Treffer: Mild increase of temperature from the thermoneutral zone inhibits reproductive activation in Syrian hamsters through epigenetic inhibition.
Title:
Mild increase of temperature from the thermoneutral zone inhibits reproductive activation in Syrian hamsters through epigenetic inhibition.
Authors:
Hnamler L; Department of Zoology, Mizoram University, Aizawl, Mizoram, India., Trivedi AK; Department of Zoology, Mizoram University, Aizawl, Mizoram, India.
Source:
Journal of neuroendocrinology [J Neuroendocrinol] 2025 Nov; Vol. 37 (11), pp. e70095. Date of Electronic Publication: 2025 Oct 01.
Publication Type:
Journal Article
Language:
English
Journal Info:
Publisher: Wiley & Sons Country of Publication: United States NLM ID: 8913461 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-2826 (Electronic) Linking ISSN: 09538194 NLM ISO Abbreviation: J Neuroendocrinol Subsets: MEDLINE
Imprint Name(s):
Publication: <2010->: Malden, MA : Wiley & Sons
Original Publication: Eynsham, Oxon, UK : Oxford University Press, c1989-
Original Publication: Eynsham, Oxon, UK : Oxford University Press, c1989-
MeSH Terms:
References:
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Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA. Fingerprints of global warming on wild animals and plants. Nature. 2003;421:57‐60.
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Gatter W. Timing and patterns of visible autumn migration: can effects of global warming be detected? J Ornithol. 1992;133(4):427‐436.
Høye TT, Post E, Schmidt NM, Trøjelsgaard K, Forchhammer MC. Shorter flowering seasons and declining abundance of flower visitors in a warmer Arctic. Nature Climate Change. 2013;3(8):759‐763.
Roslin T, Antao L, Hallfors M, et al. Phenological shifts of abiotic events, producers and consumers across a continent. Nat Clim Chang. 2021;11(3):241‐248.
Parmesan C, Ryrholm N, Stefanescu C, et al. Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature. 1999;399(6736):579‐583.
Parmesan C. Climate and species' range. Nature. 1996;382:765‐766.
Menzel A, Estrella N. In: Walther G‐R, Burga CA, Edwards PJ, eds. “Fingerprints” of Climate Change‐Adapted Behaviour and Shifting Species Ranges. Kluwer Academic; 2001:123‐137.
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Yaeram J, Setchell BP, Maddocks S. Effect of heat stress on the fertility of male mice in vivo and in vitro. Reprod Fertil Dev. 2006;18:647‐653.
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Zhu GD, Xue M, Luo Y, et al. Effect of short‐term heat shock and physiological responses to heat stress in two Bradysia adults, Bradysia odoriphaga and Bradysia difformis. Sci Rep. 2017;7:13381.
Renthlei Z, Hmar L, Kumar Trivedi A. High temperature attenuates testicular responses in tree sparrow (Passer montanus). Gen Comp Endocrinol. 2021;301:113654.
Renthlei Z, Mongku M, Yatung S, Lalpekhlui R, Trivedi AK. High temperature during photorefractory stage attenuates photoperiodic responses during photostimulatory stage in male tree sparrows (Passer montanus). Theriogenology Wild. 2024;5:100100.
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Yasuo S, Watanabe M, Nakao N, Takagi T, Follett BK. The reciprocal switching of two thyroid hormone‐activating and ‐inactivating enzyme genes is involved in the photoperiodic gonadal response of Japanese quail. Endocrinology. 2005;146:2551‐2554.
Stevenson TJ, Prendergast BJ. Reversible DNA methylation regulates seasonal photoperiodic time measurement. Proc Natl Acad Sci U S A. 2013;110(41):16651‐16656.
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Wood S, Loudon A. The pars tuberalis: the site of the circannual clock in mammals? Gen Comp Endocrinol. 2017;258:222‐235.
Bartzen‐Sprauer J, Klosen P, Ciofi P, Mikkelsen JD, Simonneaux V. Photoperiodic co‐regulation of kisseptin, neurokinin B and dynorphin in the hypothalamus of a seasonal rodent. J Neuroendocrinol. 2014;26(8):510‐520.
Revel FG, Saboureau M, Masson‐P'evet M, P'evet P, Mikkelsen JD, Simonneaux V. Kisspeptin mediates the photoperiodic control of reproduction in hamsters. Curr Biol. 2006;16:1730‐1735.
