Corticosteroids: Friends or foes of teleost fish reproduction?

Abstract

Reproduction in vertebrates is controlled by the Hypothalamus-Pituitary-Gonad axis and the main hormone actions have been extensively described. Still, despite the scattered information in fish, accumulating evidence strongly indicates that corticosteroids play essential roles in reproductive mechanisms. An integrative approach is important for understanding these implications. Animal husbandry and physiological studies at molecular to organismal levels have revealed that these corticosteroids are regulators of fish reproductive processes. But their involvements appear strongly contrasted. Indeed, for both sexes, corticosteroids present either deleterious or positive effects on fish reproduction. In this review, the authors will attempt to gather and clarify the available information about these physiological involvements. The authors will also suggest future ways to prospect corticosteroid roles in fish reproduction.

Full text

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Review
Corticosteroids: Friends or foes of teleost fish reproduction?
S. Milla⁎, N. Wang, S.N.M. Mandiki, P. Kestemont
University of Namur (FUNDP), Unit of Research in Organismal Biology (URBO), Rue de Bruxelles 61, B-5000, Namur, Belgium
a b s t r a c ta r t i c l e i n f o
Article history:
Received 18 December 2008
Received in revised form 20 February 2009
Accepted 20 February 2009
Available online 27 February 2009
Keywords:
Corticosteroids
Cortisol
Corticosteroid receptors
Fish
Physiology
Reproduction
Sex-steroids
Stress
Reproduction in vertebrates is controlled by the Hypothalamus–Pituitary–Gonad axis and the main hormone
actions have been extensively described. Still, despite the scattered information in fish, accumulating
evidence strongly indicates that corticosteroids play essential roles in reproductive mechanisms. An
integrative approach is important for understanding these implications. Animal husbandry and physiological
studies at molecular to organismal levels have revealed that these corticosteroids are regulators of fish
reproductive processes. But their involvements appear strongly contrasted. Indeed, for both sexes,
corticosteroids present either deleterious or positive effects on fish reproduction. In this review, the authors
will attempt to gather and clarify the available information about these physiological involvements. The
authors will also suggest future ways to prospect corticosteroid roles in fish reproduction.
© 2009 Elsevier Inc. All rights reserved.
Contents
1.
2.
3.
4.
5.
6.
7.
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The main corticosteroid roles in mammal reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The corticosteroids in fish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Changes in plasma corticosteroids during fish reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The role of corticosteroids in the reproduction of female fish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The role of corticosteroids in the reproduction of male fish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Future directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction
In teleost fish, corticosteroids are involved in a wide range of
physiological regulations in the fields of stress, immune and
inflammatory responses, energetic metabolism and osmoregulation.
Although these roles are well documented (Wendelaar Bonga, 1997;
Mommsen et al.,1999), corticosteroid functions in reproduction have
received limited attention. Most of the studies related to reproductive
endocrinology focused on the classical endocrine actors of the brain–
pituitary–gonad axis such as GnRH, gonadotrophins or gonadal sex-
steroids. Until now, data about corticosteroidsare quite scattered. Still,
increasing clues suggest the relevance to focus on them in order to
refine our knowledge about the endocrine control of fish reproduc-
tion. Reports about the inhibitory and stimulatory effects of
corticosteroids and stress on reproduction are sometimes controver-
sial. The aim of this review is to clarify these equivocal effects. Based
onrecent studies in thearea, we examinedtheir possible physiological
roles in regulating reproduction. Initially we provide a brief overview
of the major involvements of corticosteroids in mammals, before
outlining the available information in fish and finally discussing how
to prospect new research strategies for the exploration of corticoster-
oid functions in the future.
2. The main corticosteroid roles in mammal reproduction
Corticosteroidsaresteroidhormonesproducedfromcholesterolby
the adrenal cortex mainly.
Comparative Biochemistry and Physiology, Part A 153 (2009) 242–251
⁎ Corresponding author. Tel.: +32 81 72 43 71; fax: +32 81 72 43 62.
E-mail address: Sylvain.Milla@fundp.ac.be (S. Milla).
1095-6433/$ – see front matter © 2009 Elsevier Inc. All rights reserved.
doi:10.1016/j.cbpa.2009.02.027
Contents lists available at ScienceDirect
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journal homepage: www.elsevier.com/locate/cbpa

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They are classically divided into two groups: the glucocorticoids
and the mineralocorticoids. Many cell types contain receptors that
bind glucocorticoids allowing these hormones (mainly cortisol in
non-rodents and corticosterone in rodents) to control numerous
biological processes such as carbohydrate, lipid and protein metabo-
lism. They also play major anti-inflammatory roles and regulate the
immune response. Mineralocorticoids, mainly represented by aldos-
terone, regulate hydromineral balance, mainly by promoting sodium
retention in the kidney and acting via mineralocorticoid receptor. But
there are evidences that mineralocorticoids are involved in other
biological processes such as the regulations of cardio-vascular system
(Struthers, 1995; Duprez, 2007; Fejes-Toth and Naray-Fejes-Toth,
2007) or structural proteins (Gekle et al., 2007). Furthermore, the
presence of corticosteroid receptors in reproductive tissues including
ovary and testis leads to the consideration that corticosteroids can
exert positive or inhibitory effects on reproductive functions.
