Marine Genomics xxx (xxxx) xxxx

Contents lists available at ScienceDirect

Marine Genomics
journal homepage: www.elsevier.com/locate/margen

Review

A review of the potential genes implicated in follicular atresia in teleost fish

⁎
Paola González-Kothera,b, , Marcelo E. Olivac, Arnaud Tanguyd, Dario Moragae
a
Programa de Doctorado en Ciencias Aplicadas mención Sistemas Marinos Costeros, Facultad de Ciencias del Mar y Recursos Biológicos, Universidad de Antofagasta,
Antofagasta, Chile
b
Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Alonso de Ribera 2850, Concepción, Chile
c
Instituto de Ciencias Naturales Alexander von Humboldt, Facultad de Ciencias del Mar y Recursos Biológicos, Universidad de Antofagasta, Antofagasta, Chile
d
Sorbonne Universités, UPMC Univ Paris 06, CNRS UMR 7144, Adaptation et Diversité en Milieu Marin, Equipe ABICE, Station Biologique de Roscoff, 29680 Roscoff,
France
e
Université de Bretagne Occidentale, UMR 6539 UBO/CNRS/IRD/IFREMER, Laboratoire LEMAR, Institut Universitaire Européen de la Mer, Dumont d'Urville, 29280
Plouzané, France

A R T I C LE I N FO A B S T R A C T

Keywords: In recent years, numerous studies conducted on teleost fish have highlighted the contribution of transcriptomic
Atresia studies in elucidating the physiological mechanisms underlying the molecular events of oogenesis and follicular
Teleost fish atresia, enabling the identification of potential genes and molecular networks that participate in both the re-
Genes network productive cycle and the process of follicular atresia. Atresia can affect the reproductive potential of females by
Transcriptomic
reducing the healthy eggs that a female can spawn in both aquaculture and wild populations. The substantial
diversity of reproductive strategies exhibited by teleost fish has contributed to the difficulty in identifying
common genes between species, but a set of core genes has emerged as potential markers for atresia in relation to
apoptosis/autophagy, lipid metabolism, oxidative metabolism and other physiological processes similar to those
identified in other vertebrates, even mammals. We review the current status of the genes that have been
identified in ovaries with atretic oocytes. Our primary goal is to review the current status regarding gene ex-
pression during gonadal development and follicular atresia. This information will enable us to understand the
factors and expression patterns involved in the follicular atresia of teleost fish.

1. Introduction oogenesis, have been published for teleost fish (Lubzens et al., 2010;
Lowerre-Barbieri et al., 2011a; Lubzens et al., 2017). Like mammals,
Among the 32,500 known teleost fish species, a wide variety of the reproductive cycle of teleost fish is characterized by a sequential
reproductive traits can be found, reflecting different life history stra- progression of morphological, endocrine and molecular changes during
tegies (Nelson et al., 2016). Reproductive characteristics have mainly gametogenesis (Jalabert, 2005; Lubzens et al., 2010; Lowerre-Barbieri
been studied using anatomical criteria and classification of gonads by et al., 2011a). Fishes showed a diversity in the mechanisms involved in
histological approaches (Silva et al., 2013). Currently, the molecular sexual plasticity, gametogenesis and reproduction (Kitahashi and
approach has enabled the identification of sets of genes that participate Parhar, 2013). This diversity in fish reproductive strategies has led to
in the reproductive cycle of teleost fish, although many gene functions difficulty in the identification of the key genes participating in the
remain poorly understood (Breton and Berlinsky, 2014). Identification underlying aspects of the molecular and regulatory mechanisms of re-
of genes regulated during the different stages of gonad development is production, since genes could remain specific to each species of teleost
of major importance in studies for fish species of economic importance fish (Tingaud-Sequeira et al., 2009; Kitahashi and Parhar, 2013; Breton
for aquaculture and fisheries management, such as Salmoniformes and et al., 2019).
Pleuronectifomes (Lubzens et al., 2010; Lowerre-Barbieri et al., 2011b; For reasons not understood to date, in natural and cultured fishes,
Migaud et al., 2013). Indeed, the control of sexual maturation and the normal female reproductive cycle can show a disruption in the re-
spawning to produce high quality eggs is a primary requirement for productive process (Habibi and Andreu-Vieyra, 2007). These females
successful aquaculture production (Migaud et al., 2013). fail to complete maturation and ovulation due to the elimination of
Several reviews describing the process of reproduction, mainly vitellogenic oocytes prior to ovulation in a process known as follicular

⁎
Corresponding author at: Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Alonso de Ribera 2850, Concepción, Chile.
E-mail address: [email protected] (P. González-Kother).

https://doi.org/10.1016/j.margen.2019.100704
Received 27 December 2018; Received in revised form 31 July 2019; Accepted 3 September 2019
1874-7787/ © 2019 Published by Elsevier B.V.

Please cite this article as: Paola González-Kother, et al., Marine Genomics, https://doi.org/10.1016/j.margen.2019.100704
P. González-Kother, et al. Marine Genomics xxx (xxxx) xxxx