Ansel L, Bentsen AH, Ancel C, Bolborea M, Klosen P. Peripheral kisspeptin reverses short photoperiod‐induced gonadal regression in Syrian hamsters by promoting GNRH release. Reproduction. 2011;142:417‐425.
Revel FG, Saboureau M, Pévet P, Simonneaux V, Mikkelsen JD. RFamide‐related peptide gene is a melatonin‐driven photoperiodic gene. Endocrinology. 2008;149(3):902‐912.
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Kotula‐Balak M, Pawlicki P, Milon A, et al. The role of G‐protein‐coupled membrane estrogen receptor in mouse Leydig cell function‐in vivo and in vitro evaluation. Cell Tissue Res. 2018;374(2):389‐412.
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Yatung S, Trivedi AK. Daily and seasonal changes in steroidogenic markers in the hypothalamus and testes of tree sparrow (Passer montanus). J Neuroendocrinol. 2024;37:e13478.
Yatung S, Trivedi AK. Time‐ and season‐dependent changes in the steroidogenic markers in female tree sparrow (Passer montanus). Photochem Photobiol Sci. 2025;24(4):607‐628.
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Thackeray SJ, Sparks TH, Frederiksen M, et al. Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob Change Biol. 2010;16:3304‐3313.
H¨allfors MH, Ant~ao LH, Itter M, et al. Shifts in timing and duration of breeding for 73 boreal bird species over four decades. Proc Natl Acad Sci. 2020;117(31):18557‐18565.
Gatter W. Timing and patterns of visible autumn migration: can effects of global warming be detected? J Ornithol. 1992;133(4):427‐436.
Høye TT, Post E, Schmidt NM, Trøjelsgaard K, Forchhammer MC. Shorter flowering seasons and declining abundance of flower visitors in a warmer Arctic. Nature Climate Change. 2013;3(8):759‐763.
Roslin T, Antao L, Hallfors M, et al. Phenological shifts of abiotic events, producers and consumers across a continent. Nat Clim Chang. 2021;11(3):241‐248.
Parmesan C, Ryrholm N, Stefanescu C, et al. Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature. 1999;399(6736):579‐583.
Parmesan C. Climate and species' range. Nature. 1996;382:765‐766.
Menzel A, Estrella N. In: Walther G‐R, Burga CA, Edwards PJ, eds. “Fingerprints” of Climate Change‐Adapted Behaviour and Shifting Species Ranges. Kluwer Academic; 2001:123‐137.
Sagarin RD, Barry JP, Gilman SE, Baxter CH. Climate‐related change in an intertidal community over short and long time scales. Ecological Monographs. 1999;69:465‐490.
Ovaskainen O, Skorokhodova S, Yakovleva M, Sukhov A, Kutenkov A, Kutenkova N, Shcherbakov A, Meyke E, Delgado Mdel M. 2013. Community‐level phenological response to climate change. Proc Natl Acad Sci U S A 110(33): 13434–13439.
Brown JH, Valone TJ, Curtin CG. Reorganization of an arid ecosystem in response to recent climate change. Proc Natl Acad Sci U S A. 1997;94:9729‐9733.
Post E, Peterson RO, Stenseth NC, McLaren BE. Ecosystem consequences of wolf behavioural response to climate. Nature. 1999;401:905‐907.
Walther GR, Post E, Convey P, et al. Ecological responses to recent climate change. Nature. 2002;41:389‐395.
Immelmann K. Ecological aspects of periodic reproduction. In: Farner DS, King JR, eds. Avian Biology. Vol I. Aca‐demic Press; 1971:341‐389.
Butler GD, Wilson LT, Henneberry TJ. Heliothis virescens (lepidoptera: Noctuidae): initiation of summer diapause. J Econ Entomol. 1985;78:320‐324.
Lue Y, Hikim AP, Wang C, Im M, Leung A, Swerdloff RS. Testicular heat exposure enhances the suppression of spermatogenesis by testosterone in rats: the “two‐hit” approach to male contraceptive development. Endocrinology. 2000;141:1414‐1424.
Yaeram J, Setchell BP, Maddocks S. Effect of heat stress on the fertility of male mice in vivo and in vitro. Reprod Fertil Dev. 2006;18:647‐653.
Takahashi M. Heat stress on reproductive function and fertility in mammals. Reprod Med Biol. 2011;11(1):37‐47.
