Activation of NF-κB Protein Prevents the Transition from Juvenile Ovary to Testis and Promotes Ovarian Development in Zebrafish

Pradhan, Ajay; Khalaf, Hazem; Ochsner, Scott A.; Sreenivasan, Rajini; Koskinen, Jarno; Karlsson, Marie; Karlsson, Johannes; McKenna, Neil J.; Orbán, László; Olsson, Per‐Erik

doi:10.1074/jbc.m112.386284

Cited by 64 publications

(36 citation statements)

References 46 publications

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“…Min et al [67] found that the inhibition of NF-kB activation decreases levels of the pro-inflammatory cytokines IL-1b, IL-8 and TNF-a in human mast cell lines. It was reported that NF-kB P65 and NF-kB P52 are the subunits of NF-kB in fish [68]. In the present study, compared with low or high levels of protein, we found that at the optimal levels of dietary protein down-regulated NF-kB P65 and NF-kB P52 mRNA levels in the gills of grass carp.…”

Section: Optimal Level Of Dietary Protein Attenuated Inflammatory Ressupporting

confidence: 57%

Effects of dietary protein levels on the disease resistance, immune function and physical barrier function in the gill of grass carp ( Ctenopharyngodon idella ) after challenged with Flavobacterium columnare

Feng

Jiang

et al. 2016

Fish & Shellfish Immunology

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Section: Optimal Level Of Dietary Protein Attenuated Inflammatory Ressupporting

confidence: 57%

Effects of dietary protein levels on the disease resistance, immune function and physical barrier function in the gill of grass carp ( Ctenopharyngodon idella ) after challenged with Flavobacterium columnare

Feng

Jiang

et al. 2016

Fish & Shellfish Immunology

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“…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. On the other hand, genes related to testis differentiation such as amh and dmrt1 were up-regulated, together with male-related pathways such as the calcium signaling pathway in cardiac muscle contraction, which regulates Leydig cell steroidogenesis in mice (54).…”

Section: Discussionmentioning

confidence: 70%

“…In contrast, ovarian differentiation continues in the future females (25), with an increase in cytoplasm volume of oocytes at around 60 dpf. Transcriptomic analysis of zebrafish sex differentiation has shown that apoptosis (24), activated by the p53 signaling pathway (26), is required for testis differentiation, whereas up-regulation of the canonical Wnt and NF-κB signaling pathways is needed for ovarian differentiation (27,28).…”

mentioning

confidence: 99%

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.

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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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“…Answers likely lie in environmental factors and background genetic features that affect the strength of a meiotic oocyte-derived pro-female signal that inhibits oocyte apoptosis, probably by maintaining aromatase production (Slanchev et al 2005;Houwing et al 2007;Wang et al 2007;Siegfried and Nusslein-Volhard 2008;Rodriguez-Mari et al 2010Rodríguez-Marí and Postlethwait 2011;Pradhan et al 2012;Dranow et al 2013). In general, harsh conditions, including high density and poor nutrition, tend to promote male development (Walker-Durchanek 1980;Pelegri and Schulte-Merker 1999;Shang et al 2006;Lawrence et al 2008;Abozaid et al 2011Abozaid et al , 2012Liew et al 2012;Villamizar et al 2012).…”

Section: Domesticated Zebrafish Strains Lack a Single Strong Sexlinkementioning

confidence: 99%

Wild Sex in Zebrafish: Loss of the Natural Sex Determinant in Domesticated Strains

et al. 2014

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Sex determination can be robustly genetic, strongly environmental, or genetic subject to environmental perturbation. The genetic basis of sex determination is unknown for zebrafish (Danio rerio), a model for development and human health. We used RADtag population genomics to identify sex-linked polymorphisms. After verifying this "RAD-sex" method on medaka (Oryzias latipes), we studied two domesticated zebrafish strains (AB and TU), two natural laboratory strains (WIK and EKW), and two recent isolates from nature (NA and CB). All four natural strains had a single sex-linked region at the right tip of chromosome 4, enabling sex genotyping by PCR. Genotypes for the single nucleotide polymorphism (SNP) with the strongest statistical association to sex suggested that wild zebrafish have WZ/ZZ sex chromosomes. In natural strains, "male genotypes" became males and some "female genotypes" also became males, suggesting that the environment or genetic background can cause female-to-male sex reversal. Surprisingly, TU and AB lacked detectable sex-linked loci. Phylogenomics rooted on D. nigrofasciatus verified that all strains are monophyletic. Because AB and TU branched as a monophyletic clade, we could not rule out shared loss of the wild sex locus in a common ancestor despite their independent domestication. Mitochondrial DNA sequences showed that investigated strains represent only one of the three identified zebrafish haplogroups. Results suggest that zebrafish in nature possess a WZ/ZZ sex-determination mechanism with a major determinant lying near the right telomere of chromosome 4 that was modified during domestication. Strains providing the zebrafish reference genome lack key components of the natural sex-determination system but may have evolved variant sex-determining mechanisms during two decades in laboratory culture.. . .researchers using standard lines of zebrafish that have long been maintained in laboratories are often plagued by severe sex ratio distortions. . .. C. Lawrence, J. P. Ebersole, and R. V. Kesseli (2008) C ONSIDERING the fundamental importance of sex for species propagation, it is surprising that primary sexdetermining mechanisms are not strongly conserved among animal taxa (Bull 1983;Charlesworth 1996;Ming et al. 2011;Bachtrog et al. 2014). Closely related species or even populations of the same species can have different sexdetermining mechanisms (Takehana et al. 2007;Ross et al. 2009;Kobayashi et al. 2013;Heule et al. 2014;Larney et al. 2014). Zebrafish (Danio rerio) is a popular model for studies of vertebrate development, behavior, physiology, evolution, disease, and human health (Mills et al. 2007;Seth et al. 2013;Braasch et al. 2014;Ota and Kawahara 2014;Wilkinson et al. 2014), but researchers struggle with highly variable and distorted sex ratios, and investigations into the genetic nature of zebrafish sex determination are conflicting. To help understand these issues, we conducted a population genomic study of sex determination in multiple zebrafish strains. Zebrafish exhibit...

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Activation of NF-κB Protein Prevents the Transition from Juvenile Ovary to Testis and Promotes Ovarian Development in Zebrafish

Cited by 64 publications

References 46 publications

Effects of dietary protein levels on the disease resistance, immune function and physical barrier function in the gill of grass carp ( Ctenopharyngodon idella ) after challenged with Flavobacterium columnare

Effects of dietary protein levels on the disease resistance, immune function and physical barrier function in the gill of grass carp ( Ctenopharyngodon idella ) after challenged with Flavobacterium columnare

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

Wild Sex in Zebrafish: Loss of the Natural Sex Determinant in Domesticated Strains

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