atresia (Miranda et al., 1999; Morais et al., 2012). Follicular atresia may ovarian development is synchronized by hormones that are pre-
be an important problem in cultured fishes, when females showing dominantly produced by the brain-pituitary-gonad axis (BPG)
large amounts of vitellogenic follicles failed to mature and ovulate (Okuzawa and Gen, 2013; Chen et al., 2013; Pinto et al., 2017). Some
during the spawning season (Rideout and Tomkiewicz, 2011). The mechanisms of this BPG axis in fish are not fully understood because
process of follicular atresia remains extremely complex, and little is their regulation is complex (Lubzens et al., 2010; Zohar et al., 2010;
known about genes and other processes in the ovary that either regulate Miranda et al., 2013). Hormones are key molecules in reproduction
atresia or are the consequences of atresia (Yamamoto et al., 2016). control, such as gonadotrophin releasing hormone (GnRH), which has a
Regardless of the species studied, follicular atresia is a highly main role in the regulation of the synthesis and release of gonadotropin
regulated process that is essential for the maintenance of ovarian hormones (GtHs), follicle stimulating hormone (FSH) and luteinizing
homeostasis during the reproductive cycle (Krysko et al., 2008; hormone, (LH) (Habibi and Andreu-Vieyra, 2007; Miranda et al., 2013).
Lowerre-Barbieri et al., 2011a). In most mammals, follicular atresia is GtHs have an endocrine control of reproduction, promoting the
primarily induced by the apoptosis of granulosa cells (Thomé et al., synthesis of sex steroids through the stimulation of specific enzymes
2009; Yan et al., 2018). Instead, studies in freshwater teleost fish have and regulating gametogenesis (Lubzens et al., 2010; Levavi-Sivan et al.,
suggested that apoptosis and autophagy act during follicular atresia 2010). In mammals, GnRH has been shown to participate in follicular
(Santos et al., 2005; Valdebenito et al., 2011; Morais et al., 2012). In atresia by inducing apoptosis in oocytes, mainly in granuloma cells.
teleost fish, the development and maturation of the gonads are con- However, in teleost fish, the relationship between GnRH and ovarian
trolled by genetic and environmental factors and are regulated by a atresia is not clear (Lubzens et al., 2010; Thomé et al., 2009). For those
network of molecular signals (Chen et al., 2013). Gene expression reasons, the follicular atresia status is mainly determined using mor-
studies have been performed to identify the molecular mechanisms by phological characteristics.
which the oocytes can grow and mature during oogenesis, and putative
genes involved in oocyte development and follicular atresia have been 2.1. Transcriptomics of oogenesis
recently discovered (Villeneuve et al., 2010; Martyniuk et al., 2013).
Next-generation sequencing (NGS) technologies have strongly con- Regardless of the specific pattern of ovarian development in fish, all
tributed to the identification of genes and physiological networks that oocytes pass through a series of defined stages, generating complex
participate in oocyte development, including atresia, and more gen- transcriptomic and proteome expression networks according to the
erally to the understanding of the molecular mechanisms involved in developmental stage of the follicle (García-López et al., 2011; Lubzens
the physiology of the reproductive process. In this paper, we aim to et al., 2017; Breton et al., 2019). Currently, transcriptomic analysis
review the transcriptomic data associated with reproduction in teleost strongly contributes to a better understanding of complex biological
fish to identify genes that are expressed during atresia. processes, such as growth, reproduction, and the immune response
(Wang et al., 2009; Gallardo-Escárate et al., 2014). The transcriptome
2. Atresia of teleost fish contains different species of transcripts, including mRNAs, noncoding
RNAs and small RNAs, and gene expression levels during development
Environmental stressors, such as food availability, contaminant ex- and under different conditions have been quantified (Wang et al.,
posure, and global warming, can potentially interfere with oogenesis by 2009). miRNAs have been shown to participate in organogenesis by
disrupting the brain-pituitary-gonad axis and inducing atresia of controlling miRNA renewal and the activation and/or inhibition of
ovarian follicles (Table 1) (Babin et al., 2007; Yamamoto et al., 2011; specific transcripts' expressions at different developmental stages
Molina et al., 2018; Sullivan and Yilmaz, 2018). Atresia has been de- (Bizuayehu and Babiak, 2014). Specific miRNAs have been potentially
fined as a normal process that takes place inside the ovaries, but it is implicated in the early stages of embryo development (Giraldez, 2005),
considered a reproductive dysfunction because vitellogenic oocytes in the destabilization of maternal transcripts (Wienholds, 2005) and in
cannot complete their development, increasing atretic oocytes, a pro- cellular differentiation (Bartel, 2009).
cess also known as skipped spawning (Rideout and Tomkiewicz, 2011). The involvement of miRNAs in oogenesis has been shown in the
The increase in the proportion of atretic oocytes can have serious regulation of mechanisms involved in follicular development, vitello-
consequences for fish populations because nonspawn vitellogenic oo- genesis, oocyte maturation and sexual differentiation in the rainbow
cytes may reduce the reproductive potential of the species through a trout Oncorhynchus mykiss (Ma et al., 2012; Juanchich et al., 2013), in
decrease in the number of viable offspring produced (Rizzo and Bazzoli, the zebrafish Danio rerio (Presslauer et al., 2017; Wong et al., 2018),
1995; Miranda et al., 1999; Santos et al., 2005). and in the medaka Oryzias latipes (Bouchareb et al., 2017). Some
In the Argentinian silver side Odontesthes bonaerensis, red seabream miRNA have been specifically detected in fish testis, but due to the
Pagrus major and striped bass Morone saxatilis, a high water temperature similar functions of both ovaries and testis, their involvement in the
in the gonads provoked regression by inhibiting the expression of spe- regulation of gene expression in both gonads cannot be excluded, as
cific genes at the level of the brain-pituitary-gonads, reflected by an shown by the expression of sox9b in germinal cells present in the basal
increase in atresia (Miranda et al., 2013; Akhavan et al., 2016). Cyclic membrane, which is common to both gonads (Nishimura et al., 2016).

Table 1
Factors involved in reproductive dysfunctions and follicular atresia in teleost fish.
Factor Species Effect or Alteration Reference

Temperature Acipenser transmontanus Temperature induced oocyte development arrest and follicular atresia. Linares-Casenave et al., 2002
Odontesthes bonariensis High temperature produced disruption at all levels of reproductive Elisio et al., 2012; Miranda et al.,
axis and increased atresia. 2013
Captivity Anoplopoma fimbria Reproductive dysfunctions at different levels of the reproductive axis, Guzmán et al., 2013
including atresia.
Engraulis mordax Starvation induced atresia. Hunter and Macewicz, 1985
Endocrine disruption by chemicals Chalcalburnus tarichi Increased atresia and fibrotic areas in the ovarian tissue. Kaptaner and Ünal, 2011
Danio rerio High doses of chemical increased follicular atresia. Molina et al., 2018
Endocrine disruption by nutritional Oncorhynchus kisutch Nutritional stress induced atresia and changes in ovarian transcripts. Yamamoto et al., 2011
stress
Photoperiod Dicentrarchus labrax Changes in photoperiod induced atretic oocytes Zanuy et al., 1995

2
 P. González-Kother, et al.

Table 2
Potential molecular marker genes for follicular atresia in teleost fish.
Gene Function Gene Sequence description [Gene identification (species)] Relation with atresia [Species identification] Reference

Apoptosis bax Bcl-2 protein family[Several species] Ovary showed high protein expression during late atresia [Astyanax bimaculatus, Leporinu obtusidens, Morais et al., 2012
Prochilodu argenteus]
bcl-2 Baclin-2 protein family[Several species] Ovary showed higher protein expression in early and advanced atresia than during late atresia Morais et al., 2012
[Astyanax bimaculatus, Leporinu obtusidens, Prochilodu argenteus]
casp3 Caspase3[Oncorhynchus mykiss] Gene increased in Inhibin network during atresia [Micropterus salmoides] Martyniuk et al., 2013
Gene showed high expression during late atresia [Astyanax bimaculatus, Leporinu obtusidens, Morais et al., 2012
Prochilodu argenteus]
casp8 Caspase 8[Oncorhynchus kisutch] Gene expression increased in fasted fish with severe atresia [Oncorhynchus kisutch] Yamamoto et al., 2011
casp9 Caspase 9[Oncorhynchus kisutch] Gene increase in fasted fish with severe atresia [Oncorhynchus kisutch] Yamamoto et al., 2011
pdcd4 Programmed cell death protein 4[Salmo salar] Potential early indicator of ovarian apoptosis/atresia. [Oncorhynchus kisutch] Yamamoto et al., 2016
litaf Lipopolysaccharide-induced tumor necrosis factor (TNF)-α Gene showed high expression in fasted fish ovaries leading to high incidence of atresia [Oncorhynchus Yamamoto et al., 2016
factor[Salmo salar] kisutch]
klf6 Kruppel-like factor 6[Salmo salar] Gene is a potential early marker of apoptosis/atresia [Oncorhynchus kisutch] Yamamoto et al., 2016
Autophagy beclin-1 Beclin-1[Several species] Ovary showed high protein expression in advanced at atresia [Astyanax bimaculatus, Leporinu Morais et al., 2012
obtusidens, Prochilodu argenteus]

