Expression Profiling of Wnt Signaling Genes during Gonadal Differentiation and Gametogenesis in Rainbow Trout

Nicol, Barbara; Guiguen, Yann

doi:10.1159/000334515

Cited by 60 publications

(34 citation statements)

References 77 publications

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“…In fish, masculinization by elevated temperature usually involves down-regulation of profemale genes, such as cyp19a1a and foxl2, and up-regulation of promale genes, such as dmrt1 or amh (8)(9)(10)(11)(12)(13)(14). In accordance with this general pattern, the FHT2 females with a male-like gonadal transcriptome exhibited down-regulation of both key profemale genes such as cyp19a1a and vtg5 as well as downregulation of profemale pathways such as oocyte meiosis, progesterone-mediated oocyte maturation, canonical Wnt signaling (28,53), and Fanconi anemia (26). Another profemale pathway, the NF-κB pathway, involved in blocking apoptosis through an inflammatory process during ovarian development (27), was not affected, although some of its genes (e.g., bcl2, nfkb, tradd) were down-regulated.…”

Section: Discussionmentioning

confidence: 66%

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

Ribas

Liew

Díaz

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

120

136

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Understanding environmental influences on sex ratios is important for the study of the evolution of sex-determining mechanisms and for evaluating the effects of global warming and chemical pollution. Fishes exhibit sexual plasticity, but the underlying mechanisms of environmental effects on their reproduction are unclear even in the well-established teleost research model, the zebrafish. Here we established the conditions to study the effects of elevated temperature on zebrafish sex. We showed that sex ratio response to elevated temperature is family-specific and typically leads to masculinization (female-to-male sex reversal), resulting in neomales. These results uncovered genotype-by-environment interactions that support a polygenic sex determination system in domesticated (laboratory) zebrafish. We found that some heat-treated fish had gene expression profiles similar to untreated controls of the same sex, indicating that they were resistant to thermal effects. Further, most neomales had gonadal transcriptomes similar to that of regular males. Strikingly, we discovered heat-treated females that displayed a normal ovarian phenotype but with a "male-like" gonadal transcriptome. Such major transcriptomic reprogramming with preserved organ structure has never been reported. Juveniles were also found to have a male-like transcriptome shortly after exposure to heat. These findings were validated by analyzing the expression of genes and signaling pathways associated with sex differentiation. Our results revealed a lasting thermal effect on zebrafish gonads, suggesting new avenues for detection of functional consequences of elevated temperature in natural fish populations in a global warming scenario.A major paradox in developmental biology is the lack of conservation of sex-determining mechanisms even in closely related taxa (1). Thus, in mammals and birds, sex is genetically canalized by a chromosomal sex determination (CSD) system of male (XX/XY in mammals) or female (ZW/ZZ in birds) heterogamety, driven by the action of a master sex-determining gene: sry in mammals and dmrt1 in birds (1). In contrast, fish sex can be very plastic, with the combination of genetic and environmental influences (2). In addition to fish species with CSD, there are species with polygenic sex determination (PSD), in which sex depends on the combined action of several promale and profemale genetic factors, and species with temperature-dependent sex determination (TSD) (3). Understanding how the environment influences sex ratios in vertebrates is of fundamental importance in the study of the evolution of sex-determining mechanisms (4, 5). It is also of practical relevance in evaluating the effects of climate change and chemical pollution (6, 7).The effects of temperature on gene expression during sex differentiation have been investigated in different teleost species, including the African catfish, Clarias gariepinus (8), European sea bass, Dicentrarchus labrax (9, 10), Japanese flounder, Paralichthys olivaceus (11), pejerrey, Odontesthes...

