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Introduction – Overview of the the water, either in specialized nests guarded by one or
Brain–Hypophyseal–Gonadal Axis both parents or in the open water. Several teleost fish such
as the guppy (Poecilia reticulata) are viviparous.
Environmental signals, in conjunction with social cues, are
conveyed by sensory signals to various brain centers cul
minating in the hypothalamus. In the absence of hypophyseal Oogenesis
portal system, hypothalamic nerve fibers branch throughout
the adenohypophysis to regulate the synthesis and release of Oogonial Proliferation and Meiosis
the gonadotropic hormones, follicle-stimulating hormone Oogonia proliferate mitotically under the stimulation of
(FSH) and luteinizing hormone (LH). Dopamine secreted E2 (Figure 2). Meiotic division commences in a subpo
by the hypothalamus may inhibit LH release. FSH and LH, pulation of the oogonia that can be visualized by the
in turn, bind to their respective receptors in the gonads presence of synaptonemal complexes (a hallmark feature
(FSH-R and LH-R, respectively). of homologous chromosomal synapses). Another marker
The gonads respond by secretion of sex steroid hor of meiosis is Spo11, a protein involved in the creation of
mones; estradiol 17� (E2) in females that promotes double-stranded breaks in the DNA at early stages of
oogonial proliferation and vitellogenesis, and progesto meiotic recombination. Addition of DHP to the medium
gens such as 17�,20� dihydroxy-4-pregnen-3-one (DHP) of cultured ovarian fragments results in increased abun
that promotes initiation of germ cell meiosis and follicular dance of synaptonemal complexes and increased
maturation and ovulation (Figure 1(a)). In males, these expression of Spo11, indicating that DHP acts to induce
are androgens, mainly 11 ketotestosterone (11-KT), that meiosis in the oogonia of teleost ovary (Figure 2).
regulate spermatogenesis and spermiogenesis, as well as
DHP that initiates the meiotic division of spermatogonia
Oocyte Growth
and controls the spermatozoa maturation and spermia
tion. DHP in its free or conjugated forms serve as As the oocyte starts growing during fish puberty, it is still
pheromones as well. Generally, fertilization occurs in arrested at the prophase of the first meiotic division
1500
Encyclopedia of Fish Physiology: From Genome to Environment, 2011, Vol. 2, 1500-1508, DOI: 10.1016/B978-0-1237-4553-8.00058-7
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Hormonal Control of Reproduction and Growth | Endocrine Regulation of Fish Reproduction 1501
Hypothalamus Hypothalamus
DA GnRH DA GnRH
FSH LH
Pituitary Pituitary
LH
FSH MIS (DHP or 20β-S)
MPF (cdc2 kinase and cyclin B)
Estradiol-17β
MIS
Liver MPF
Vitellogenins
Choriogenins Central GV Migrating Peripheral Breakdown Ovulation
Figure 1 (a) An overview of the endocrine chain, brain–pituitary–gonadal axis (BPG axis) in model female fish during the vitellogenic
phase. (b) An overview of the BPG axis during final oocyte maturation and ovulation.
Meiosis I
Estradiol 17β DHP Meiotic maturation
1n DNA
Metaphase II Fertilization 1n 2n
2n Fertilized egg
Short arrest
Figure 2 Stages of fish oogenesis and their endocrine regulation.
(Figure 2). At this phase, it sequesters yolk precursors Mutual Regulation of the Follicle Cells and
(vitellogenins) and chorionic proteins (choriogenins) mainly the Oocyte
produced by the liver under estrogenic stimulation. The yolk
accumulates in the oocyte which increases in diameter. FSH The granulosa cells surrounding the oocyte and the
regulates both the secretion of estradiol and the incorporation oocyte itself maintain a mutual communication system
of vitellogenins into the oocytes (Figure 1(a)). by which molecules of the epithelial growth factor
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1502 Hormonal Control of Reproduction and Growth | Endocrine Regulation of Fish Reproduction
(EGF) family secreted by the oocyte affect the adja that stimulates spermatogonial mitotic proliferation
cent granulosa cells. Activin, a major mediator of fish (Figure 3).
pituitary gonadotropins, is released by the somatic Experimental increase or decrease in the FSH and
cells of the follicle and affects the oocyte through FSH-Rs expression in the testis of African catfish
activin receptors present in this germ cell. (Clarias gariepinus) resulted in respective changes in
Sertoli cell proliferation and testicular growth, suggesting
that in fish, as in mammals, FSH in cooperation with
Oocyte Maturation
androgens is probably the regulator of Sertoli cell
The post-vitellogenic oocyte may remain quiescent for number.