3
Apoptosis/autophagy cathepsin-D Cathepsin-D[Several species] Protein expression increased more in early and advanced than in late atresia [Astyanax bimaculatus, Morais et al., 2012
Leporinu obtusidens, Prochilodu argenteus]
Antiapoptotic function s100a10 S100A10 calcium binding protein[Epinephelus coioides] Gene showed up-regulation in atretic ovaries [Solea senegalensis] Tingaud-Sequeira et al.,
2009
Apoptosis-related function fst Follistatin[Oryzias latipes] Gene is a potential marker of ovarian age [Oryzias latipes] Herpin et al., 2013
Follistatin[Danio rerio] FST network decreased during atresia [Micropterus salmoides] Martyniuk et al., 2013
krt79 Type 2 keratin k 8b (S2) [Oncorhynchus mykiss] Gene is a potential early marker of altered ovarian follicle growth [Oncorhynchus kisutch] Yamamoto et al., 2016
s8 Type 1 keratin s8[Oncorhynchus mykiss] Gene showed down-regulation in fasted fish ovaries [Oncorhynchus kisutch] Yamamoto et al., 2016
thbs Thrombospondin[Bos taurus] Gene showed up-regulation in atretic ovaries [Solea senegalensis] Tingaud-Sequeira et al.,
2009
Lipid metabolic process apoc1 Apolipoprotein C-I[Hemibarbus mylodon] Gene expression was up-regulated in atretic ovaries [Solea senegalensis] Tingaud-Sequeira et al.,
2009
fabp11 fatty acid-binding protein (FABP) [Solea senegalensis] Gene was strongly upregulated in Agullero et al., 2007
somatic cells surrounding atretic follicles [Solea senegalensis]
amh Anti-Mullerian hormone[Oncorhynchus kisutch] Gene expression increased in atresia and caused a reduction of the healthy ovarian follicles Yamamoto et al., 2016
[Oncorhynchus kisutch]
alv Alveolin [Oncorhynchus mykiss] Gene is expressed in oocytes that fail to develop into vitellogenic oocytes in fasted fish [Oncorhynchus Yamamoto et al., 2016
kisutch]
hsd3b hydroxy-delta-5-steroid dehydrogenase 3 beta [Salvelinus Gene expression changed before atresia became evident [Oncorhynchus kisutch] Yamamoto et al., 2016
alpinus]
Marine Genomics xxx (xxxx) xxxx
P. González-Kother, et al. Marine Genomics xxx (xxxx) xxxx

In the zebrafish D. rerio, a similar trend is observed for miR-22, which atresia or as an early marker of impaired follicle development and/or
plays a major role in spermatogenesis and has potential involvement in atresia, but the function of the gene remains unknown (Yamamoto
maternal development (Zhang et al., 2017). In rainbow trout O. mykiss, et al., 2016). Genes of the klf family, such as klf6 and klf16, have been
the expression pattern of miRNAs is also modified according to the identified in teleost fish (Charlier et al., 2012; Yamamoto et al., 2016).
postovulatory stage, altering egg quality, and two miRNAs, let-7 and The gene klf6, identified in O. kisutch, has been proposed as an early
miR-21, have been shown to regulate the development of eggs (Ma marker of apoptosis/atresia (Yamamoto et al., 2016), while the func-
et al., 2012). In the Nile tilapia Oreochromis niloticus, the embryos of tion of klf16 remains unclear in O. mykiss, although it could be involved
females and males are characterized by different expression patterns of in oogenesis by playing important roles during intrafollicular compe-
miRNAs (Eshel et al., 2014). In the testes in tilapia at later stages, the tence acquisition (Charlier et al., 2012).
most abundantly expressed miRNA families are miR-33a, miR-132, The lipopolysaccharide-induced tumor necrosis factor (TNF)-alpha
miR-135b, and miR-212 (Xiao et al., 2014). However, no data regarding factor (litaf) is a transcription factor that plays an important role in
the involvement and regulation of miRNAs during atresia are available, regulating the expression of TNF-α, and this gene may induce the ex-
offering a new area of research. pression of Tnf-α, increasing the incidence of atresia, as indicated in O.
In fishes of at least six orders (Characiformes, Salmoniformes, kisutch (Yamamoto et al., 2011; Yamamoto et al., 2016). However, the
Beloniformes, Gadiformes, Perciformes and Pleuronectifomes), recent study of both the expression and biological relevance of litaf in fish is
transcriptomic studies allowed the identification of 20 core genes that still very limited (Lv et al., 2017).
play a potential role in atresia (Table 2) that are mainly associated with The transcript associated with the prevention of apoptosis, S100-
apoptosis or indicate aging ovaries associated with atresia (Agullero like calcium binding protein (s100a10), was shown to be upregulated in
et al., 2007; Tingaud-Sequeira et al., 2009; Yamamoto et al., 2011; atretic ovaries of Solea senegalensis (Tingaud-Sequeira et al., 2009).
Morais et al., 2012; Herpin et al., 2013; Yamamoto et al., 2016). In wild Follistatin (FST), a local regulator of gonadal functions, is a pow-
largemouth bass, Micropterus salmoides, 3664 genes have been identi- erful inhibitor of follicle stimulating hormone (FSH) secretion (Chong
fied in ovarian development, of which 15 were associated with folli- et al., 2015), and FST is a multifunctional regulatory protein involved in
cular atresia (Martyniuk et al., 2013). In a culture of coho salmon numerous physiological activities such as reproduction, development,
Oncorhynchus kisutch with food restriction, 30 genes were associated neural induction, myogenesis and immunoregulation (Armand et al.,