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Section: Discussionmentioning

confidence: 66%

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

Ribas

Liew

Díaz

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

120

136

View full text Add to dashboard Cite

show abstract

“…Thus, gonadal differentiation may involve other members of the Wnt gene family. Indeed, other wnt genes have been shown to display a sex-specific expression at different stages of development in the rainbow trout (Nicol & Guiguen 2011). Moreover, transgenic inhibition of wnt signaling results in male-biased sex ratios, suggesting that Wnt signaling is a conserved key pathway during gonadal differentiation in zebrafish (Sreenivasan et al 2014).…”

Section: Teleost Fishesmentioning

confidence: 99%

R-spondin1, WNT4, and the CTNNB1 signaling pathway: strict control over ovarian differentiation

Chassot¹,

Gillot²,

Chaboissier³

2014

Reproduction

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Sex differentiation is a unique developmental process. Starting from a bipotential gonad, it gives rise to the ovary and the testis, two highly specialized organs that differ morphologically and physiologically despite sharing common reproductive and endocrine functions. This highlights the specific plasticity of the gonadal precursors and the existence of complex antagonistic genetic regulation. Mammalian sex determination is controlled by paternal transmission of the Y-linked gene, sex-determining region Y (SRY). Using mouse models, it has been shown that the main role of Sry is to activate the expression of the transcription factor Sox9; either one of these two genes is necessary and sufficient to allow testicular development through Sertoli cell differentiation. Thus, defects in SRY/Sry and/or SOX9/Sox9 expression result in male-to-female sex reversal of XY individuals. Molecular mechanisms governing ovarian differentiation remained unknown for a long time, until the discovery of the roles of R-spondin1 (RSPO1) and WNT4. In XX individuals, activation of the b-catenin signaling pathway by the secreted proteins RSPO1 and WNT4 is required to allow granulosa cell differentiation and, in turn, ovarian differentiation. Thus, mutations in RSPO1 result in female-to-male sex reversal of XX patients, and mouse models have allowed the identification of genetic cascades activated by RSPO1 and WNT4 to regulate ovarian development. In this review, we will discuss the respective roles of RSPO1, WNT4, and the b-catenin signaling pathway during ovarian differentiation in mice.Reproduction (2014) 148 R97-R110

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“…It was well documented that estrogen is necessary for the maintenance of Rspo1 expression in a direct or indirect manner in oviparous species [19]. Recent studies revealed that Wnt signaling is implicated in multiple processes of male and female gonadal development in rainbow trout [28]. Therefore, it is essential and critical to explore whether Rspo/Wnt/β-catenin signaling pathway plays a key role in fish sex determination and differentiation, just like its role in mammals.…”

Section: Introductionmentioning

confidence: 99%

R-spondins are involved in the ovarian differentiation in a teleost, medaka (Oryzias latipes)

Zhou

Charkraborty

et al. 2012

BMC Dev Biol

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BackgroundIn mammals, R-spondin (Rspo), an activator of the Wnt/β-catenin signaling pathway, has been shown to be involved in ovarian differentiation. However, the role of the Rspo/Wnt/β-catenin signaling pathway in fish gonads is still unknown.ResultsIn the present study, full-length cDNAs of Rspo1, 2 and 3 were cloned from the gonads of medaka (Oryzias latipes). The deduced amino acid sequences of mRspo1-3 were shown to have a similar structural organization. Phylogenetic analysis showed that Rspo1, 2 and 3 were specifically clustered into three distinct clads. Tissue distribution revealed that three Rspo genes were abundantly expressed in the brain and ovary. Real-time PCR analysis around hatching (S33-5dah) demonstrated that three Rspo genes were specifically enhanced in female gonads from S38. In situ hybridization (ISH) analysis demonstrated that three Rspo genes were expressed in the germ cell in ovary, but not in testis. Fluorescence multi-color ISH showed that Rspo1 was expressed in both somatic cells and germ cells at 10dah. Exposure to ethinylestradiol (EE2) in XY individuals for one week dramatically enhanced the expression of three Rspo genes both at 0dah and in adulthood.ConclusionsThese results suggest that the Rspo-activating signaling pathway is involved in the ovarian differentiation and maintenance in medaka.

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Expression Profiling of Wnt Signaling Genes during Gonadal Differentiation and Gametogenesis in Rainbow Trout

Cited by 60 publications

References 77 publications

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

R-spondin1, WNT4, and the CTNNB1 signaling pathway: strict control over ovarian differentiation

R-spondins are involved in the ovarian differentiation in a teleost, medaka (Oryzias latipes)

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