several months but following environmental, social, or Gonadotropic stimulation in the Japanese eel
pheromonal cues, it begins the process of final matura (Anguilla japonica) shifts a subpopulation of spermato
tion, that is, the resumption of meiosis (Figure 2). This gonial germ cells from a renewal line to a proliferation
will commence with a surge in gonadotropin-releasing line ensuing by meiosis. Gonadotropins (mainly FSH)
hormone (GnRH), with or without a decrease in dopa elicit a surge in the secretion of 11-KT from Leydig
minergic inhibition, followed by a rise in circulating LH. cells to stimulate in Sertoli cells the production
Upon binding of LH to its receptors on the granulosa of several mediators such as activin B, insulin-like
cells, the ovarian follicle starts the process of maturation, growth factor I (IGF-I), and anti-Müllerian hormone
beginning with the production of the maturation- (AMH). The action of 11-KT on this spermatogonial
inducing steroid (maturation-inducing steroid (MIS) line is positively mediated by activin B and IGF-I,
such as DHP or 17�-20�,21 Trihydroxy-4-pregnen-3 and negatively by AMH (Figure 3). However, the
one (20�-S)). Binding of the MIS to its receptors on the initiation of meiotic division leading to the formation
oocyte plasma membrane is followed by activation of the of spermatids is induced by DHP, which is produced
maturation-promoting factor (MPF), a complex consist by the germ cells themselves, exerting their effect on
ing of existing cdc2-kinase and newly synthesized cyclin the germ cells in a paracrine or autocrine manner
B. (Figure 1(b)). The process of oocyte maturation is (Figure 3). The need for DHP to initiate meiosis
reflected morphologically by the migration of the germ was demonstrated by 11-KT stimulating DNA replica
inal vesicle (GV) toward the animal pole (GV migration) tion and meiosis in organ culture of eel testes and
and the disintegration of its membrane, a stage known as anti-DHP serum blocking this effect. Moreover, addi
GV breakdown (GVBD) (Figures 1(b) and 2). The tion of DHP resulted in the expression of two
chromosomes then condense, a spindle is formed, and meiosis-specific markers DMC1 and Spo11, and the
the first polar body is extruded which marks the end of appearance of synaptonemal complexes in testicular
the first meiotic division (Figure 2). At this stage the sections.
oocytes absorb water and inflate; this is especially pro Immature spermatozoa undergo sperm maturation,
nounced in marine fish with pelagic eggs, the pressure which is also regulated by DHP acting directly on sper
within the follicle increases, the follicular wall is rup matozoa to activate carbonic anhydrase. This enzymatic
tured, and the oocyte is released (ovulated) into the activation is followed by an increase in the seminal plasma
ovarian lumen or to the coelomic cavity. The meiosis pH, which augments intrasperm cAMP levels to enable
is arrested again at metaphase II. Completion of the their motility (Figure 3).
second meiotic division and extrusion of the second
polar body are further delayed and will proceed only if
the egg is fertilized (Figure 2). Gonadal Steroids
Formation of Gonadal Steroids in Fish
Fish gonadal steroids are mainly synthesized through
Spermatogenesis pathways similar to those in other vertebrates with a few
exceptions (Figure 4). Testosterone in fish testis is hydro
Endocrine Regulation of Spermatogenesis
xylated at carbon 11 by P450-11� and, after oxidation by
Spermatogenesis consists of several successive processes, 11�- hydroxysteroid dehydrogenase (11�-HSD), is con
each regulated by a distinct set of hormones. Mitotic verted into 11-KT that is the potent androgen of teleost
divisions of spermatogonia that lead to germ cell renewal fish. In certain fish, testosterone hydroxylation occurs in
are regulated by E2 secreted by the interstitial Leydig an extra-testicular tissue, the liver. The conversion of 17
cells under gonadotropic stimulation, mainly FSH. Upon hydroxyprogesterone by 20�-HSD produces DHP that
binding of E2 to their receptors in the Sertoli cells, the acts as the MIS in many fishes. However, in a number of
