Heat shock factor 1 protects germ cell proliferation during early ovarian differentiation in medaka

Furukawa, Fumiya; Hamasaki, Shin; Hara, Seiji; Uchimura, Tomoya; Shiraishi, Eri; Osafune, Natsumi; Takagi, Hisanori; Yazawa, Takashi; Kamei, Yasuhiro; Kitano, Takeshi

doi:10.1038/s41598-019-43472-4

Cited by 20 publications

(14 citation statements)

References 37 publications

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“…Though not well studied in the context of sex determination, heat shock factors and proteins have been implicated in female sex determination in mammals and fish, and may also play a conserved role in the ovarian pathway in P. vitticeps (79,124–127). Surprisingly, only one gene associated with canonical heat shock response ( HSP40 , also known as DNAJC28 ) was differentially expressed following exposure to high temperature in stage 6 ZZf females compared to ZWf embryos (Additional file S3).…”

Section: Resultsmentioning

confidence: 99%

Two transcriptionally distinct pathways drive female development in a reptile with both genetic and temperature dependent sex determination

Whiteley

Holleley

Wagner

et al. 2021

Preprint

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How temperature determines sex remains unknown. A recent hypothesis proposes that conserved cellular mechanisms (calcium and redox; CaRe status) sense temperature and identify genes and regulatory pathways likely to be involved in driving sexual development. We take advantage of the unique sex determining system of the model organism, Pogona vitticeps, to assess predictions of this hypothesis. P. vitticeps has ZZ male: ZW female sex chromosomes whose influence can be overridden in genetic males by high temperatures, causing male-to-female sex reversal. We compare a developmental transcriptome series of ZWf females and temperature sex reversed ZZf females. We demonstrate that early developmental cascades differ dramatically between genetically driven and thermally driven females, later converging to produce a common outcome (ovaries). We show that genes proposed as regulators of thermosensitive sex determination play a role in temperature sex reversal. Our study greatly advances the search for the mechanisms by which temperature determines sex.

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Section: Resultsmentioning

confidence: 99%

Two transcriptionally distinct pathways drive female development in a reptile with both genetic and temperature dependent sex determination

Whiteley

Holleley

Wagner

et al. 2021

Preprint

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“…Total RNA was extracted from the gonad regions (20 pooled samples) of XX larvae at 0 dph using NucleoSpin RNA XS (Takara Bio, Shiga, Japan) according to the manufacturer’s protocol 44 . The XX larvae untreated (control), or treated with HT or cortisol from 0 dpf to 0 dph were selected by the existence of leucophores and the gonad regions containing the guts were cut out under a stereo microscope MZ (Leica Microsystems, Wetzlar, Germany) as described previously 15 .…”

Section: Methodsmentioning

confidence: 99%

Peroxisome proliferator-activated receptor alpha is involved in the temperature-induced sex differentiation of a vertebrate