Zhu GD, Xue M, Luo Y, et al. Effect of short‐term heat shock and physiological responses to heat stress in two Bradysia adults, Bradysia odoriphaga and Bradysia difformis. Sci Rep. 2017;7:13381.
Renthlei Z, Hmar L, Kumar Trivedi A. High temperature attenuates testicular responses in tree sparrow (Passer montanus). Gen Comp Endocrinol. 2021;301:113654.
Renthlei Z, Mongku M, Yatung S, Lalpekhlui R, Trivedi AK. High temperature during photorefractory stage attenuates photoperiodic responses during photostimulatory stage in male tree sparrows (Passer montanus). Theriogenology Wild. 2024;5:100100.
Dardente H, Wyse CA, Birnie MJ, et al. A molecular switch for photoperiod responsiveness in mammals. Curr Biol. 2010;20(24):2193‐2198.
Masumoto KH, Ukai‐Tadenuma M, Kasukawa T, et al. Acute induction of Eya3 by late‐night light stimulation triggers TSHβ expression in photoperiodism. Curr Biol. 2010;20(24):2199‐2206.
Yasuo S, Watanabe M, Nakao N, Takagi T, Follett BK. The reciprocal switching of two thyroid hormone‐activating and ‐inactivating enzyme genes is involved in the photoperiodic gonadal response of Japanese quail. Endocrinology. 2005;146:2551‐2554.
Stevenson TJ, Prendergast BJ. Reversible DNA methylation regulates seasonal photoperiodic time measurement. Proc Natl Acad Sci U S A. 2013;110(41):16651‐16656.
Petri I, Diedrich V, Wilson D, et al. Orchestration of gene expression across the seasons: hypothalamic gene expression in natural photoperiod throughout the year in the Siberian hamster. Sci Rep. 2016;6:1‐9.
Wood S, Loudon A. The pars tuberalis: the site of the circannual clock in mammals? Gen Comp Endocrinol. 2017;258:222‐235.
Bartzen‐Sprauer J, Klosen P, Ciofi P, Mikkelsen JD, Simonneaux V. Photoperiodic co‐regulation of kisseptin, neurokinin B and dynorphin in the hypothalamus of a seasonal rodent. J Neuroendocrinol. 2014;26(8):510‐520.
Revel FG, Saboureau M, Masson‐P'evet M, P'evet P, Mikkelsen JD, Simonneaux V. Kisspeptin mediates the photoperiodic control of reproduction in hamsters. Curr Biol. 2006;16:1730‐1735.
Ansel L, Bentsen AH, Ancel C, Bolborea M, Klosen P. Peripheral kisspeptin reverses short photoperiod‐induced gonadal regression in Syrian hamsters by promoting GNRH release. Reproduction. 2011;142:417‐425.
Revel FG, Saboureau M, Pévet P, Simonneaux V, Mikkelsen JD. RFamide‐related peptide gene is a melatonin‐driven photoperiodic gene. Endocrinology. 2008;149(3):902‐912.
Schiffer L, Barnard L, Baranowski ES, et al. Human steroid biosynthesis, metabolism and excretion are differentially reflected by serum and urine steroid metabolomes: a comprehensive review. J Steroid Biochem Mol Biol. 2019;194:105439.
Lanz RB, Razani B, Goldberg AD, O'Malley BW. Distinct RNA motifs are important for coactivation of steroid hormone receptors by steroid receptor RNA activator (SRA). Proc Natl Acad Sci U S A. 2002;99:16081‐16086.
Wyce A, Bai Y, Nagpal S, Thompson CC. Research resource: the androgen receptor modulates expression of genes with critical roles in muscle development and function. Mol Endocrinol. 2010;24(8):1665‐1674.
Khristi V, Chakravarthi VP, Singh P, et al. ESR2 regulates granulosa cell genes essential for follicle maturation and ovulation. Mol Cell Endocrinol. 2018;474:214‐226.
Kotula‐Balak M, Pawlicki P, Milon A, et al. The role of G‐protein‐coupled membrane estrogen receptor in mouse Leydig cell function‐in vivo and in vitro evaluation. Cell Tissue Res. 2018;374(2):389‐412.
Liu XY, Dangel AW, Kelley RI, et al. The gene mutated in bare patches and striated mice encodes a novel 3beta‐hydroxysteroid dehydrogenase. Nat Genet. 1999;22:182‐187.
Eddershaw AR, Stubbs CJ, Edwardes LV, et al. Characterization of the kinetic mechanism of human protein arginine methyltransferase 5. Biochemistry. 2020;59(50):4775‐4786.