Regarding females, there is a general consensus to say that
glucocorticoids can exert inhibitory effect on the whole Hypothalamus–
Pituitary–Gonad axis including ovarian steroidogenesis (Michael et al.,
1993). Therefore, it is hypothesized that they are detrimental to
reproduction. However, in a recent review, Tilbrook et al. (2000)
underscored that in vivo disruptive effects of glucocorticoids in non-
rodent mammals are not systematic. Actually, according to Brann
and Mahesh (1991), corticosteroids may also play a positive role in the
regulationoffollicledevelopment,asacutelyelevatedlevelsmayincrease
both FSH and LH releases, contrary to chronic corticosteroid exposure.
There is also no general agreement about the roles of corticoster-
oids and especially glucocorticoids in the regulation of oocyte
maturation. In human and other mammals, there is a preovulatory
increase of follicular cortisol content during the luteinizing hormone
surge leading to ovulation, while levels are reduced during the rest of
the menstrual cycle (Harlowet al.,1997; Andersen, 2002; Acosta et al.,
2005). It has been suggested that cortisol exerts a positive action
during ovulation in human (Fateh et al., 1989; Jimena et al., 1992;
Andersen, 2002) but it had no effect on oocyte maturation in mouse
(Andersen, 2003) and was suggested to be inhibitory in pig, albeit at
pharmacological doses (Yang et al., 1999). In human, the increase of
intrafollicular cortisol would result from an increase of cortisone
uptake from the circulating fluid. There, this latterwould be converted
into cortisol by 11β-HSD enzyme that would switch from type-2 into
type-1 near the ovulation period (Lewicka et al., 2003). Nevertheless,
it is not clear yet whether the peri-ovulatory increase of follicular
cortisol is a cause or a consequence of human oocyte maturation
(Michael, 2003). According to Hillier (2001), it might be involved in
Table 1
Plasma concentrations of corticosteroids in the plasma of some immature and mature, male and female teleosts (ng/mL).
SteroidsSpeciesReproductive status Female
22–38
MaleReference Method
11-dehydrocorticosterone
11-deoxycortisol
11-deoxycortisol
11-deoxycortisol
Chalcalburnus tarichi
Pleuronectes americanus
Pleuronectes platessa
Hoplostethus atlanticus
Mature
Mature
Mature
Mature
Immature
Mature
Immature
Mature
Immature
Mature
Mature
Immature
Mature
Mature
Immature
Mature
Mature
Immature
Mature
Immature
Mature
Immature
Mature
Immature
Mature
Immature
Mature
Immature
Mature
Immature
Mature
Immature
Mature
Mature
Immature
Mature
Mature
Immature
Mature
Mature
Immature
Mature
Mature
Mature
Mature
Immature
Unal et al. (2006)
Campbell et al. (1976)
Scott and Canario (1990)
Pankhurst and Conroy (1988)
HPLC
Double isotope derivative assay
HPLC+RIA
RIA
0.6–1.9
32
2–5
1–3
1–9
1–5
18.1
0–3
b0.1
2–4
11-deoxycortisol
Perca fluviatilis
Noaksson et al. (2005)HRGC/HRMS
11-deoxycortisol
11-deoxycortisol
11-deoxycorticosterone
11-deoxycorticosterone
Oncorhynchus mykiss
Oncorhynchus mykiss
Cyprinus carpio
Oncorhynchus mykiss
4.8
Campbell et al. (1980)
Doyon et al. (2006)
Kime and Dolben (1985)
Milla et al. (2008)
Double isotope derivative assay
RIA
RIA
RIA
1
0.02–0.1
3.1
11-deoxycorticosterone
11-deoxycorticosterone
Oncorhynchus mykiss
Tilapia aurea
2
22.2
0.6
0.5
12–15
1–3
60
8
40
5–15
30–80
10–15
Campbell et al. (1980)
Katz and Eckstein (1974)
Double isotope derivative assay
Chromatography+isotope derivative assay
11-deoxycorticosterone
Cortisol
Pleuronectes americanus
Pleuronectes platessa
1
11–14
1–4
Campbell et al. (1976)
Wingfield and Grimm (1977)
Double isotope derivative assay
RIA
Cortisol
Dicentrarchus labrax
Rocha and Reis-Henriques (1999)RIA
Cortisol
Platichthys flesus
Lu et al. (2007)RIA
Cortisol
Fundulus heteroclitus
Bradford and Taylor (1987)RIA
Cortisol
Oncorhynchus mykiss
20–25
2–4
Hou et al. (2001)RIA
Cortisol
Oncorhynchus mykiss
70
10–20
Koldkjær et al. (2004) RIA
Cortisol
Oncorhynchus tshawytscha
397
76
300–350
40–70
52
Barry et al. (2001)ELISA
Cortisol
Oncorhynchus masou
300–400
30–90
Westring et al. (2008)TR-FIA
Cortisol
Cortisol
Oncorhynchus nerka
Oncorhynchus nerka
Woodhead (1975)
Carruth et al. (2000)
Chromatography
RIA
457
259
140–200
15–50
1–7
71–120
125–140
10–30
Cortisol
Cortisol
Oncorhynchus nerka
Salmo trutta
50–85
5–20
1–7
57–89
Kubokawa et al. (1999)
Pickering and Christie (1981)
RIA
RIA
Cortisol
Cortisol
Catostomus commersoni
Piaractus mesopotamicus
Scott et al. (1984)
Gazola et al. (1996)
RIA
RIA
Corticosterone
Cortisone
Cortisone
Cortisone
Oncorhynchus nerka
Oncorhynchus nerka
Salmo salar
Pleuronectes americanus
73
61
50
12.7
1.2–1.4
Woodhead (1975)
Woodhead (1975)
Idler et al. (1964)
Campbell et al. (1976)
Chromatography
Chromatography
Chromatography
Double isotope derivative assay
70–160
7.9
0.8–1.8
243
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the anti-inflammatory response to tissue injuries caused by ovulation.