latter secrete the spermatogonial stem-cell renewal factor marine perciform fish, the MIS is 17�,20�,21-trihydroxy
(possibly gonadal soma-derived growth factor (GSDF)) 4-pregnen-3-one (21��S). This steroid too derives from
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Hormonal Control of Reproduction and Growth | Endocrine Regulation of Fish Reproduction 1503
FSH, LH
Germ cells
Leydig cell
E2 11-KT
DHP
Sertoli cell
Spermatogonial
stem-cell Increase in
Activin B IGF-I
renewal factor AMH seminal plasma pH
DMC1 Carbonic
Spo11 anhydrase
3β–HSD
17α-Hydroxypregnenolone
HO Pregnenolone HO
HO
Dehydroepiandrosterone
3β−HSD CH3 P450c17–I CH3 O
C=O
(with 17–20 Lyase) C=O
activity (17–20 lyase) 17β–HSD
OH
OH
O
Androstenedione
O
O
17α-Hydroxyprogesterone
Progesterone O
CH3 P450arom
C=O P450c–11β
Testosterone
P450c17–II OH
(No lyase activity)
HO OH
HO
O 17α-Hydroxyprogesterone 11β-Hydroxytestosterone
CH2OH
O
HO
C=O P450c21
20β−HSD Estradiol-17β 17β–HSD
OH
11β–HSD O
11-Deoxycortisol
O CH3 HO
CH2OH
O
20β–HSD HO-C-H HO-C-H HO
OH OH
Estrone
O O
17α-20β, 21 trihydroxy-4-pregnen-3-one 17α-20β dihydroxy-4-pregnen-3-one 11- Ketotestosterone
Figure 4 The main pathways in the formation of free gonadal steroids in fish, downstream from the pregnenolone step. Upstream
steps are similar to those in mammals and are not shown here. The gonadal steroids specific to teleost fish are 11-KT, the most effective
androgen, and DHP, a C21 steroid acting as maturation-inducing steroid (MIS); In several marine teleosts, the MIS activity is carried
out by another progestogen, 17�,20�,21-trihydroxy-4-pregnen-3-one (20�–S), produced through oxidation of 11-deoxycortisol by 20�
hydroxysteroid dehydrogenase.
to DHP is performed by the granulosa cells possessing and 10 conserved cysteines. LH� and FSH� subunits each
20�-HSD (Figure 4). contain 12 conserved cysteines linked by six disulfide
bridges. This structure is conserved in fish LH� subunits,
but not in FSH�, which is the least conserved gene.
Gonadotropins and Their Regulation All LH� gene promoters isolated from fish contain
putative response elements for Sf-1 and Pitx1, but unlike
The fish pituitary produces and secretes two gonadotro- their mammalian counterparts, the teleost proximal pro-
pins: FSH and LH. Both are heterodimeric glycoproteins moters do not contain an early growth response factor 1
formed by a shared �-subunit (GP�) noncovalently (Egr-1). The latter appears to have been replaced by the
linked to a specific �-subunit. Each subunit, �, FSH�, estrogen receptor (ER). Comparison of FSH�59 flanking
and LH�, is encoded by a distinct gene. region in the fish studies so far revealed that they all share
Molecular cloning techniques allowed so far the isola- several putative response elements, such as GSE, CRE,
tion of the genes encoding the gonadotropin subunits for half sites of ERE, and activating protein 1 response ele
56 fish species belonging to 14 teleost orders. The phylo- ment (AP1), the recognition site for the Fos and Jun
genetic relationships of fish gonadotropins, together with transcription factors.
their structural and biological characteristics, provided
the evidence for their classification as the piscine counter-
Recombinant Gonadotropins
parts of the mammalian FSH and LH.
The �-subunit is the most conserved among fish spe- Fish gonadotropin research has traditionally relied on the
cies and contains two potential sites for N-glycosylation laborious isolation and incomplete purification of the
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Hormonal Control of Reproduction and Growth | Endocrine Regulation of Fish Reproduction 1505
native hormones extracted from thousands of fish pitui vertebrates. It increases the amounts of mRNA encoding
tary glands. The isolation and cloning of cDNAs encoding gonadotropin subunits in the pituitary. The response of
piscine gonadotropin subunits enabled the production of GP� and LH� mRNAs to GnRH implantation in matur
recombinant hormones (rFSH and rLH) through their ing females or males is higher than that of FSH�,
expression in heterologous systems. However, to endow indicating differences in the hypothalamic regulation of
the products with the correct biological activity, they the two gonadotropins.