with the reproductive process, and eight were closely associated with 2003; Liu et al., 2014). Chong et al. (2015) suggested that follistatin
follicular atresia (Yamamoto et al., 2016). In Senegalese sole, Solea may participate in caspase3-dependent apoptosis through the Bcl2/Bax
senegalensis, an extensive study allowed the identification of 118 ESTs, gene family in bovine granulosa cells. In teleost fish, the fst gene is
including 18 transcripts that were differentially regulated when com- implicated in folliculogenesis and oocyte maturation, and an early and
pared to atresia with vitellogenic and mature ovaries (Tingaud-Sequeira specific expression of fst during ovarian differentiation may be the
et al., 2009). earliest marker of ovarian differentiation. Fst may be a marker of de-
The identification of genes in the breeding cycle of Micropterus veloping oocytes in the rainbow trout Oncorhynchus mykiss (Nicol et al.,
salmoides has enabled the identification of several networks playing a 2013). Conversely, in the medaka Oryzia latipes, fst gene expression was
role in oocyte maturation and genes exhibiting a strong downregulation linked to ovary age, because its expression was higher in the ovarian
in atresia (Martyniuk et al., 2013). During atresia, downregulated epithelium and interstitium of old ovaries (Herpin et al., 2013). In
pathways include gap junction and actin cytoskeleton regulation, go- contrast, in the largemouth bass M. salmoides, the fst gene is down-
nadotrope and mast cell activation, and vasopressin receptor signaling, regulated in atretic ovaries (Martyniuk et al., 2013).
while upregulated pathways include oxidative phosphorylation and Thrombospondin (thbs), also known as TSP1, was the first anti-an-
reactive oxygen species (ROS) metabolism (Martyniuk et al., 2013). giogenic agent, and apoptosis was shown to be the main mechanism of
This review identified potential genes involved in follicular atresia its anti-angiogenic activity (Mirochnik et al., 2008). In primate ovaries,
in teleost fish, mainly associated with the expression of apoptosis genes TSP1 is upregulated and may be involved in the cessation of angio-
and lipid process genes. genesis in follicles undergoing atresia (Thomas et al., 2008). In atretic
ovaries of Solea senegalensis, thbs was upregulated, and this gene was
2.2. Apoptosis/autophagy-related genes expressed in hypertrophied and vacuolized follicular cells of atretic
follicles (Tingaud-Sequeira et al., 2009).
Several studies have indicated that both apoptosis and autophagy Humans keratin sustains cell architecture by serving as a cytoske-
could act cooperatively during follicular atresia to ensure more efficient leton, and it is also involved in the regulation of cell metabolism and
ovarian regression after spawning (Thomé et al., 2009; Morais et al., signaling, thereby influencing cell proliferation, migration and apop-
2012). Apoptosis also involves the sequential activation of a cascade of tosis (Komine, 2018). In teleost fish, several keratin genes are expressed
caspases that have been linked to atresia (Habibi and Andreu-Vieyra, in the ovarian stroma and somatic follicle cells (Schaffeld et al., 2002).
2007). In the coho salmon Oncorhynchus kisutch, the involvement of In Oncorhynchus kisutch, the keratin genes s8 (type 1 keratin s8) and
caspase-8 and caspase-9 has been demonstrated, especially in fasted krt79 (type 2 keratin k8b (S2)) exhibit a downregulation in fasted fish
females (Yamamoto et al., 2016). In the freshwater characiforme fishes, ovaries that precedes measurable size changes, suggesting that these
Astyanax bimaculatus, Leporinum obtusidens, and Prochilodus argenteus, genes could be early markers of altered ovarian follicle growth
Morais et al. (2012) proposed a model that explains the participation of (Yamamoto et al., 2016). In O. mykiss, higher expression of keratin 18
caspase-3, the Bcl-2 protein family (bcl-2 and bax), the lysosomal ca- and keratin 8 was observed in low quality eggs (Aegerter et al., 2005).
thepsin-D and beclin-1 in the regulation of follicular atresia via au- In S. senegalensis, keratin 8 was identified in vitellogenic ovaries, but at
tophagy and apoptosis in fish ovaries, with those genes being over- lower levels, while type II keratin E3-like protein was upregulated in
expressed in the follicular and thecal cells during early and advanced mature ovaries (Tingaud-Sequeira et al., 2009). Other types of keratins
regression of ovaries. Additional apoptosis related genes, mainly cas- have been identified in this species, such as keratin type I, CK19 and
pase-3, are related to Bcl-2 and Bax genes and regulate the follicular CK19 and keratin 5, but the relationship of these genes to atresia is
atresia and apoptosis of granulosa cells (Nassauw et al., 1999). unknown (Cerdà et al., 2008).
Other genes identified with a potential relationship to apoptosis/
atresia are programmed cell death protein 4 (pdcd4), genes of the 2.3. Lipid metabolic process-related genes
Kruppel-like factor family (klf) and lipopolysaccharide-induced tumor
necrosis factor (TNF)-alpha factor (litaf). In fasted Oncorhynchus kisutch, The alveolin gene (alv), a member of the astacin metalloprotease
the pdcd4 gene may act as an early indicator of ovarian apoptosis/ family that encodes cortical alveoli components, is specifically