To date, the role of cortisol during peri-ovulatory period has not been
entirely elucidated.
Prenatal maternal stress has been found to have long-lasting
effects on the behavioural and physiological development of the
offspring. In the case of human, this maternal stress is often associated
to an increase of cortisol in the women plasma and in the foetus
(De Weerth and Buitelaar, 2005). During gestation, cortisol levels
normally gradually increase in the serum and amniotic fluid of
pregnant woman (Challis et al., 1983; Sarkar et al., 2007). High
expression of 11β-HSD type-2, which oxidizes cortisol into cortisone,
has been measured in both foetus and placenta from mid-gestation to
parturition (Seckl and Chapman, 1997). Both low expression of
this enzyme or high cortisol/dexamethasone levels in the pregnant
female/woman were associated to decrease placental weight and
lower bodyweight at birth (Seckl and Chapman, 1997; reviewed
by Michael and Papageorghiou, 2008). It was hypothesized that
11β-HSD2 may protect the foetus from deleterious actions of active
cortisol/corticosterone (Sun et al., 1999). These deleterious effects
may happen during early, mid- or late pregnancy and impact foetus
but also further child/young animal development (e.g. hyperten-
sion, post-natal learning capacities, cognitive function and response
to stress) (Michael and Papageorghiou, 2008). Regarding the role of
mineralocorticoids, aldosterone production increases during preg-
nancy in order to allow the water retention needed for volume
expansion (Escher and Mohaupt, 2007).
In males, glucocorticoids and especially cortisol or corticosterone
seemtohaveaninhibitoryeffectallalongthespermatogenesisprocess
(Weber et al., 2000). These glucocorticoids inhibit testosterone
production within the Leydig cells via a pathway mediated by the
glucocorticoid receptor (Ge et al., 2005a). In addition, glucocorticoids
may induce spermatogonia and spermatocyte apoptosis and decrease
sperm yield (Gao et al., 2003; Wagner and Claus, 2004). However,
according to Wagner and Claus (2004), it is not clear whether these
effectsarepartofanormalregulativestepordetrimentaltotheanimal.
The activity of 11β-hydroxysteroid dehydrogenase (11βHSD2) within
Leydig/Sertoli cells would protectthetestis fromthe adverse effects of
cortisol or corticosterone by converting these hormones into inactive
cortisone or 11-dihydrocorticosterone, respectively (Nacharaju et al.,
1997; Ge et al., 2005a).
Contrary to glucocorticoids, mineralocorticoids seem to exert some
positive actions in male reproduction. Mineralocorticoid receptor
was found to be expressed in Leydig and Sertoli cells, as well as in
spermatozoa (Geet al.,2005b;Fiore et al., 2006).Themineralocorticoid
hormone aldosterone might be involved in the regulation of spermatic
fluid osmolarity and in spermatozoa motility (Fiore et al., 2006). In
addition it appears that it would also stimulate testosterone production
within the Leydig cells (Ge et al., 2005b).
3. The corticosteroids in fish
Corticosteroids are mainly synthesized in the interrenal tissue in
teleost fish. This tissue which is embedded inside the anterior part of
the kidney is homologous to mammalian adrenal cortex. Contrary to
mammals, the interrenal tissue doesnot forma compactglandandthe
anatomical distinction between cortical and medullary zonations is
lacking. Indeed, the postcardinal veins and their branch are sur-
rounded by close clusters of chromaffin cells (medullary homologue)
and steroidogenic cells (cortical homologue) (Wendelaar Bonga,
1997). Whereas the corticosteroid biosynthesis pathways differ
between fish and mammals (Prunet et al., 2006), there are not great
differencesbetweenthecorticosteroidpattern.Themaindivergenceis
the absence of the mineralocorticoid aldosterone in fish (Gilmour,
2005). Otherwise, to our knowledge, 18-hydroxycorticosterone and
1α-dehydroxycorticosterone have not been detected in the teleost
plasma yet. In conformity with the findings in other vertebrates,
themaincorticosteroidsisolatedfromfishbloodarecortisol,cortisone,
11-deoxycortisol and corticosterone. But, their concentrations depend
on the species, sex and reproductive status (Table 1).
Female and male gonads may have alsothe capacity to produce the
main corticosteroids (cortisol, 11-deoxycortisol, corticosterone and
11-deoxycorticosterone).First,inthefishspeciesinvestigated,theyown
all the enzymes responsible for their synthesis even if 11-β hydroxylase
geneexpressionwasnotabundantintheovary(Figs.1and2:Kobayashi
et al., 1998; Kusakabe et al., 2002; Kazeto et al., 2003; Li et al., 2003;
Socorro et al., 2007; Zhou et al., 2007). Second,11-deoxycorticosteroids
(11-deoxycortisol and 11-deoxycorticosterone) were shown to be
important products of ovarian and/or testicular steroidogenesis
(Colombo et al., 1973, 1978; Tesone and Charreau, 1980; Kime et al.,
1992). Third, the presence of cortisol and 11-deoxycortisol in ovary,
sperm and seminal fluid supports that gonadal corticosteroidogenesis
(Canario and Scott,1990; Scott et al.,1991a,b).