Hara

Furukawa

Mukai

et al. 2020

Sci Rep

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Medaka (Oryzias latipes) is a teleost fish with an XX/XY sex determination system, similar to that of mammals. However, under high temperature conditions, XX medaka is masculinised by elevation of cortisol, the major teleost glucocorticoid. in this study, to identify novel factors in the gonads acting downstream from cortisol during sexual differentiation, we performed RNA sequencing (RNA-seq) analysis using the gonadal regions of larvae reared at normal temperature with and without cortisol, and at high temperature. The RNA-seq and real-time PCR analyses showed that expression of some peroxisome proliferator-activated receptor α (PPARα) signalling-targeted genes was increased by cortisol. PPARα agonist treatment induced masculinisation of XX medaka in some cases, and co-treatment of the agonist with cortisol further induced masculinisation, whereas treatment of pparaa knockout medaka with cortisol or the agonist did not induce masculinisation. this study provides the first evidence that PPARα is involved in environmental sex determination in vertebrates. Many vertebrates have males and females that reproduce sexually. Sex is genotypically determined in many species, but sex determination is greatly affected by ambient temperature in poikilothermic vertebrates, including reptiles, amphibians, and fish 1. Furthermore, environmental factors, such as pH 2 , density 3 , and social factors 4 , are suggested to override genetic sex determination in some teleost fish. However, the molecular mechanisms of environmental sex determination in these species remain poorly understood. Medaka (Oryzias latipes) is a small teleost fish that offers many advantages, including the availability of many useful strains 5. Transgenic (Tg) techniques and the gene knockout systems using clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 (Cas9), are established 6-8. Moreover, the sex-determining gene dmy (also known as dmrt1bY) on the Y chromosome has been identified in this fish 9. Therefore, medaka is a useful animal model for vertebrate genetic analysis of the sex determination and differentiation. The first appearance of morphological sex differentiation in medaka is the difference in the number of germ cells before hatching, as germ cells in genetic females (XX) undergo a rapid proliferation and subsequently initiate oogenesis while they remain quiescent in genetic males (XY) 10,11. High temperature (HT) treatment during the sex differentiation inhibits germ cell proliferation and oocyte development in XX medaka, and causes masculinisation 12-14. HT also causes masculinisation through elevating the levels of cortisol, the major teleost glucocorticoid 15. Furthermore, exposure of XX medaka to cortisol or HT increases expression of gonadal soma-derived growth factor (gsdf) and decreases expression of cytochrome P450 family 19 subfamily A member 1a (cyp19a1a) by 5 days post-hatching (dph) 16. However, it remains unclear how HT-elevated cortisol induces the masculinisation of XX medaka. Cortisol...

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“…Furukawa et al [54] shows that the HSF1 is a very important regulator in the ovarian differentiation of Medaka. They made a HSF1 knock-out animal and found that HSF1 protects the female germ cells under heat stress.…”

Section: Discussionmentioning

confidence: 99%

Examination the effect of post-hatch heat-treatment and heat-stress in Transylvanian Naked Neck chicken

Tóth

Szabadi

Lázár

et al. 2020

Preprint

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Background One of the most critical global problem nowadays is the increased environmental temperature. Agriculture is very susceptible to this adverse effect because the productivity of animals and poultry decreased. Although several studies reported the effects of heat-stress in chicken, the expression profile of heat-shock proteins and heat shock factors was not investigated in the gonads and germ cells of Transylvanian Naked Neck chickens. Methods In the first experiment, 24 hours after hatching 80 chicks were heat treated on 38.5oC ambient temperature with 60% humidity for 12 hours. After maturation, their primary productivity parameters, such as egg production, abnormalities in embryo development, sperm quantity, concentration, and motility were studied following two weeks of heat-stress on 30 °C room temperature. In the second experiment, the thermal manipulation of 60 chicks was the same but 15 treated and 15 control chicks were sacrificed immediately after the treatment. The other 15–15 chickens were raised to maturity. Expression levels for two heat-shock proteins and four heat shock factors were determined by real-time PCR in the gonads of heat-treated and heat-stressed chickens. Results We found that the heat-treated layers had significantly higher egg production than the control group in heat-stressed conditions. In cockerels, the sperm quality did not differ significantly between the heat-treated and heat-stressed group and the heat-stressed but not heat-treated group. We examined the expression pattern of HSPs and HSFs in the gonads. We found that the expression of HSP90 and HSF4 increased significantly (p < 0.05) in heat-treated female chick gonads but in adult females the expression of HSF2 and HSF3 were significantly lower compared to the control. In case of adult heat-treated males, the HSP70, HSF1 and HSF3 expression levels showed a significant increase in both gonads, compared to the control expression levels (P < 0.05). Conclusion Heat shock proteins and heat-shock factors protect cells against different stressors, including heat stress. Our findings show a significant effect on egg production but not on the sperm quality after post-hatch heat treatment in heat stress condition. The presented significant differences might be related to the increased expression level of HSP90 and HSF4 in heat-treated chickens.

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Heat shock factor 1 protects germ cell proliferation during early ovarian differentiation in medaka

Cited by 20 publications

References 37 publications

Two transcriptionally distinct pathways drive female development in a reptile with both genetic and temperature dependent sex determination

Two transcriptionally distinct pathways drive female development in a reptile with both genetic and temperature dependent sex determination

Peroxisome proliferator-activated receptor alpha is involved in the temperature-induced sex differentiation of a vertebrate

Examination the effect of post-hatch heat-treatment and heat-stress in Transylvanian Naked Neck chicken

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