4
P. González-Kother, et al. Marine Genomics xxx (xxxx) xxxx

expressed in the oocytes of teleost fish such as Oryzias latipes (Shibata cell growth and differentiation, apoptosis, and cellular homeostasis.
et al., 2012), Micropterus salmoides (Martyniuk et al., 2013), the Atlantic Amh has been identified in fish ovaries (Yamamoto et al., 2016), and
bluefin tuna, Thunnus thynnus (Gardner et al., 2012) and Oncorhynchus similar to what occurs in mammalian females, the serum levels of amh
kisutch (Yamamoto et al., 2016). In O. kisutch, alv is strongly expressed could be considered a good marker of ovarian follicle reserve and fer-
in previtellogenic oocytes and has decreased expression during vi- tility potential, since amh plays an important role in folliculogenesis
tellogenesis, while being maintained at elevated levels in secondary (Rodríguez-Mari et al., 2005). In fasted Oncorhynchus kisutch, a decrease
follicles that have a slow development and fail to initiate vitellogenesis of amh expression may indicate increases in atresia and reduction of the
in fasted fish (Yamamoto et al., 2016). This result may indicate the healthy ovarian follicle pool (Yamamoto et al., 2016), while in healthy
potential of this gene as a marker of atresia in fish with non-normal O. mykiss, this gene has been identified only in the testis (Baron et al.,
nutritional aspects, mainly in cultured fish. 2005). Meanwhile, amh in Gadus morhua showed various patterns of
The members of the superfamily of lipid-binding proteins (LBP), expression according to the oocyte developmental stage (Breton and
which are called fatty acid-binding proteins (FABPs) and play a primary Berlinsky, 2014).
role in the regulation of fatty acid uptake and intracellular transport, In O. kisutch, prolonged nutritional stress may disrupt the re-
have been associated with atresia (Chmurzyńska, 2006). During their productive system and induce follicular atresia in part via reductions in
growth, oocytes accumulate high amounts of neutral lipids (NLs) in the downstream effects of steroidogenesis-related genes (hsd3b) and E2
ooplasm lipid droplets, and these lipids are later utilized as an energy production (Yamamoto et al., 2011). The hsd3b (hydroxy-delta-5-
resource by developing embryos and larvae (Ryu et al., 2013). The steroid dehydrogenase 3 beta) gene encodes steroidogenic enzymes
FABP-related genes have also been identified in ovaries of a group- involved in estradiol 17β (E2) and showed clear differences in expres-
synchronous species, the flatfish Solea senegalensis (Agullero et al., sion between fed and fasted fish before morphological signs of ovarian
2007), in the asynchronous ovarian follicle development of Thunnus atresia were apparent (Yamamoto et al., 2011; Yamamoto et al., 2016).
thynnus (Gardner et al., 2012) and in Morone salmoides (Britton et al.,
2010; Martyniuk et al., 2013). Different functions have been suggested 3. Conclusion
for FABPs in these species. In S. senegalensis, fabp11 mRNA was found in
previtellogenic oocytes and was strongly upregulated in somatic cells This review enables us to identify potential genes involved in
surrounding atretic follicles (Agullero et al., 2007), while in T. thynnus, atresia, mainly associated with apoptosis and lipid processing. The
fabp11 seems to be involved in membrane trafficking and the seques- identification of genes and pathways involved in atresia could allow the
tration of lipids in oocytes for normal embryo development (Gardner identification of potential genetic biomarkers that could be used both in
et al., 2012). Additionally, in T. thynnus, nine different fabps transcripts aquaculture and in breeding studies in wild populations, especially in
have been identified in ovaries, especially the TTC01498 transcript, those subject to high fishing exploitation. The advancement of new
which shows a high similarity to FABP11 and could play a role in fatty sequencing technologies may also be a powerful tool for the discovery
acid trafficking specifically related to oocyte atresia (Gardner et al., of genes and regulatory networks due to the considerable diversities of
2012). Until now, fabp11 has been identified only in teleost fish in reproductive strategies shown by teleost fish.
several organs, including the liver and gonads (Crovetto and Córdoba,
2016). Several FABPs (named FABP1 to FABP-12) have been described Funding
in mammals as being potentially involved in pathways regulating
cancer development (Amiri et al., 2018). The FABPs proteins could be Provided by CONICYT N° 21130197 doctoral scholarship (to P.
used as protein markers for the prognosis and diagnosis of cancers. González-Kother) and CONICYT+PAI/ ATRACCION DE CAPITAL
FABP5 has been localized in a specific population of ovarian macro- HUMANO AVANZADO DEL EXTRANJERO + Folio N°PAI80160001 (to
phages in advanced atretic follicles of adult mice (Nourani et al., 2005). P.GeK, D.M and M.E.O); “Laboratoire d'Excellence” LabexMER (ANR-
Additionally, FABP4, a mediator of lipid trafficking in adipocytes, has a 10-LABX-19) and co-funded by a grant from the French government
key role in the interaction of cancer cells with adipocytes, which pro- under the program “Investissements d'Avenir” (to P.G-K).
vides fatty acids to the cancer cells and fuels rapid tumor growth
(Nieman et al., 2011). The relation of FABPs to the metabolism/pa- References
thology of ovaries or follicular atresia in mammals and teleost fish,
respectively, indicates that FAPBs are potential molecular markers to Aegerter, S., Jalabert, B., Bobe, J., 2005. Large scale real-time PCR analysis of mRNA
study for atresia. abundance in rainbow trout eggs in relationship with egg quality and post-ovulatory
ageing. Mol. Reprod. Dev. 72, 377–385.
In atretic ovaries of Solea senegalensis, the gene encoding apolipo- Agullero, M.J., Andre, M., Morais, S., Cerdà, J., Babin, P.J., 2007. High transcript level of
protein A-I (apoc) was upregulated. Apolipoproteins have been identi- fatty acid-binding protein 11 but not of very low-density lipoprotein receptor is
fied in O. mykiss, G. morhua, striped bass Morone saxatilis, M. salmoides correlated to ovarian follicle atresia in a teleost fish (Solea senegalensis). Biol. Reprod.
77, 504–516.
and T. thunnus and show differential expression patterns throughout Akhavan, S.R., Salati, A.P., Falahatkar, B., Jalali, S.A.H., 2016. Changes of vitellogenin
oocyte development (Cerdà et al., 2008; Gardner et al., 2012; and lipase in captive Sterlet sturgeon Acipenser ruthenus females during pre-
Martyniuk et al., 2013; Breton and Berlinsky, 2014). The zebrafish D. vitellogenesis to early atresia. Fish Physiol. Biochem. 42, 967–978. https://doi.org/
10.1007/s10695-015-0189-8.
rerio has been proposed as a model for understanding apolipoprotein
Amiri, M., Yousefnia, S., Forootan, F.S., Peymani, M., Ghaedi, K., Esfahani, M.H.N., 2018.
biology and its relationship to lipid metabolism, especially in larval Diverse roles of fatty acid binding proteins (FABPs) in development and pathogenesis
models. The overexpression of apoA-IV has been associated with a de- of cancers. Gene 676, 171–183. https://doi.org/10.1016/j.gene.2018.07.035.
Armand, A.-S., Gaspera, B.D., Launay, T., Charbonnier, F., Gallien, C.L., Chanoine, C.,
crease of high-fat food intake in larval zebrafish, indicating that dif-
2003. Expression and neural control of Follistatin versus Myostatin genes during
ferential expression of apolipoprotein genes of could serve as an in- regeneration of mouse soleus. Dev. Dyn. 227, 256–265.
dicator of health or disease in larvae (Otis et al., 2015). Apolipoproteins Babin, P.J., 1987. Apolipoproteins and the association of egg yolk proteins with plasma
can play a role in the transport of cholesterol and act as a precursor for high density lipoproteins after ovulation and follicular atresia in the rainbow trout
(Salmo gairdneri). J. Biol. Chem. 262 (9), 4290–4296.
all steroid hormones related to metabolism and vitellogenesis uptake Babin, P.J., Cerdà, J., Lubzens, E., 2007. The Fish Oocyte. From Basic Studies to
(Babin, 1987; Tingaud-Siqueira et al., 2009), as occurs in Salmo gaird- Biotechnological Applications. Springer, Dordrecht, NL.
neri, where apoliproteins and the resorption of yolk during follicular Baron, D., Houlgatte, R., Fostier, A., Guiguen, Y., 2005. Large-scale temporal gene ex-
pression profiling during gonadal differentiation and early gametogenesis in rainbow
atresia were correlated with the presence of egg yolk proteins combined trout. Biol. Reprod. 73, 959–966. https://doi.org/10.1095/biolreprod.105.041830.
with HDL (Babin, 1987). Bartel, D.P., 2009. MicroRNAs: target recognition and regulatory functions. Cell 136,
The anti-Mullerian hormone (amh) gene, a member of the Tgf-beta 215–233.
Bizuayehu, T.T., Babiak, I., 2014. MicroRNA in teleost fish. Genome Biol. Evol. 6,
superfamily, plays an important role in signaling pathways related to