To manage their physiological actions, corticosteroids bind to
nuclear receptors which act as ligand-dependent transcription factors.
The relative ability of corticosteroids to evoke the transcriptional
activities of corticosteroid receptors is of paramount importance to
estimate their capacity to exert physiological actions. In rainbow trout
Oncorhynchus mykiss, cortisol and, to a lesser extent,11-deoxycortisol
Fig.1. Schema of the probable pathways of corticosteroid biosynthesis in female teleost. Solid black arrows show that the enzyme catalysing the steroid metabolism is active in the
gonad; the grey arrows indicate that the enzyme required for that step is expressed in the gonad but its activity needs to be confirmed.
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and corticosterone appeared to transactivate in vitro the two gluco-
corticoid receptors (Bury et al., 2003). Interestingly, the two
glucocorticoid receptors but also both GR2 isoforms in the
cichlid Haplochromis burtoni are differentially sensitive to cortisol
(Greenwood et al., 2003; Bury et al., 2003). The situation is far from
clear for the mineralocorticoid receptor for which both cortisol and
11-deoxycorticosterone (DOC) arelikelyto act as physiological ligands
(Sturm et al., 2005). In H. burtoni, the mineralocorticoid receptor
sensitivity was similar to the mammalian one, in being more sensitive
to both cortisol and aldosterone than the glucocorticoid receptors
(Greenwood et al., 2003). Corticosteroid receptors gene expression
(gluco- and mineralocorticoid receptors) has been found in the male/
female gonads. In rainbow trout, the transcripts were detected in the
ovary (Sturm et al., 2005; Milla et al., 2006). Both corticosteroid
receptors were also identified in the testis of trout and other species
(Colombe et al., 2000; Park et al., 2007; Filby and Tyler, 2007; Milla
et al., 2008). In the testis, mineralocorticoid receptor is strategically
located along thereproductiveaxis andthusis in a position toregulate
reproductive function (Milla et al., 2008). Finally, the presence of
factors known to interfere with the corticosteroid actions in mammals
supports the implication of corticosteroids in fish reproduction. In this
regard, 11β-hydroxysteroid dehydrogenase which prevents illicit
activation of the mineralocorticoid receptor in mammals by cataboliz-
ing cortisol (Farman and Rafestin-Oblin, 2001), is expressed in the
ovary and testis, particularly from mid-gametogenesis to the final
stages of maturation, and displays some activities at least in the testis
(Kusakabe et al., 2003; Ozaki et al., 2006; Milla et al., 2006). Overall,
production, receptivity and metabolic capacity of corticosteroids in
the gonads are thus a first argument to suppose some potential
implications in teleost reproduction.
4. Changes in plasma corticosteroids during fish reproduction
Whereas the seasonal changes of the classical sex-steroid
concentrations (androgens, estrogens…) during a reproductive cycle
have been extensively investigated so far, data about the variations of
plasma corticosteroid concentrations are limited. Still, as a determi-
nant indicatorof corticosteroid roles in fish reproduction, their plasma
levels vary greatly throughout the reproductive cycle. In both sexes,
some fish species exhibit a broad increase in plasma cortisol levels
during the pre-spawning or spawning period (Wingfield and Grimm,
1977; Pickering and Christie, 1981; Kusakabe et al., 2003; Noaksson
et al., 2005; Westring et al., 2008) even if this result was not observed
in some species like black bream Acanthopagrus butcheri (Haddy and
Pankhurst, 1999). As plasma cortisol levels in mature fish have been
measured at high concentrations in several fish species, often more
elevated than in immature fish (Table 1), one can hypothesize that a
plasma cortisol up-regulation at the breeding season may concern
numerous species. More precisely, in rainbow trout, brown trout
Salmo trutta, goldfish Carassius auratus and common carp Cyprinus
carpio a surge in plasma cortisol was measured at the time of
ovulation but such a transient increase needs to be investigated in
other fish species (Cook et al.,1980; Pickering and Christie,1981; Bry,
1985; Kime andDolben,1985). Fewstudies have compared the plasma
cortisol profiles during the reproductive cycle for both sexes but it
seems, at least in salmonids, that the elevation starts earlier in males
than in females but that the amplitude is higher in females (Pickering
and Christie, 1981; Table 1).
This difference in the plasma cortisol profile might also been
species-specific as illustrated by the broad levels measured plasma of
the salmon species (Table 1). This salmon example also illustrates the
specificity of diadromic fish for which the preparation to mating
coincides with numerous physiological changes including in the
osmoregulatory and metabolic processes. In the wild, salmons
experience a large and sustained rise in plasma cortisol levels during
the pre-spawning and/or spawning period (Carruth et al., 2000;
Westringet al., 2008). Progressive hyperplasia of the interrenal tissues
coincidently with the increase of corticosteroid concentrations was
described in salmons during their anadromous spawning migrations
(Robertson and Wexler, 1959; Hane and Robertson, 1959). In fish,
cortisol release is involved in metabolic function and osmoregulation
(Mommsen et al., 1999). In particular, several studies support that
cortisol would be implicated in the salmonid adaptation to freshwater
by stimulating the hyperosmoregulatory mechanisms (Mc Cormick,
2001; Kiilerich et al., 2007). Also, the gonadal maturation is
accompanied with changes in metabolic parameters known to be
driven by cortisol, such as enhanced liver amino acid catabolism and
gluconeogenesis leading to glucose increase for coping with stress
during migration (Kubokawa et al.,1999). It meansthatthis prolonged
hypersecretion of cortisol may be due to reproduction but also to face
with the dramatic changes in their physiology.
