidal as well as interparenchymatous spaces are frequent. There are a number of large desmosomes between the cytoplasmic processes, and all Ito cells seem to be interconnected by these junctions. The cytoplasm in the cell bodies and cell processes is occupied by bundles of intermediate filaments, while organelles are poorly developed. Small vesicles and caveolae are arranged along the plasma membrane. Scanning electron microscopy shows distinct three-dimensional networks consisting of Ito cells and their processes, which might be supporting elements of the liver tissue. We wish to emphasize the concept of this hepatoskeletal system.
The ultrastructure of atrial and ventricular myocardial cells from Acipenser stellatus is described. The cells of the atrium are more loosely connected than those of the ventricle. Cell contact is by simple intercalated discs and by desmosomes. The cells are flattened, with peripheral myofibrils and a central region of mitochondria and the nucleus. The sarcoplasmic reticulum consists of subsarcolemmal tubules, that frequently extend towards the central mitochondria. Dyads are small and positioned at any sarcomeric level. No T-tubules are present. Specific granules are restricted to the atrial cell, and are sometimes present within the SR tubules.
Proliferative lesions have been found in the coronary arteries of five specimens of dogfish shark (Scyliorhinus canicula). Three specimens lacked the internal elastic membrane and had a diffuse thickening of the intima obliterating most of the vascular lumen in several intramyocardial branches. Two specimens had intimal nodules in one of the main coronary conal trunks, where breaking and splitting of the internal elastic membrane and fibrosis of the tunica media were observed. These lesions appear similar to those described in salmonid fishes, but are less frequent. Although high concentrations of blood cholesterol and ApoB-containing lipoproteins have been related to the development of coronary lesions in these bony fishes, the dogfish sharks described in this paper showed low serum concentrations of both total cholesterol (0.33 to 1.64 mg per ml) and triglycerides (0.61 to 0.17 mg per ml).
After removal of connective tissues by the NaOH maceration method, adrenal gland stellate cells of monkeys, rats and rabbits were studied by scanning electron microscopy. The stellate cells were situated in the perivascular and interstitial spaces and showed an ovoid cell body with numerous round or flat processes. Through these processes they were in contact with other adjacent stellate cells and thus formed a continuous cellular net around capillaries and parenchymal cells. This net, which probably provides a cellular scaffolding for the gland, may also play additional roles such as capillary contraction and nutrition for adjacent parenchymal cells.
Lymphoid (lymphomyeloid) tissues in sturgeons (hybrid sturgeon, Huso huso X Acipenser ruthenus, and white Pacific sturgeon, A. transmontanus) were investigated by dissection, histology and transmission electron microscopy. The main lymphomyeloid tissues are the thymus, the spleen, the anterior part of the kidney, the meningeal myeloid tissue, the pericardial tissue and lymphoid masses of the intestine, especially in the spiral valve. The kidney is the main hemopoietic tissue. The meningeal tissue is bone marrow-like (myeloid), mainly granulopoietic, but it also contains lymphoid elements. The pericardial tissue is predominantly lymphoid. The pericardial tissue has a lymph node-like appearance. It seems to be the site of interaction between lymphocytes and vascular endothelium. The thymus contains cortex and medulla. The spleen, as in higher vertebrates, is differentiated into white and red pulp. The highly diversiform and well developed lymphoid tissues of sturgeons may serve as basis of efficient immune mechanisms.
An examination of cell contacts was made in the atrial and ventricular muscle of Teleost fish. The intercalated discs consist of two types of junction resembling fascia and macula adherens. Small focal areas of gap junctions were shown to be numerous away from the regions of intercalated disc between the myocardial cells.
The most important mechanical property of the artery wall is its non-linear elasticity. Over the last century, this has been well-documented in vessels in many animals, from humans to lobsters. Arteries must be distensible to provide capacitance and pulse-smoothing in the circulation, but they must also be stable to inflation over a range of pressure. These mechanical requirements are met by strain-dependent increases in the elastic modulus of the vascular wall, manifest by a J-shaped stress-strain curve, as typically exhibited by other soft biological tissues. All vertebrates and invertebrates with closed circulatory systems have arteries with this non-linear behaviour, but specific tissue properties vary to give correct function for the physiological pressure range of each species. In all cases, the non-linear elasticity is a product of the parallel arrangement of rubbery and stiff connective tissue elements in the artery wall, and differences in composition and tissue architecture can account for the observed variations in mechanical properties. This phenomenon is most pronounced in large whales, in which very high compliance in the aortic arch and exceptionally low compliance in the descending aorta occur, and is correlated with specific modifications in the arterial structure.
Sturgeons are bony fish that retain structural traits typical of the more primitive Chondrostei. From an evolutionary viewpoint, sturgeons are considered relic fish. However, they show remarkable ecological plasticity and are well adapted to contemporary environmental conditions. Although development of the cardiovascular system is critical for all organs and systems, and is affected by evolutionary changes, the structure of the sturgeon heart has been mostly overlooked. This is also true for the conus arteriosus, which, as in Chondrostei, is endowed with several rows of valves and a layer of contractile myocardium. This work reports on the structure of the valves, the endocardium, and the subendocardium of the conus arteriosus of the sturgeon (Acipenser naccarii) heart. It is part of a broader study that aims to cover the entire structure of the sturgeon heart. The conus arteriosus of 15 A. naccarii hearts, ranging in age from juveniles to sexually-differentiated adults, has been studied by conventional light, transmission (TEM), and scanning electron microscopy (SEM). In addition, maceration of the soft tissues with NaOH, and actin localization by fluorescent phalloidin has been used. The conus is a tubular chamber that arises from the right ventricular side and presents two constrictions at the conus-ventricle and conus-aorta junctions. The conus is endowed with three rows of valves: one distal and two proximal. The segment of the conus located between the distal and the two proximal rows is devoid of valvular structures. The distal row has four leaflets, while the two proximal rows show the greatest variation in leaflet number, size, and shape. All leaflets have collagenous chordae tendineae arising from the free border and from the parietal side of the leaflets. The endocardium is a flat endothelium which shows a thick, irregular basement membrane. The leaflet body is formed by a loose connective tissue which blends with the subendocardium. The subendocardium is a connective tissue consisting of myofibroblasts, collagen, and elastin. It is divided into two distinct areas: one proximal, which shows little elastin and poorly organized collagen; and one distal, which is rich in elastin, with cells and extracellular fibers organized into layers that are oriented in alternative circumferential and longitudinal directions. The present report is the first systematic analysis of the structure of the sturgeon conus. Descriptions of the conus valves should recognize the existence of three valve rows only. The variability in valve morphology, and the loose structure of the leaflet tissue make it unlikely that the valves play an effective role in preventing blood backflow. In this regard, the ventricle-conus constriction may act as a sphincter. The subendocardium is an elastic coat capable of actively sustaining the tissue deformation that accompanies the heart contractile cycle. Further comparative studies are needed to provide deeper insight into the structural changes that accompany phyletic diversification.
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