Peritrophic membrane role in enhancing digestive efficiency. Theoretical and experimental models

Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, C.P. 26077, 05513-970, São Paulo, Brazil.
Journal of Insect Physiology (Impact Factor: 2.47). 09/2008; 54(10-11):1413-22. DOI: 10.1016/j.jinsphys.2008.08.002
Source: PubMed


The peritrophic membrane (PM) is an anatomical structure surrounding the food bolus in most insects. Rejecting the idea that PM has evolved from coating mucus to play the same protective role as it, novel functions were proposed and experimentally tested. The theoretical principles underlying the digestive enzyme recycling mechanism were described and used to develop an algorithm to calculate enzyme distributions along the midgut and to infer secretory and absorptive sites. The activity of a Spodoptera frugiperda microvillar aminopeptidase decreases by 50% if placed in the presence of midgut contents. S. frugiperda trypsin preparations placed into dialysis bags in stirred and unstirred media have activities of 210 and 160%, respectively, over the activities of samples in a test tube. The ectoperitrophic fluid (EF) present in the midgut caeca of Rhynchosciara americana may be collected. If the enzymes restricted to this fluid are assayed in the presence of PM contents (PMC) their activities decrease by at least 58%. The lack of PM caused by calcofluor feeding impairs growth due to an increase in the metabolic cost associated with the conversion of food into body mass. This probably results from an increase in digestive enzyme excretion and useless homeostatic attempt to reestablish destroyed midgut gradients. The experimental models support the view that PM enhances digestive efficiency by: (a) prevention of non-specific binding of undigested material onto cell surface; (b) prevention of excretion by allowing enzyme recycling powered by an ectoperitrophic counterflux of fluid; (c) removal from inside PM of the oligomeric molecules that may inhibit the enzymes involved in initial digestion; (d) restriction of oligomer hydrolases to ectoperitrophic space (ECS) to avoid probable partial inhibition by non-dispersed undigested food. Finally, PM functions are discussed regarding insects feeding on any diet.

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    • "The insect midgut epithelium lacks a mucus coating, the peritrophic membrane is considered to be the analogous to that of the mucus that lubricates the mucosa, protecting against food abrasion and microorganisms (Caldeira et al. 2007, Bolognesi et al. 2008). However, the peritrophic membrane also has specific functions depending on the fact that it compartmentalizes the midgut lumen into an endoperitrophic space (inside peritrophic membrane) and an ectoperitrophic space (space between peritrophic membrane and midgut epithelium ; Bolognesi et al. 2008). This functions to 1) prevent non-specific food binding onto the cell surface; (2) restrict oligomer hydrolases to the ectoperitrophic space; and (3) prevent enzyme excretion by allowing enzyme recycling (Caldeira et al. 2007). "
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    ABSTRACT: The analyses of the insect species found on decomposing remains may provide useful information for the estimation of the minimum time elapsed since death and other parameters, such as causes and circumstances of death. The majority of research has focused on the early colonizing species, typically blowflies, while research concerning late colonizing insects is currently sparse. Dermestid beetles of the genus Dermestes L. (Coleoptera: Dermestidae) are one of the predominant insect species associated with decomposing remains during dry decay and skeletal stages of decomposition. In some dry environments, Dermestes species are likely to be the only necrophagous insects feeding on the decomposing remains. Furthermore, Dermestes species (immature and adults), their remains (cast skins and fecal material), and their artifacts (pupal chambers) are frequently found associated with ancient remains (e.g., mummies, fossils). Dermestes species have a worldwide distribution and are considered important in decomposition processes, forensic investigations, and economically as a known pest of stored products. Despite their recognized forensic importance, there is limited data documenting the ecology, biology, and the growth rates of the forensically relevant species. The aim of this review is to provide a comprehensive synopsis on the available literature concerning Dermestes species associated with forensic cases. In particular, aspects of colonization behavior, growth rates for forensic taxa and potential best practice guidelines for forensic casework encompassing late colonizing Dermestes species are discussed. © The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For Permissions, please email:
    Journal of Medical Entomology 07/2015; 52(5):1-15. DOI:10.1093/jme/tjv106 · 1.95 Impact Factor
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    • "The PM proteins are released into the midgut lumen by microapocrine secretion (Bolognesi et al., 2001; Serrão et al., 2008; Terra and Ferreira, 2012; Fialho et al., 2013; Toprak et al., 2013). The PM is produced along the midgut epithelium, which is classified as type I PM, or it is produced in the restricted region of the anterior midgut (the cardia), which is classified as type II PM (Wigglesworth, 1930, 1972; Richards and Richards, 1977; King, 1988; Peters, 1992; Tellam et al., 2000; Marques-Silva et al., 2005). "
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    ABSTRACT: The midgut is a region of the digestive tract of bees with the lumen lined by a peritrophic membrane that is composed of chitin and proteins (peritrophins). The origin of the peritrophins in the midgut of adult bees is unknown. This study used an anti-peritrophin 55-kDa antibody to immunolocalize the sites of the peritrophic membrane synthesis in nine species of adult bees’ representatives of different families and sociability levels. In all studied species the peritrophin-55 is produced by digestive cells in the entire midgut in the rough endoplasmic reticulum following transference to Golgi apparatus and released by secretory vesicles, which fuses with the plasma membrane and microvilli. Thus, in the representatives of different groups of bees, the PM is of type I.
    Micron 10/2014; 68. DOI:10.1016/j.micron.2014.09.009 · 1.99 Impact Factor
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    • "The compartmentalization of digestion and the existence of the endo-ectoperitrophic circulation increase digestive efficiency by allowing the removal of oligomers obtained in the initial digestion and reutilizing digestive enzymes to obtain new oligomers, which are hydrolyzed within the ectoperitrophic space. Since the enzymes produced are not evacuated, but recycled, there is considerable energy saving (Bolognesi et al., 2008). Further research, however, is needed to better understand how the endo-ectoperitrophic circulation mechanism affects the shrimp's digestive physiology and how this could be manipulated in order to maximize the output performance of shrimps in captivity. "
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    ABSTRACT: The effect of dietary protein concentration on the spatial distribution of digestive proteinases in the shrimp Litopenaeus vannamei indicates the existence of endo-ectoperitrophic enzyme circulation in this species. Samples recovered from the midgut gland tissues, stomach contents, three different portions of the midgut and feces were used for quantitative and qualitative analysis of the composition and distribution of the digestive proteinases. Animals were divided into three different groups: (1) animals (controls) fed a commercial 35% protein diet, (2) animals fed a commercial diet supplemented with ovalbumin to a final protein concentration of 60%; (3) animals fed a 80% protein diet. Quantitative determinations using different substrates and zymograms showed that increasing protein concentration in the diet alters the distribution of proteinases along the digestive tract. Composition of proteinases in the midgut gland, stomach contents, midgut sections and feces were similar, but not identical. Chymotrypsin and trypsin paralogues were identified in all enzyme sources in a concentration gradient along the midgut in the control shrimp, the expected distribution supporting the existence of a recycling mechanism. The occurrence of a peritrophic membrane in other Decapoda suggests that endo-ectoperitrophic circulation of digestive enzymes and nutrients may also occur in other crustaceans and also extends beyond the Insecta.
    Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology 05/2014; 172(1). DOI:10.1016/j.cbpb.2014.04.010 · 1.55 Impact Factor
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