Except for cortisol, the plasma levels of most of the corticosteroids
appearloworundetectableoutsidethereproductiveseason.However,
at the mating period, substantial plasmatic amounts were measured
for most of them in some fish species without any clear sex influence
(Table 1). In salmonids and other fish families, corticosteroids like
Fig. 2. Schema of the probable pathways of corticosteroid biosynthesis in male teleost. Solid black arrows show that the enzyme catalysing the steroid metabolism is active in the
gonad; the grey arrows indicate that the enzyme required for that step is expressed in the gonad but its activity needs to be confirmed. Unfilled arrow indicates lack of clear
information.
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11-deoxycorticosterone (DOC) and 11-deoxycortisol were reported
to be highly up-regulated in the plasma at the time of reproduction, in
both sexes. For instance, a 38-fold increase of plasma DOC levels was
measured in Tilapia aurea during ovulation (Katz and Eckstein, 1974).
However, these elevations (11-deoxycorticosterone, 11-deoxycortisol)
were not observed in all species, highlighting probable species
differences which remain to be established (Table 1). In any case,
when this peak occurs, its synchronicity with blood MIS (Maturation-
Inducing Steroid) increase is in agreement with a role of these
corticosteroids in the final stages of reproduction (Noaksson et al.,
2005; Milla et al., 2008).
5. The role of corticosteroids in the reproduction of female fish
In fish, stress causes adverse effects on female reproductive
performances. Depending on the period and the intensity of stressor
application, it may cause follicular atresia, advance or delay oocyte
maturation and ovulation or affect egg size, fertilization success,
spawning behaviour and progeny quality (Clearwater and Pankhurst,
1997; Coward et al.,1998; Schreck et al., 2001; Okumura et al., 2002).
Deleterious effects of stress on vitellogenesis have been extensively
studied in salmonids. For example, female brook trout Salvelinus
fontinalis facing with acid stress had lower vitellogenin levels (Roy
et al., 1990). In rainbow trout, females subjected to repeated acute
stress during oogenesis produced smaller eggs, in accordance with
vitellogenesis disruption (Campbell et al.,1992). These effects may be
mediated by cortisol, which has been shown to interfere with
vitellogenesis (Fig. 3). In Arctic charr Salvelinus alpinus, cortisol
affected the vitellogenin production controlled by estrogen (Berg
et al., 2004) and also directly inhibited the production of estrogen in
rainbow trout and tilapia Oreochromis mossambicus (Carragher and
Sumpter, 1990; Foo and Lam, 1993; Reddy et al., 1999; Pankhurst and
Van Der Kraak, 2000). These results could be explained by some
types of interactions between the glucocorticoid receptor and the
estrogen receptor (ER). In vivo cortisol treatment caused a drop of
cytosolic E2-binding sites in the liver and a reduction in plasma
vitellogenin quantity in trout (Carragher et al., 1989; Pottinger and
Pickering,1990). Glucocorticoid receptor activation prevents estradiol
frompositivelyregulatingtheERexpression(Lethimonieretal.,2000).
Furthermore, the glucocorticoid and estrogen receptor distributions
overlap in the trout brain and pituitary indicating further potential
interferences between the glucocorticoids and estrogen pathways
(Teitsma et al., 1999). The information about the effects of the other
corticosteroidsisveryscarce.Theirweakabilitytotransactivateinvitro
the glucocorticoid receptors (Bury et al., 2003) does not support such
effect on vitellogenesis depletion.
The reported effects of corticosteroids on GnRH and gonadotropins
productions are also consistent with the interference of corticoster-
oids with the Hypothalamus–Pituitary–Gonad (HPG) axis. The wide-
spread expression of rainbow trout glucocorticoid receptor in the
brain and pituitary shows that neurons and pituitary cells, involved in
the control of the reproductive axis, are probably targets for
glucocorticoids (Teitsma et al., 1999). In immature fish, cortisol
treatments induced elevation of pituitary LH in eel Anguilla anguilla
and rainbow trout. These results evoke a positive function of
glucocorticoids in the first sexual maturation (Crim et al., 1981;
Dufour et al.,1983; Huang et al.,1999). By contrast, in maturing brown
trout, the pituitary and plasma gonadotropins were depleted by
cortisol treatment (Carragher et al., 1989). In female fish, androgens
are suspected to be implicated in the regulations of final stages
synchronization and GnRH/gonadotropins secretion (Redding and
Patino,1993; Nagahama et al.,1994). The effects of cortisol or stress on
plasma androgens suppression (Carragher et al.,1989; Campbell et al.,
1994; Cleary and Pankhurst, 2000) also support that corticosteroids
indirectly disrupt the HPG axis. Collectively, these works suggest that
corticosteroids not only affect estrogens but also probably disrupt
GnRH and gonadotropin actions. Therefore, it appears that corticos-
teroids may exert inhibitory effects on vitellogenesis. Nevertheless, as
these works mainly focused on salmonids, it would be interesting to
investigate that scheme in other fish families.
Conversely, sex-steroids regulate corticosteroid productions further
supporting their reciprocal interaction along the reproductive cycle.