Wang Y, Zhu T, Li Q, et al. Prmt5 is required for germ cell survival during spermatogenesis in mice. Sci Rep. 2015;5:11031.
Chen M, Dong F, Chen M, et al. PRMT5 regulates ovarian follicle development by facilitating Wt1 translation. Elife. 2021;10:e68930.
Yatung S, Trivedi AK. Daily and seasonal changes in steroidogenic markers in the hypothalamus and testes of tree sparrow (Passer montanus). J Neuroendocrinol. 2024;37:e13478.
Yatung S, Trivedi AK. Time‐ and season‐dependent changes in the steroidogenic markers in female tree sparrow (Passer montanus). Photochem Photobiol Sci. 2025;24(4):607‐628.
Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet. 2002;6:415‐428.
Feinberg AP, Tycko B. The history of cancer epigenetics. Nat Rev Cancer. 2004;4(2):143‐153.
Esteller M. Epigenetics in cancer. N Engl J Med. 2008;358:1148‐1159.
Fernandez MC, Yu A, Moawad AR, O'Flaherty C. Peroxiredoxin 6 regulates the phosphoinositide 3‐kinase/AKT pathway to maintain human sperm viability. Mol Hum Reprod. 2012;25(12):787‐796.
Stevenson TJ. Epigenetic regulation of biological rhythms: an evolutionary ancient molecular timer. Trends Genet. 2018;34(2):90‐100.
Métivier R, Gallais R, Tiffoche C, et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature. 2008;452(7183):45‐50.
Duong HA, Robles MS, Knutti D, Weitz CJ. A molecular mechanism for circadian clock negative feedback. Science. 2011;332(6036):1436‐1439.
Herb BR, Wolschin F, Hansen KD, et al. Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat Neurosci. 2012;15(10):1371‐1373.
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Grant Information:
5/10/FR/07/2021-RBMCH Indian Council of Medical Research; 202223-NFST-MIZ-01807 Ministry of Tribal Affairs, Government of India
Contributed Indexing:
Keywords: epigenetics; reproduction; seasonality; steroidogenesis; temperature
Entry Date(s):
Date Created: 20251002 Date Completed: 20251102 Latest Revision: 20251102
Update Code:
20251103
DOI:
10.1111/jne.70095
PMID:
41035131
Database:
MEDLINE
Weitere Informationen
The rapid increase in urbanization is drastically altering the habitat composition of the wild population. Urbanization is predominantly changing the landscape, composition of flora and fauna, availability of night light, and the rise in temperature. In the natural habitat, photoperiod and temperature are inseparable. In the present study, we examined the effect of mild temperature change from the thermoneutral zone of Syrian hamsters on reproduction-linked activities. To investigate the neuroendocrine mechanisms underlying heat stress effects on reproduction in hamsters, two experiments were performed on adult male animals. In experiment one, animals were divided into two groups (n = 5/group) and exposed to a long photoperiod (15L:9D) with either low (LT; 20 ± 2°C) or high temperature (HT; 32 ± 2°C). After 21 days, all animals were sampled. In experiment two, hamsters (n = 20) were divided equally into two groups and were exposed to the first short photoperiod of 8L:16D, but with low temperature (LT; 20 ± 2°C) or high temperature (HT; 32 ± 2°C). After 30 days, all animals were exposed to a long day (15L:9D), but animals from each temperature treatment were divided equally into two groups (n = 5/group). Half of the animals (n = 5) of low temperature remained in low temperature (LL group) while the remaining animals were moved to high temperature (LH group). Similarly, half of the animals (n = 5) of high temperature remained in high temperature (HH group), and the rest of the animals were moved to low temperature (HL group). Body mass and testicular volume were measured at different intervals. After 30 days of long-day treatment, the animals were sampled. Findings suggest that exposure to 3 weeks of high temperature attenuates testicular growth, coupled with low testosterone levels and downregulation of Kiss1, Eya3, Tshβ, GnRh, Tet1, Tet2, and Hat1, while upregulation of Dio3, GnIh, Dnmt1, Dnmt3A, Hdac1, and Hdac5 occurs in HT groups. Results from experiment two suggest that low temperature promotes, while high temperature attenuates reproduction and the linked phenomenon. Together, these findings suggest that high temperature modulates the reproductive responses of Syrian hamsters.
(© 2025 British Society for Neuroendocrinology.)