have to be glycosylated, folded, and assembled as a het GnRH effects vary with a fish’s reproductive stage. In
erodimers. All recombinant LH and/or FSH produced so maturing salmonids sGnRH elevates pituitary mRNAs
far in teleosts can bind and activate the respective recep encoding for GP� and FSH�, but not that of LH�. The
tors, and stimulate sex-steroid output from isolated response of the gonadotropin subunit mRNAs to GnRH
gonadal tissue. The lack of cross-contamination of these in common carp (Cyprinus carpio) too is differential and
recombinant hormones enables the study of LH and FSH depends on the gender and reproductive stage. Thus,
differential functions. In addition, it is anticipated that information regarding the reproductive stage is poten
recombinant gonadotropins will find use in spawning tially conveyed via the steroid hormone profile that can
induction in aquaculture. modulate the response and make it specific to each phase
(Figures 1 and 5). The three forms of GnRH present in
the brain of gilthead seabream (Sparus aurata) and Nile
Regulation of Gonadotropin Synthesis and
tilapia (sbGnRH ¼ GnRH1; cGnRHII ¼ GnRH2;
Secretion
sGnRH ¼ GnRH3) all have LH-stimulating activity in
The hypothalamus regulates synthesis and release of mature females. However, the form most abundant in
gonadotropins through multiple neurohormones. The the pituitary of mature fish, GnRH1, is the least potent
major ones are GnRH in its various forms, kisspeptins in inducing LH release.
and dopamine, and potentially other hormones such as
�-aminobutyric acid (GABA), pituitary adenylate
cyclase-activating peptide (PACAP), norepinephrine, Dopaminergic inhibition of gonadotropins
neuropeptide Y (NPY), serotonin, secretoneurin, ghrelin, Dopamine inhibits both basal and GnRH-stimulated LH
leptin, and glutamate (Figure 5). Of special interest are secretion (Figure 5). In vitro experiments, as validated
hormones associated with growth and metabolism (IGF by molecular studies, show that dopamine D2-like, but
1, glutamate, leptin, and ghrelin), which signifies a rela not D1-like, receptors inhibit gonadotropin secretion
tionship between reproduction, energy reserves, and body directly in the pituitary. In fact, cyprinid spawning
mass of the fish (Figure 5). induction in aquaculture uses dopamine D2 antagonists,
such as domperidone, pimozide, or metoclopramide, to
Gonadotropin-releasing hormone facilitate the stimulation by GnRH of LH release and
GnRH stimulates the production and release of ovulation. Nevertheless, the dopaminergic inhibition
gonadotropins from the pituitary of teleosts as in other does not operate in all fish and is lacking altogether in
Kisspeptin
PACAP
GABA
LH
NPY
Leptin
+
Gonadal
steroids and IGF-I Ghrelin –
Glutamate
peptides
Figure 5 Regulation of LH secretion. Schematic presentation of brain and gonadal regulation of LH secretion. Hormones related
to metabolism and growth are indicated by blue arrows.
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1506 Hormonal Control of Reproduction and Growth | Endocrine Regulation of Fish Reproduction
Atlantic croaker (Micropogonias undulatus) and gilthead gene, namely Kiss2, exists in teleost fish. Apparently, the
sea bream. two Kiss genes arose by gene duplication early in verte
brate evolution, and Kiss2 gene might have been lost in
Kisspeptin regulation of gonadotropins the mammalian lineage (Figure 6). Kiss1 and Kiss2 in
Kisspeptin, a member of the RF amide peptide family, has zebrafish are regionally expressed within the hypothala
important roles in mammals in timing of puberty, main mus, and may exert differential or distinct effects on LH
taining gonadal functions, photoperiod control of seasonal and FSH expression and secretion.
breeding, metabolic gating of fertility, and insulin secre Fish possess two Kiss receptors: kiss1ra and kiss1rb.
tion. Kisspeptin has been proposed to be a novel Sequence identity and genome synteny analyses indicate
gatekeeper for the gonadotropic axis of fish mainly due that zebrafish kiss1ra is a human KISS1R ortholog,
to its potent stimulation of gonadotropin secretion whereas kiss1rb is a specific fish form. Both kisspeptins
(Figure 5). and their receptors are abundantly expressed in the brain,
Kiss1 was cloned in several fish species and its invol notably in the hypothalamus, suggesting that these
vement in gonadotropin release and signaling of sexual ligand–receptor pairs have neuroendocrine and neuro
maturation/puberty has been confirmed so far in medaka modulatory roles. Fish kisspeptins differ in their signal
(Oryzias latipes), zebrafish (Danio rerio) and the European transduction pathways, tissue distribution, and their gene
sea bass (Dicentrarchus labrax). In addition, a second Kiss expression pattern toward puberty.