Estradiol suppressed in vitro cortisol production in interrenals collected
at spawning time in chinook salmon Oncorhynchus tshawytscha,
and collected from immature kokanee salmon Oncorhynchus nerka
(McQuillan et al., 2003), which confirms the reciprocal antagonism
between both steroids even if that result was not observed in immature
rainbow trout (Barry et al., 1997; McQuillan et al., 2003). By contrast,
in vivo, estrogens were reported to promote cortisol production in
immature trout (Pottinger et al., 1996). It is conceivable that this
Fig. 3. Schema of the main corticosteroid implications in female teleost reproduction. MIS: Maturation-Inducing Steroid; 11-DC: 11-deoxycortisol; DOC: 11-deoxycorticosterone.
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discrepancy is related to cortisol target within the Hypothalamus–
Pituitary–Interrenal (HPI) axis. Also in rainbow trout, 17α-20ß-
dihydroxyprogesterone which is the MIS was effective to stimulate
cortisolproductionintheinterrenalofimmaturefish(Barryetal.,1997).
Therefore, sex-steroids may act on tissue implicated in cortisol
production to modulate the whole physiological corticosteroid
response.
The transient rise of plasma corticosteroids around ovulation is in
agreement with their biological effects on peri-ovulatory mechan-
isms. In the 70s, numerous investigators attempted to identify
the major steroids involved in oocyte maturation and ovulation.
When identifying 17α-20ß-dihydroxyprogesterone and 17α-20ß-
trihydroxyprogesterone as the MIS, corticosteroids were also inten-
sively tested for their ability to participate in the final stages of oocyte
maturation and ovulation. Treatments with LH stimulated in vitro
follicular and interrenal synthesis of DOC and cortisol (Sundararaj and
Goswami, 1969; Colombo et al., 1973) in agreement with peri-
ovulatory role of both steroids. In vivo hCG injection in catfish Heterop-
neustes fossilis induced oocyte maturation coincidently with plasma
cortisolandcorticosteroneincrease(MishraandJoy,2006).Cortisolwas
demonstrated to be quite effective in inducing oocyte meiotic matura-
tion in several fish species (see for review Goetz, 1983). In vitro tests
alsoshowedthatDOCbutalso11-deoxycortisolandcorticosteronewere
able to trigger oocyte maturation in numerous freshwater species even
if high doseswere sometimes necessarytoobserve these effects (Goetz,
1983 for review; Rahman et al., 2001). In a recent work, the
corticosteroid 11-deoxycortisol was even more potent than MIS to
induce oocyte maturation (Unal et al., 2008). Moreover, when testing
somesteroid combinations, a synergy in the maturational responsewas
demonstrated between corticosteroids and MIS. For example, in vitro
treatmentswithcortisolincreasedthesensitivityofoocytestotheMISin
rainbow trout (Jalabert and Fostier, 1984). In the view of these
interactions,ithasbeenhypothesizedthatthebindingofcorticosteroids
to plasma proteins during oocyte maturation would free unbound
MIS and facilitates its action (Goetz, 1983). Thus, although the MIS are
today identified, these in vitro results support that corticosteroids
might be directly and/or indirectly involved in final oocyte maturation
control. But, the plasma concentrations of corticosteroids, not markedly
higher than MIS levels during this period, raise the question about
the extent of this physiological significance. Associated with oocyte
maturation,oocytehydrationisabiologicalprocessshowntobeinduced
invitrobycortisolinrainbowtrout(Milla etal.,2006).Injectionsofhigh
doses of cortisol promoted ovarian tissue hydration associated with an
increase of sodium content in the ayu (Plecoglossus altivelis) (Hirose
et al., 1974). But, except DOC, no other corticosteroids have ever been
tested.Finally,ovulationwasinducedbytreatmentswithcorticosteroids
(cortisol,11-deoxycortisolandDOC)indiversefishspecies(Hiroseetal.,
1974; Goetz and Theofan, 1979; Haider and Rao, 1994; Small, 2004).
So, corticosteroids may be actors of the endocrine control of the final
stages of reproduction, in several fish species.
Untilnow,themajorityofthestudieswerededicatedtounderstand
the oviparous model. Still, in the ovoviviparous model guppy Poecilia
reticulata, the cortisol level dropped during fertilization followed by a
rise during gestation and then a strong decline at the periparturition
period (Venkatesh et al., 1990). Associated with the cortisol effect on
gestation prolongation, it is also hypothesized that cortisol is also
important in maintaining gestation (Venkatesh et al.,1991).
To sum-up (Fig. 3), the current state of knowledge is in favour of
harmful effects of cortisol during vitellogenesis by interference with
ovarian sex-steroids signaling. However, cortisol might participate in
the fish pubertystimulation byenhancing pituitarygonadotropins at the
onsetofoogenesis.Moreover,themaincorticosteroids,includingcortisol,
seem to be involved in the regulation of peri-ovulatory mechanisms
despite a disruption of the HPG axis in the case of high cortisol levels.
6. The role of corticosteroids in the reproduction of male fish
Similarly to females, corticosteroids influence male reproduction
(Fig. 4). But, the available investigations mainly focused on cortisol
involvement. Low plasma cortisol levels were observed during sperma-
togenesisinmalefish(PickeringandChristie,1981;Houetal.,2001).This
could be a physiological adaptation to protect the testes against the
adverse effects of cortisol (Pottinger et al.,1995). Indeed, this steroid has
numerous deleterious effects on male reproduction. When facing
stressful situations or cortisol treatment, a delay in the testicular
development was observed, marked by smaller gonads, retardation in
spermatogenesis and lower sperm quality (Campbell et al., 1992;
Consten et al., 2001). In common carp, the administration of RU486, a
potent glucocorticoid receptor antagonist, prevented the decrease of
gonad growth and the delay of the spermatogenesis time-course,
Fig. 4. Schema of the main corticosteroid implications in male teleost reproduction. MIS: Maturation-Inducing Steroid; DOC: 11-deoxycorticosterone.
