An aromatase inhibitor or high water temperature induce oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal

Uchida, Daisuke; Yamashita, Michiaki; Kitano, Takeshi; Iguchi, Taisen

doi:10.1016/s1095-6433(03)00178-8

Cited by 256 publications

(208 citation statements)

References 23 publications

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“…We found that elevating the temperature from 28°C to 33°C increased the somatic growth rate, but this growth increase was not the key determinant of sexual differentiation in our study (i.e., it did not favor the development of females). Instead, male-skewed sex ratios in the elevated temperature and/or clotrimazole exposure treatments appeared to be mediated by the inhibition of P450(CYP)19 aromatase, as has been found in other studies (39,40,42). Gene expression of cyp19a1a encoding aromatase was up-regulated in the few females remaining in the inbred, elevated temperature, and/or high-level clotrimazole exposure treatments, and we hypothesize that this up-regulation was the result of a compensatory response to P450(CYP)19 aromatase inhibition in these individuals.…”

Section: Discussionsupporting

confidence: 59%

“…The zebrafish is a freshwater species native to the Indian subcontinent and has been studied widely as a model animal in biomedical and environmental science (36)(37)(38). Importantly, the sex-determining mechanism in zebrafish is known to be modified by environmental factors, and independent exposures to elevated water temperatures (21,39), and to chemicals that inhibit aromatase, have been shown to induce male development in this species (39,40). The enzyme aromatase [cytochrome P450(CYP)19] mediates the conversion of male hormones (androgens) to female hormones (estrogens), and thus plays a pivotal role in sex assignment in zebrafish and other vertebrates (41).…”

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confidence: 99%

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Climate change and pollution speed declines in zebrafish populations

Brown

Owen

Peters

et al. 2015

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

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Endocrine disrupting chemicals (EDCs) are potent environmental contaminants, and their effects on wildlife populations could be exacerbated by climate change, especially in species with environmental sex determination. Endangered species may be particularly at risk because inbreeding depression and stochastic fluctuations in male and female numbers are often observed in the small populations that typify these taxa. Here, we assessed the interactive effects of water temperature and EDC exposure on sexual development and population viability of inbred and outbred zebrafish (Danio rerio). Water temperatures adopted were 28°C (current ambient mean spawning temperature) and 33°C (projected for the year 2100). The EDC selected was clotrimazole (at 2 μg/L and 10 μg/L), a widely used antifungal chemical that inhibits a key steroidogenic enzyme [cytochrome P450(CYP19) aromatase] required for estrogen synthesis in vertebrates. Elevated water temperature and clotrimazole exposure independently induced maleskewed sex ratios, and the effects of clotrimazole were greater at the higher temperature. Male sex ratio skews also occurred for the lower clotrimazole exposure concentration at the higher water temperature in inbred fish but not in outbred fish. Population viability analysis showed that population growth rates declined sharply in response to male skews and declines for inbred populations occurred at lower male skews than for outbred populations. These results indicate that elevated temperature associated with climate change can amplify the effects of EDCs and these effects are likely to be most acute in small, inbred populations exhibiting environmental sex determination and/or differentiation.

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Section: Discussionsupporting

confidence: 59%

mentioning

confidence: 99%

Climate change and pollution speed declines in zebrafish populations

Brown

Owen

Peters

et al. 2015

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

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“…Therefore, the balance between estrogens and androgens is crucial for sex differentiation in fish; the inhibition of aromatase suppresses estrogen formation, thereby disturbing the normal sex ratio and resulting in a male-dominant population. In a previous study, female zebrafish larvae that were exposed to an aromatase inhibitor (fadrozole) showed gonadal masculinization (Uchida et al, 2004;Fenske and Segner, 2004), and the aromatase inhibitor suppressed the CYP19 gene expression in the gonads of these genetically masculinized females. This finding shows the association between the CYP19 aromatase enzyme activity and the differential regulation of CYP19A and CYP19B expression.…”

Section: Discussionmentioning

confidence: 89%

Chronic exposure to environmental levels of tribromophenol impairs zebrafish reproduction

Deng

Liu

et al. 2010

Toxicology and Applied Pharmacology

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“…In domesticated zebrafish, the effects of elevated temperature have been studied after exposure periods concerning embryos (35), juveniles (36,37), or development until adults (38,39). In agreement with the general pattern in fish (18), elevated temperatures result in a higher number of males, although, surprisingly, one study reported more females (40).…”

mentioning

confidence: 78%

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.

119

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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An aromatase inhibitor or high water temperature induce oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal

Cited by 256 publications

References 23 publications

Climate change and pollution speed declines in zebrafish populations

Climate change and pollution speed declines in zebrafish populations

Chronic exposure to environmental levels of tribromophenol impairs zebrafish reproduction

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

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