5
P. González-Kother, et al. Marine Genomics xxx (xxxx) xxxx

1911–1937. keratin/regulation-of-expression-of-keratins-and-their-pathogenic-roles-in-
Bouchareb, A., Le Cam, A., Montfort, J., Gay, S., Nguyen, T., Bobe, J., Thermes, V., 2017. keratinopathies.
Genome-wide identification of novel ovarian-predominant miRNAs: new insights Krysko, D.V., Diez-Fraile, A., Criel, G., Svistunov, A.A., Vandenabeele, P., D'Herde, K.,
from the medaka (Oryzias latipes). Sci. Rep. 7, 40241. 2008. Life and death of female gametes during oogenesis and folliculogenesis.
Breton, T.S., Berlinsky, D.L., 2014. Characterizing ovarian gene expression during oocyte Apoptosis 13, 1065–1087. https://doi.org/10.1007/s10495-008-0238-1.
growth in Atlantic cod (Gadus morhua). Comp. Biochem. Physiol. Part D 9, 1–10. Levavi-Sivan, B., Bogerd, J., Mañanós, E.L., Gómez, A., Lareyre, J.J., 2010. Perspectives
https://doi.org/10.1016/j.cbd.2013.11.001. on fish gonadotropins and their receptors. Gen. Comp. Endocrinol. 165, 412–437.
Britton, J.R., Harper, D.M., Oyugi, D.O., 2010. Is the fast growth of an equatorial https://doi.org/10.1016/j.ygcen.2009.07.019.
Micropterus salmoides population explained by high water temperature? Ecol. Freshw. Linares-Casenave, J., Van Eenennaam, J.P., Doroshov, S.I., 2002. Ultrastructural and
Fish 19, 228–238. https://doi.org/10.1111/j.1600-0633.2010.00407.x. histological observations on temperature-induced follicular ovarian atresia in the
Cerdà, J., Mercadé, J., Lozano, J.J., Manchado, M., Tingaud-Sequeira, A., Astola, A., white sturgeon. J. Appl. Ichthyol. 18 (4–6), 382–390.
Infante, C., Halm, S., Viñas, J., Castellana, B., Asensio, E., Cañavate, P., Martínez- Liu, Z., Xue, L., Shen, W., Ying, J., Zhang, Z., 2014. Spatio-temporal expression pattern
Rodríguez, G., Piferrer, F., Planas, J.V., Prat, F., Yúfera, M., Durany, O., Subirada, F., and fasting response of follistatin gene in teleost Larimichthys crocea. Genes Genom.
Rosell, E., Maes, T., 2008. Genomic resources for a commercial flatfish, the 36, 205–214. https://doi.org/10.1007/s13258-013-0159-4.
Senegalese sole (Solea senegalensis): EST sequencing, oligo microarray design, an- Lowerre-Barbieri, S.K., Brown-Peterson, N.J., Murua, H., Tomkiewicz, J., Wyanski, D.M.,
ddevelopment of the Soleamold bioinformatic platform. BMC Genomics 9, 508. Saborido-Rey, F., 2011a. Emerging issues and methodological advances in fisheries
https://doi.org/10.1186/1471-2164-9-508. reproductive biology. Mar. Coast. Fish. 3, 32–51.
Charlier, C., Montfort, J., Chabrol, O., Brisard, D., Nguyen, T., Le Cam, A., Richard- Lowerre-Barbieri, S.K., Ganias, K., Saborido-Rey, F., Murua, H., Hunter, J.R., 2011b.
Parpaillon, L., Moreews, F., Pontarotti, P., Uzbekova, S., Chesnel, F., Bobe, J., 2012. Reproductive timing in marine fishes: variability, temporal scales, and methods. Mar.
Oocyte-somatic cells interactions, lessons from evolution. BMC Genomics 13, 560. Coast. Fish. 3, 71–91.
Chen, J., Hu, W., Zhu, Z.Y., 2013. Progress in studies of fish reproductive development Lubzens, E., Young, G., Bobe, J., Cerdà, J., 2010. Oogenesis in teleosts: how fish eggs are
regulation. Chin. Sci. Bull. 58, 7–16. https://doi.org/10.1007/s11434-012-5577-1. formed. Gen. Comp. Endocrinol. 165, 367–389. https://doi.org/10.1016/j.ygcen.
Chmurzyńska, A., 2006. The multigene family of fatty acid binding proteins (FABPs): 2009.05.022.
function, structure and polymorphism. J. Appl. Genet. 47 (1), 39–48. Lubzens, E., Bobe, J., Young, G., Sullivan, C.V., 2017. Maternal investment in fish oocytes
Chong, Z., Dong, P., Riaz, H., Shi, L., Yu, X., Cheng, Y., Yang, L., 2015. Disruption of and eggs: the molecular cargo and its contributions to fertility and early develop-
follistatin by RNAi increases apoptosis, arrests S-phase of cell cycle and decreases ment. Aquaculture 472, 107–143. https://doi.org/10.1016/j.aquaculture.2016.10.
estradiol production in bovine granulosa cells. Anim. Reprod. Sci. 155, 80–88. 029.
https://doi.org/10.1016/j.anireprosci.2015.02.003 0378-4320/. Lv, Y., Xiang, X., Jiang, Y., Tang, L., Zhou, Y., Zhong, H., Xiao, J., Yan, J., 2017.
Crovetto, C.A., Córdoba, O.L., 2016. Structural and biochemical characterization and Identification and characterization of lipopolysaccharide induced TNF_ factor from
evolutionary relationships of the fatty acid-binding protein 10 (Fabp10) of hake blunt snout bream, Megalobrama amblycephala. Int. J. Mol. Sci. 18, 233. https://doi.
(Merluccius hubbsi). Fish Physiol. Biochem. 42, 149–165. https://doi.org/10.1007/ org/10.3390/ijms18020233.
s10695-015-0126-x. Ma, H., Hostuttler, M., Wei, H., Rexroad, C.E., Yao, J., 2012. Characterization of the
Elisio, M., Chalde, T., Miranda, L.A., 2012. Effects of short periods of warm water fluc- rainbow trout egg MicroRNA Transcriptome. PLoS One 7, e39649.
tuations on reproductive endocrine axis of the pejerrey (Odontesthes bonariensis) Martyniuk, J.C., Prucha, M.S., Doperalski, N.J., Antczak, P., Kroll, K.J., Falciani, F.,
spawning. Comp. Biochem. Physiol. A 163, 47–55. Barber, D.S., Denslow, N.D., 2013. Gene expression networks underlying ovarian
Eshel, O., Shirak, A., Dor, L., Band, M., Zak, T., Markovich-Gordon, M., Chalifa-Caspi, V., development in wild largemouth bass (Micropterus salmoides). PLoS One 8 (3),
Feldmesser, E., Weller, J.I., Seroussi, E., Hulata, G., Ron, R., 2014. Identification of e59093. https://doi.org/10.1371/journal.pone.0059093.
male-specific amh duplication, sexually differentially expressed genes and microRNAs Migaud, H., Bell, G., Cabrita, E., McAndrew, B., Davie, A., Bobe, J., Herráez, M.P.,
at early embryonic development of Nile tilapia (Oreochromis niloticus). BMC Carrillo, M., 2013. Gamete quality and broodstock management in temperate fish.
Genomics 15, 774. https://doi.org/10.1186/1471-2164-15-774. Rev. Aquac. 5 (Suppl. 1), S194–S223. https://doi.org/10.1111/raq.12025.
Gallardo-Escárate, C., Valenzuela-Muñoz, V., Nuñez-Acuña, G., 2014. RNA-Seq analysis Miranda, A.C.L., Bazzoli, N., Rizzo, E., Sato, Y., 1999. Ovarian follicular atresia in two