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showing that these cortisol impacts are managed via the glucocorticoid
receptor pathway (Goos and Consten,2002). Nevertheless, using a testis
incubationtestintheJapaneseeel(Anguillajaponica),Ozakietal.(2006)
pointedoutthatcortisoldirectlyenhancesDNAreplicationandmitosisin
spermatogonia when added at moderate doses (0.1–100 ng/mL).
However, excess of cortisol (100 ng/mL) inhibited the 11-ketotestoster-
one effect on spermatogonia proliferation. In accordance with a positive
regulatory effect of cortisol on spermatogenesis, administration of that
steroid in immature knifefish Notopterus notopterus increased their
gonado-somatic index (GSI) and activated spermatogenesis (Shankar
and Kulkarni, 2000). These discrepancies between studies could be
related to dose and/or species differences and underline the complexity
to draw strong conclusions about the adverse cortisol effects on fish
spermatogenesis.
Cortisol also inhibits the sex-steroid secretion at least during the
spermatogenesis process. After stressor applications or cortisol
administration during spermatogenesis, the plasma androgen levels
were lower in treated fish than in controls (Pickering et al., 1987;
Carragher et al., 1989; Pottinger, 1999; Goos and Consten, 2002;
Consten et al., 2002; Lister et al., 2008). These observations suggest
that cortisol effect on spermatogenesis retardation is partly caused by
inhibition of androgen productions (Consten et al., 2002; Pickering
et al., 1987; Scott and Baynes, 1982). But, we cannot preclude any
inhibitory effects on the brain–pituitary–gonad axis by depressing
brain GnRH content, pituitary FSH and LH and plasma gonadotropin
levels as shown in common carp (Consten et al., 2001).
During the spermiation period, cortisol has also negative effects on
some reproductive parameters such as testis growth for example
(Carragher et al., 1989). Domesticated male striped bass Morone
saxatilis selected as high cortisol stress responders tended to begin
their spermiation earlier and exhibited a longer spermiation period
(Castranova et al., 2005). In rainbow trout, a direct negative cortisol
effect on the MIS testicular production was reported (Milla et al.,
2008). As this latter is probably implicated in spermiation induction
and/or amplification, this supports the hypothesis that cortisol affects
the achievement of the last steps of male reproduction.
Even if fewpositiveeffects on spermatogenesis havebeen reported
(see above), the great majority of the studies indicate that cortisol is
an inhibitory hormone of male reproductive physiology over the
wholereproductive cycle (Fig. 4). There arealso someevidences of the
relationship between the corticosteroid plasma levels and the mating
behaviour. In Neolamprologus pulcher, the cortisol level was found to
be higher in dominant fish compared to subordinates (Bender et al.,
2006). Conversely, in H. burtoni, dominant territorial males which
predominantly access to females exhibit lower cortisol levels
associated with higher phenotypical ability to reproduction (Fox
et al.,1997). Similarly, subordinate Arctic charr showed more elevated
plasma concentrations of cortisol (Elofsson et al., 2000). But, it is
difficult to know whether this plasma level is the result or the cause of
the social position. Indeed, this plasma cortisol level may serve to
provide a quick burst of energy to face with male intraspecies
confrontations, either to fight or escape. Otherwise, this differential
plasma corticosteroid level might reflect an ability to communicate
during mating. Corticosteroids are released in the water, notably at
the reproduction period (Lower et al., 2004; Ellis et al., 2005) and the
sensitivity of olfactory epithelium, even weak, to sulphated corticos-
teroids in mature fish (cortisol and 11-deoxycortisol) (Sorensen et al.,
1995) prevent us from ruling out their implication as reproductive
pheromonal factors.
Interestingly, a plasmacortisol increase is also observed inparental
male bluegill sunfish Lepomis macrochirus after hatching at the time of
parental care start suggesting some cortisol physiological implications
in such behaviour (Magee et al., 2006). Based on the relations
between corticosteroid levels and the parental care in birds (Wing-
field and Ramenofsky, 1999), it would be interesting to test this
relationship in the rare fish species providing this behaviour.
7. Future directions
Several reasons may explain the complexity to assess the
corticosteroid implication in fish reproduction. First, the physiological
state of the animal is highly modified during mating (final stages of
oogenesis, reproduction). On the one hand, as cortisol is the main
stress hormone in fish, its plasma variations correlate with the
occurrence of various stressful situations. Some works also suggest
that corticosteroid receptors are also regulated after different stresses
(Terova et al., 2007; Stolte et al., 2008). Mating period is accompanied
with huge modifications in the behaviour, leading to a higher
sensitivity to stress. Focusing on cortisol during reproduction must
be thus undertaken with higher caution regarding the potential
interaction between plasma cortisol levels and mating activities. In
consequence, blood sampling should be rapidly carried out to avoid
any cortisol contamination due to a stressful physiological state.
Regarding the other corticosteroids, if the effects of stress on their
blood plasma release remain undetermined, one should pay the same
attention to them. On the other hand, reproduction often corresponds
to a fasting period, or is at least accompanied with a decrease of
feeding. As the plasma glucocorticoid levels are linked to the fish
nutritional status, it may therefore be difficult to distinguish between
the glucocorticoid fluctuations linked to reproductive physiological
state and those linked to the alteration of the energetic metabolism.