98 Hamster KISS1
92 Mouse KISS1
Cow KISS1
47
98 Sheep KISS1
92
Pig KISS1
99 Human KISS1
Xenopus KISS1A
49 Opossum KISS1
80
89 Platypus KISS1
94 Grouper KISS2
96 European Seabass KISS2
Medaka KISS2
66 Goldfish KISS2
100 Zebrafish KISS2
0.2
Figure 6 Phylogenetic analysis of kisspeptins. Unrooted phylogenetic trees of kisspeptin sequences generated with a MEGA version
4. Numbers at nodes indicate the bootstrap values as percentages obtained from 1000 replicates. Scale bar indicates the substitution
rate per amino acid. Hamster – Siberian hamster (Phodopus sungarus); mouse – House mouse (Mus musculus); cow (Bos taurus); sheep
(Ovis aries); human (Homo sapiens); xenopus (Xenopus tropicalis); opossum – gray short-tail opossum (Monodelphis domestica);
platypus (Ornithorhynchus anatinus); goldfish (Carassius auratus); zebrafish (Danio rerio); medaka (Oryzias latipes); European sea bass
(Dicentrarchus labrax); grouper – orange-spotted grouper (Epinephelus coioides); grass lizard – Japanese grass lizard (Takydromus
tachydromoides); sockeye salmon – sockeye salmon (Oncorhynchus nerka).
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Hormonal Control of Reproduction and Growth | Endocrine Regulation of Fish Reproduction 1507
Regulation by gonadal steroids the hormone. The transmembrane domain is the most
Steroids released from gonads can feed back and reg conserved part of these receptors, both in structure
ulate the production and release of FSH and LH. This and amino acid sequence. It has seven �-helices
type of feedback effect (positive or negative) varies with composed of 22–28 hydrophobic amino acids, with
the gonadal phase of reproductive development. each crossing the lipid bilayer and being connected
Positive or negative feedback mechanisms operate by three intracellular and three extracellular loops.
either indirectly through certain hypothalamic nuclei, The transmembrane domain is responsible for recep
or directly on the pituitary cells. Negative feedback of tor activation and signal transduction of the hormone.
gonadal steroids on gonadotropin secretion was demon Generally, the cellular localization of the gonadotro
strated using gonadectomy and steroid-replacement pin receptors agrees with their steroidogenic biopotencies
protocols in certain teleost species. In rainbow trout in mature fish. In situ hybridization studies in African
(Oncorhynchus mykiss), the negative feedback of estro catfish revealed FSH-R expression in Sertoli cells, but
gens on the pituitary is direct or indirect through in contrast to other vertebrates, FSH-R is expressed in the
GnRH inhibition, and potentially by E2 upregulation interstitial Leydig cells too, together with LH-R. In
of dopamine receptor mRNA. Nevertheless, a positive European sea bass, FSH-R transcripts are detected in
feedback of gonadal steroid also operates in fish, but the follicular cells surrounding the pre- and early vitello
only early in gonadal development. Estrogens and aro genic oocytes but not on fully grown oocytes, indicating
matizable androgens can stimulate LH�-subunit gene the involvement of FSH-R in the recruitment of new
expression and increase pituitary LH protein levels in oocyte generation and initiation of vitellogenesis.
juveniles of several fish species. FSH-R was localized in the theca layer and inten
sely on granulosa cells of vitellogenic ovaries of coho
Regulation by gonadal peptides salmon (Oncorhynchus kisutch), whereas in the preovula
Activins are peptides composed of two �-subunits that tory follicle, it occurred in the theca and interstitial
form either hetero- or homodimers: activin A (�a þ �a), connective tissue, but not in the granulosa. At all stages
activin BA (�a þ �b), and activin B (�b þ �b). Activins of oogenesis, only granulosa cells of the preovulatory
A and B increase FSH� and reduce LH� mRNA levels follicle exhibited LH-R, which is in line with LH
in cultured pituitary cells. Furthermore, follistatin, an function in oocyte maturation.
activin-binding protein, can reverse the effects of exo The expression of LH-R in males is consistently cor
genous activin on FSH� and LH� expression, and also related with spermiation and spawning in all fish species
stimulate basal expression of FSH� gene. In goldfish studied so far.