using De novo Transcriptome assembly as a reference for the Salmon louse Caligus teleost species: a histological and ultrastructural study. Tissue Cell 31 (5), 480–488.
rogercresseyi. PLoS One 9 (4), e92239. https://doi.org/10.1371/journal.pone. Miranda, L.A., Chalde, T., Elisio, M., Strussmann, C.A., 2013. Effects of global warming on
0092239. fish reproductive endocrine axis, with special emphasis in pejerrey Odontesthes bo-
García-López, Á., Sánchez-Amaya, M.I., Prat, F., 2011. 2011. Targeted gene expression nariensis. Gen. Comp. Endocrinol. 192, 45–54. https://doi.org/10.1016/j.ygcen.
profiling in European sea bass (Dicentrarchus labrax, L.) follicles from primary growth 2013.02.034.
to late vitellogenesis. Comp. Biochem. Physiol. Part A 160, 374–380. https://doi.org/ Mirochnik, Y., Kwiatek, A., Volpert, O.V., 2008. Thrombospondin and apoptosis: mole-
10.1016/j.cbpa.2011.07.006. cular mechanisms and use for design of complementation treatments. Curr. Drug
Gardner, L.D., Jayasundara, N., Castilho, P.C., Block, B., 2012. Microarray gene expres- Targets 9 (10), 851–862.
sion profiles from mature gonad tissues of Atlantic bluefin tuna, Thunnus thynnus in Molina, A.M., Abril, N., Morales-Prieto, N., Monterde, J.G., Lora, A.J., Ayala, N., Moyano,
the Gulf of Mexico. BMC Genomics 13, 530. R., 2018. Evaluation of toxicological endpoints in female zebrafish after bisphenol a
Giraldez, A.J., 2005. MicroRNAs regulate brain morphogenesis in Zebrafish. Science 308, exposure. Food Chem. Toxicol. 112, 19–25. https://doi.org/10.1016/j.fct.2017.12.
833–838. 026.
Guzmán, J.M., Luckenbach, J.A., Swanson, P., 2013. Molecular characterization and Morais, R.D.V.S., Thomé, R.G., Lemos, F.S., Bazzoli, N., Rizzo, E., 2012. Autophagy and
quantification of sablefish (Anoplopoma fimbria) gonadotropins and their receptors: apoptosis interplay during follicular atresia in fish ovary: morphological and in-
reproductive dysfunction in female captive broodstock. Gen. Comp. Endocrinol. 193, munocytochemical study. Cell Tissue Res. 347, 467–478.
37–47. Nassauw, L.V., Tao, L., Harrisson, F., 1999. Distribution of apoptosis-related proteins in
Habibi, H.R., Andreu-Vieyra, C.V., 2007. Hormonal regulation of follicular atresia in the quail ovary during folliculogenesis: BCL-2, BAX and CPP32. Acta Histochem. 101,
teleost fish. In: Babin, P.J. (Ed.), The Fish Oocyte: From Basic Studies to 103–112.
Biotechnological Applications. Springer, Dordrecht, NL, pp. 235–253. Nelson, J.S., Grande, T.C., Wilson, M.V.H., 2016. Fishes of the World, 5th edition. John
Herpin, A., Adolfi, M.C., Nicol, B., Hinzmann, M., Schmidt, C., Klughammer, J., Engel, M., Wiley & Son, New Jersey.
Tanaka, M., Guiguen, Y., Schartl, M., 2013. Divergent expression regulation of gonad Nicol, B., Yano, A., Jouanno, E., Guerin, A., Fostier, A., Guiguen, Y., 2013. Follistatin is an
development genes in Medaka shows incomplete conservation of the downstream early player in rainbow trout ovarian differentiation and is both Colocalized with
regulatory network of vertebrate sex determination. Mol. Biol. Evol. 30 (10), aromatase and regulated by the Wnt pathway. Sex. Dev. https://doi.org/10.1159/
2328–2346. 000350687.
Hunter, J.R., Macewicz, B.J., 1985. Rates of atresia in the ovary of captive and wild Nieman, K.M., Kenny, H.A., Penicka, C.V., Ladanyi, A., Buell-Gutbrod, R., Zillhardt, M.R.,
northern anchovy; Engraulis mordax. Fish. Bull. 83 (2), 129–136. Romero, I.L., Carey, M.S., Mills, G.B., Hotamisligil, G.S., Yamada, S.D., Peter, M.E.,
Jalabert, B., 2005. Particularities of reproduction and oogenesis in teleost fish compared Gwin, K., Lengyel, E., 2011. Adipocytes promote ovarian cancer metastasis and
to mammals. Reprod. Nutr. Dev. 45, 261–279. provide energy for rapid tumor growth. Nat. Med. 17 (11), 1498–1503. https://doi.
Juanchich, A., Le Cam, A., Montfort, J., Guiguen, Y., Bobe, J., 2013. Identification of org/10.1038/nm.2492.
differentially expressed miRNAs and their potential targets during fish ovarian de- Nishimura, T., Nakamura, S., Tanaka, M., 2016. A structurally and functionally common
velopment. Biol. Reprod. 88 (5), 1–11. https://doi.org/10.1095/biolreprod.112. unit in testes and ovaries of Medaka (Oryzias latipes), a teleost fish. Sex. Dev. 10,
105361. 159–165.
Kaptaner, B., Ünal, G., 2011. Effects of 17a-Ethynylestradiol and Nonylphenol on liver Nourani, M.R., Owada, Y., Kitanaka, N., Abdelwahab, S.A., Iwasa, H., Sakagami, H.,
and gonadal apoptosis and histopathology in Chalcalburnus tarichi. Environ. Toxicol.. Spener, F., Kondo, H., 2005. Localization of epidermal-type fatty acid binding protein
https://doi.org/10.1002/tox.20585. in macrophages in advanced atretic follicles of adult mice. J. Mol. Histol. 36,
Breton, T.S., Kenterb, L.W., Greenlawa, K., Montgomerya, J., Goetzc, G.W., Berlinskyd, 391–400. https://doi.org/10.1007/s10735-005-9005-6.
D.L., Luckenbache, J.A., 2019. Initiation of sex change and gonadal gene expression Okuzawa, K., Gen, K., 2013. High water temperature impairs ovarian activity and gene
in black sea bass (Centropristis striata) exposed to exemestane, an aromatase inhibitor. expression in the brain–pituitary–gonadal axis in female red seabream during the
Comp. Biochem. Physiol. A 228, 51–61. https://doi.org/10.1016/j.cbpa.2018.10. spawning season. Gen. Comp. Endocrinol. 194, 24–30. https://doi.org/10.1016/j.
024. ygcen.2013.08.015.
Kitahashi, T., Parhar, I.S., 2013. Comparative aspects of kisspeptin gene regulation. Gen. Otis, J.P., Zeituni, E.M., Thierer, J.H., Anderson, J.L., Brown, A.C., Boehm, E.D.,
Comp. Endocrinol. 181, 197–202. https://doi.org/10.1016/j.ygcen.2012.10.003. Cerchione, D.M., Ceasrine, A.M., Avraham-Davidi, I., Tempelhof, H., Yaniv, K.,
Komine, M., 2018. Regulation of Expression of Keratins and their Pathogenic Roles in Farber, S.A., 2015. Zebrafish as a model for apolipoprotein biology: comprehensive
Keratinopathies, Keratin, Miroslav Blumenberg. IntechOpenhttps://doi.org/10. expression analysis and a role for ApoA-IV in regulating food intake. Dis. Model.
5772/intechopen.79140. Available from: https://www.intechopen.com/books/ Mech. 8, 295–309. https://doi.org/10.1242/dmm.018754.