More generally, as suggested earlier in the salmon example, all the
potential interactionsbetweenthecorticotropic axisandreproduction
in fish should be appropriately considered.
Second, potential relationships between corticosteroids and sex-
steroids should be taken into consideration. In the classically
described corticosteroid transduction pathway, corticosteroids acti-
vate corticosteroid receptors to exert their physiological actions.
However, some corticosteroids are able to bind to gonadal progesto-
gen receptors. In Arctic charr, 11-deoxycorticosterone (DOC), the
putative teleost mineralocorticoid, was shown to bind to an ovarian
progestogen membrane receptor. But, in that study, no other
corticosteroids were tested (Berg et al., 2005). Moreover, DOC and/or
to a lesser extent 11-deoxycortisol bound substantially a nuclear
and membrane progestogen receptor in spotted sea trout Cynoscion
nebulosus.But,cortisoldoesnotseemtobeanagonistof thesereceptors
(Pinter and Thomas,1995; Zhu et al., 2003). In male Japanese eel, DOC
also displayed a high affinity for a nuclear 17α-20ß-dihydroxyproges-
terone (MIS) receptor in the testis and once more, cortisol did not bind
or activate it (Todo et al., 2000). That steroid binding profile was also
observed in sperm membrane progestogen receptor in Atlantic croaker
Micropogonias undulatus (Thomas et al., 2005). These results lead us
to hypothesize that some corticosteroids including DOC interfere with
MIS in its transduction pathway, in accordance with the reported
physiological interactions between these steroids and MIS. Conse-
quently, future studies on corticosteroid involvements should take into
account potential corticosteroid effects via the progestogen receptor
signaling. Besides, the reported effect of DOC on sperm fluidity
also suggests that this steroid would play some roles in fish reproduc-
tion, either acting on the mineralocorticoid receptor or via progestogen
receptors (Milla et al., 2008).
More generally, in the view of the described corticosteroid effects
(oocyte maturation, ovulation, spermatogonia proliferation, sperm
hydration), it is observed that corticosteroids either act in combina-
tion with sex-steroids or exert effects previously demonstrated to be
managed by other hormones. By analogy with their roles in
maintaining energetic, immune and ionic homeostasis in fish biology,
we can speculate that, contrary to sex-steroids which trigger
reproductive process, corticosteroids are involved in their adjustment.
Their potential link with the sex-steroids should be integrated in
the future experimental designs.
Third, as shown by Ozaki et al. (2006), the effects of cortisol
on spermatogonia proliferation may be dose-dependent, either
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Page 8

stimulatory at low physiological concentrations or inhibitory at high
concentrations.Thus, studiesoncorticosteroid effectsonreproduction
should be undertaken with a broad range of steroid concentrations to
make sure to grasp all possibilities. In that way, more attention should
be paid to 11β-hydroxysteroid dehydrogenase action, which converts
cortisol into cortisone in the case of elevated levels in the plasma, as
shown in mammals. The study of its activitycould inform us about the
need for the fish to reestablish the cortisol levels at stimulatory
concentrations in the case of too high plasma concentrations. Besides,
the other conditions of cortisol application (doses, timing and
duration of application…) should also be accurately appreciated to
better clarify the potential cortisol actions.
Finally, if the use of the mammalian model to explain the teleost
physiology is often unsuitable, such comparison may allow exploring
new area in fish. For several decades, the apparent absence of
aldosterone and mineralocorticoid receptor in fish conferred them a
corticosteroid scheme very different from mammals. Still, the
discovery of mineralocorticoid receptor and its putative ligand DOC
reopened the debate about the similarities between fish and
mammals. If we attempt to highlight some similarities between
those models, we note that the implications of corticosteroids in
female reproduction (oogenesis inhibition, peri-ovulatory process
stimulation, gonadotropins regulation) are similar. In male fish,
whereas the adverse effects of glucocorticoids on reproduction are
close to mammals, their controversial effects on spermatogonia
proliferation between the fish and mammalian models may be related
to dose effects. Regarding mineralocorticoids, the effects of aldoster-
one on sperm quality including spermatozoa concentration or
androgen production may be sufficient arguments to hypothesize
such roles of mineralocorticoids in teleost reproduction. More
generally, the recent findings about the roles of cortisol and
aldosterone during reproduction in mammals may open new
perspectives regarding the endocrine control of reproduction in
other vertebrates like fish.
In summary, teleost gonads are able to produce and respond to
corticosteroids stimulation. Cortisol, the main corticosteroid, mainly
displays direct deleterious effects on female and male gametogenesis
(Figs. 3 and 4). But, the observations of these negative impacts might
be related to elevated plasma concentrations. The relationship
between corticosteroids and sex-steroids shows that corticosteroids
also indirectly interferewiththe HPGaxis in bothsexes (Figs. 3 and4).
By contrast, they exhibit a spectrum of direct positive activities during
the final stages, particularly in females (oocyte maturation, ovula-
tion). The changes in corticosteroid levels noted at this moment may
be related to these multiple functions. Taken together, the available
information strongly indicates that corticosteroid hormones may
highly participate to the modulation of the reproductive endocrine
control.
Acknowledgement
S.M. was supported by the Belgian National Funds for Scientific
Research (FNRS), contract 2. 4570. 06.
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