(Carassius auratus), Smad3 is likely the principal signal
transducing molecule involved in activin stimulation of
Unorthodox Sites for Kiss, GnRH, and
FSH� expression. While activin was first identified as
Gonadotropins
an FSH stimulator and its effect on FSH biosynthesis
has been well studied in a variety of fish, the details of Recently, evidence is accumulating that the gonads pro
its action mechanism are poorly understood. duce and release hormones, and contain receptors that
originally were thought to be restricted to the hypotha
lamus and pituitary. Oocytes of the gilthead sea bream
Gonadotropin Receptors
produce and release GtHs, processes that can be
In line with the gonadotropic duality, two distinct recep enhanced by GnRH and reduced by an GnRH antago
tors occur in fish gonads: the FSH-R and the LH-R. Both nist. In the African catfish, GnRH-1 and GnRH-2
show different expression profiles during follicular devel mRNAs are expressed in the testis, and GnRH-2
opment. Expression of FSH-R is associated mRNA in the ovary. In addition, kiss1 and kiss1r occur
predominantly with vitellogenesis, while the LH-R is in the ovary and testes of various fish. These
prevalent during oocyte maturation and ovulation. local regulatory axes could finely tune the activity of
Studies on gonadotropin receptors selectivity in repre hypothalamic–pituitary–gonadal axis. Nevertheless,
sentatives of three teleost orders (salmoniformes, further research is still required before an updated com
siluriformes, and cypriniformes) indicated that FSH-Rs prehensive model for this endocrine regulation of fish
not only show a preference for FSH but also respond to reproduction can be formulated.
LH, whereas LH-Rs specifically respond to LH only.
Amago salmon (Oncorhynchus rhodurus) is the only known See also: Hormones in Communication: Hormonal
exception to this scheme. Pheromones. The Pituitary: Pituitary Gland or
The FSH-Rs and LH-Rs are G-protein-coupled Hypophysis. The Reproductive Organs and Processes:
receptors (GPCRs) whose large extracellular domain Anatomy and Histology of Fish Testis; Regulation of
contributes to the recognition and specific binding of Spermatogenesis; Vitellogenesis in Fishes.
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1508 Hormonal Control of Reproduction and Growth | Endocrine Regulation of Fish Reproduction
Further Reading Miura T and Miura C (2001) Japanese eel: Model for analysis of
spermatogenesis. Zoological Science 18: 1055–1063.
Aizen J, Kasuto H, Golan M, et al. (2007) Tilapia follicle-stimulating Miura T and Miura C (2003) Molecular control mechanisms of
hormone (FSH): Immunochemistry, stimulation by gonadotropin- fish spermatogenesis. Fish Physiology and Biochemistry 28: 181–186.
releasing hormone, and effect of biologically active recombinant FSH Nagahama Y and Yamashita M (2008) Regulation of oocyte
on steroid secretion. Biology of Reproduction 76: 692–700. maturation in fish. Development Growth and Differentiation
Devlin RH and Nagahama Y (2002) Sex determination and sex 50: S195–S219.
differentiation in fish: An overview of genetic, physiological, and Schulz RW, França LR, Lareyre JJ, et al. (2010) Spermatogenesis in fish.
environmental influences. Aquaculture 208: 191–364. General and Comparative Endocrinology 165: 390–411.
Ge E (2005) Intrafollicular paracrine communication in the zebrafish Wong TT and Zohar Y (2004) Novel expression of gonadotropin subunit
ovary: The state of the art of an emerging model for the study of genes in oocytes of the gilthead seabream (Sparus aurata).
vertebrate folliculogenesis. Molecular and Cellular Endocrinology Endocrinology 145: 5210–5220.
237: 1–10. Yaron Z and Levavi-Sivan B (2006) Reproduction. In: Evans DH and
Levavi-Sivan B, Bogerd J, Mañañós EL, Gómez A, and Lareyre JJ Claibourne JB (eds.) The Physiology of Fishes, 3rd edn.,
(2010) Perspectives on fish gonadotropins and their receptors. pp.343–386. Boca Raton, FL: CRC Press/Taylor and Francis.
General and Comparative Endocrinology 165: 412–437. Zhou L-Y, Wang D-S, Kobayashi T, et al. (2007) A novel type of
Lubzens E, Young G, Bobe J, and Cerdà J (2010) Oogenesis in teleosts: P450c17 lacking the lyase activity responsible for C21-steroid
How fish eggs are formed. General and Comparative Endocrinology biosynthesis in the fish ovary and head kidney. Endocrinology
165: 367–389. 148: 4282–4291.