6
P. González-Kother, et al. Marine Genomics xxx (xxxx) xxxx

Pinto, P.I.S., Andrade, A.R., Estêvão, M.D., Alvarado, M.V., Felip, A., 2017. Power DM, Tingaud-Sequeira, A., Chauvigné, F., Lozano, J., Agulleiro, M.J., Asensio, E., Cerdà, J.,
duplicated membrane estrogen receptors in the European sea bass (Dicentrarchus 2009. New insights into molecular pathways associated with flatfish ovarian devel-
labrax): phylogeny, expression and regulation throughout the reproductive cycle. J. opment and atresia revealed by transcriptional analysis. BMC Genomics 10, 434.
Steroid Biochem. Mol. Biol. https://doi.org/10.1016/j.jsbmb.2017.12.019. Valdebenito, I., Paiva, L., Berland, M., 2011. Atresia folicular en peces: una revisión.
Presslauer, C., Tilahun Bizuayehu, T., Kopp, M., Fernandes, J.M.O., Babiak, I., 2017. Arch. Med. Vet. 43, 11–25.
Dynamics of miRNA transcriptome during gonadal development of zebrafish. Sci. Villeneuve, D.L., Garcia-Reyero, N., Martinovic, D., Cavallin, J.E., Mueller, N.D.,
Rep. 7, 43850. Wehmas, L.C., Kahl, M.D., Linnum, A.L., Perkins, E.J., Ankley, G.T., 2010. Influence
Rideout, R.M., Tomkiewicz, J., 2011. Skipped spawning in fishes: more common than you of ovarian stage on transcript profiles in fathead minnow (Pimephales promelas) ovary
might think. Mar. Coast. Fish. 3, 176–189. tissue. Aquat. Toxicol. 98, 354–366.
Rizzo, E., Bazzoli, N., 1995. Follicular atresia in curimatá-pioa Prochilodus affinis Wang, Z., Gerstein, M., Snyder, M., 2009. RNA-Seq: a revolutionary tool for tran-
Reinhardt, 1874 (Pisces, Characiformes). Rev. Bras. Biol. 55 (4), 697–703. scriptomics. Nat. Rev. Genet. 10 (1), 57–63. https://doi.org/10.1038/nrg2484.
Rodríguez-Mari, A., Yan, Y.-L., BreMiller, R.A., Wilson, C., Cañestro, C., Postlethwait, Wienholds, E., 2005. MicroRNA expression in Zebrafish embryonic development. Science
J.H., 2005. Characterization and expression pattern of zebrafish anti-Müllerian hor- 309, 310–311.
mone (amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Wong, Q.W., Sun, M.A., Lau, S.W., Parsania, C., Zhou, S., Zhong, S., Ge, W., 2018.
Gene Expr. Patterns 5, 655–667. https://doi.org/10.1016/j.modgep.2005.02.008. Identification and characterization of a specific 13-miRNA expression signature
Ryu, Y.-W., Tanaka, R., Kasahara, A., Ito, Y., Hiramatsu, N., Todo, T., Sullivan, C.V., Hara, during follicle activation in the zebrafish ovary. Biol. Reprod. 98 (1), 42–53. https://
A., 2013. Molecular cloning and transcript expression of genes encoding two types of doi.org/10.1093/biolre/iox160.
lipoprotein lipase in the ovary of cutthroat trout, Oncorhynchus clarki. Zool. Sci. 30 Xiao, J., Zhong, H., Zhou, Y., Yu, F., Gao, Y., Luo, Y.J., Tang, Z.Y., Guo, Z.B., Guo, E.Y.,
(3), 224–237. https://doi.org/10.2108/zsj.30.224. Gan, X., Zhang, M., Zhang, Y.P., 2014. Identification and characterization of
Santos, H.B., Rizzo, E., Bazzoli, N., Sato, Y., Moro, L., 2005. Ovarian regression and microRNAs in ovary and testis of Nile tilapia (Oreochromis niloticus) by using solexa
apoptosis in the south American teleost Leporinus taeniatus Lütken (Characiformes, sequencing technology. PLoS One 9 (1), e868212014.
Anostomidae) from the São Francisco Basin. J. Fish Biol. 67, 1446–1459. https://doi. Yamamoto, Y., Luckenbach, J.A., Goetz, F.W., Young, G., Swanson, P., 2011. Disruption
org/10.1111/j.1095-8649.2005.00854.x. of the salmon reproductive endocrine axis through prolonged nutritional stress:
Schaffeld, M., Haberkamp, M., Braziulis, E., Lieb, B., Mark, J., 2002. Type II keratin changes in circulating hormone levels and transcripts for ovarian genes involved in
cDNAs from the rainbow trout: implications for keratin evolution. Differentiation 70, steroidogenesis and apoptosis. Gen. Comp. Endocrinol. 172, 331–343. https://doi.
292–299. org/10.1016/j.ygcen.2011.03.017.
Shibata, Y., Iwamatsu, T., Suzuki, N., Young, G., Naruse, K., Nagahama, Y., Yoshikuni, M., Yamamoto, Y., Luckenbach, J.A., Young, G., Swanson, P., 2016. Alterations in gene ex-
2012. An oocyte-specific astacin family protease, alveolin, is released from cortical pression during fasting-induced atresia of early secondary ovarian follicles of coho
granules to trigger egg envelope hardening during fertilization in medaka (Oryzias salmon, Oncorhynchus kisutch. Comp. Biochem. Physiol. Part A 201, 1–11. https://
latipes). Dev. Biol. 372, 239–248. https://doi.org/10.1016/j.ydbio.2012.09.016. doi.org/10.1016/j.cbpa.2016.06.016.
Silva, F.F.G., Slotte, A., Johannessen, A., Kennedy, J.S., Kjesbu, O.S., 2013. Strategies for Yan, W., Zhou, S., Shen, W., et al., 2018. Suppression of SEMA6C promotes preantral
partition between body growth and reproductive investment in migratory and sta- follicles atresia with decreased cell junctions in mice ovaries. J. Cell. Physiol. 234,
tionary populations of spring-spawning Atlantic herring (Clupea harengus L.). Fish. 4934–4943. https://doi.org/10.1002/jcp.27294.
Res. 138, 71–79. https://doi.org/10.1016/j.fishres.2012.07.013. Zanuy, S., Prat, F., Carrillo, M., Bromage, N., 1995. Effects of constant photoperiod on
Sullivan, C.V., Yilmaz, S.O., 2018. Vitellogenesis and yolk protein, fish. Encycl. Reprod. 6, spawning and plasma 17β-oestradiol levels of sea bass (Dicentrarchus labrax L.).
266–277. https://doi.org/10.1016/B978-0-12-809633-8.20567-0. Aquat. Living Resour. 8, 147–152.
Thomas, F.H., Wilson, H., Silvestri, A., Fraser, H.M., 2008. Thrombospondin-1 expression Zhang, J., Liu, W., Jin, Y., Jia, P., Jia, K., Yi, M., 2017. MiR-202-5p is a novel germ plasm-
is increased during follicular atresia in the primate ovary. Endocrinology 149 (1), specific microRNA in zebrafish. Sci. Rep. 7. https://doi.org/10.1038/s41598-017-
185–192. https://doi.org/10.1210/en.2007-0835. 07675-x.
Thomé, R.G., Santos, H.B., Arantes, F.P., Domingos, F.F.T., Bazzoli, N., Rizzo, E., 2009. Zohar, Y., Muñoz-Cueto, J.A., Elizur, A., Kah, O.I., 2010. Neuroendocrinology of re-
Dual roles for autophagy during follicular atresia in fish ovary. Autophagy 51, production in teleost fish. Gen. Comp. Endocrinol. 165, 438–455.
117–119.