Hypothermia and Reproductive Function of Male Mammals
- 作者: Kuznetsova E.V.1, Tikhonova N.B.1, Ponomarenko E.A.1, Kuznetsov V.A.2, Nizyaeva N.V.1
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隶属关系:
- Avtsyn Research Institute of Human Morphology
- Sechenov First Moscow State Medical University
- 期: 卷 111, 编号 2 (2025)
- 页面: 195-209
- 栏目: REVIEW
- URL: https://cardiosomatics.ru/0869-8139/article/view/679304
- DOI: https://doi.org/10.31857/S0869813925020019
- EDN: https://elibrary.ru/UJAXGD
- ID: 679304
如何引用文章
详细
The human and animal reproductive systems are sensitive to temperature, but there are very few studies on the effects of hypothermia. The widespread application of therapeutic hypothermia requires a comprehensive study of the time-delayed effects of low temperature on a variety of physiological systems. Hibernating mammals have a significant potential for reactivation of the reproductive system after prolonged hypothermia and can serve as an important experimental model for the development of new methods of treatment and prevention of human reproductive diseases. This review presents an analysis of currently available data on disorders in the mammalian reproductive system under hypothermia, and also discusses the mechanisms of natural protection of reproductive function in hibernating mammals.
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作者简介
E. Kuznetsova
Avtsyn Research Institute of Human Morphology
编辑信件的主要联系方式.
Email: kuznetsovaekvl@gmail.com
俄罗斯联邦, Moscow
N. Tikhonova
Avtsyn Research Institute of Human Morphology
Email: kuznetsovaekvl@gmail.com
俄罗斯联邦, Moscow
E. Ponomarenko
Avtsyn Research Institute of Human Morphology
Email: kuznetsovaekvl@gmail.com
俄罗斯联邦, Moscow
V. Kuznetsov
Sechenov First Moscow State Medical University
Email: kuznetsovaekvl@gmail.com
俄罗斯联邦, Moscow
N. Nizyaeva
Avtsyn Research Institute of Human Morphology
Email: kuznetsovaekvl@gmail.com
俄罗斯联邦, Moscow
参考
- Mohr SM, Bagriantsev SN, Gracheva EO (2020) Cellular, Molecular, and Physiological Adaptations of Hibernation: The Solution to Environmental Challenges. Annu Rev Cell Dev Biol 36: 315–338. https://doi.org/10.1146/annurev-cellbio-012820-095945
- Giroud S, Habold C, Nespolo RF, Mejías C, Terrien J, Logan SM, Henning RH, Storey KB (2020) The Torpid State: Recent Advances in Metabolic Adaptations and Protective Mechanisms. Front Physiol 11: 623665. https://doi.org/10.3389/fphys.2020.623665
- Yang Y, Hao Z, An N, Han Y, Miao W, Storey KB, Lefai E, Liu X, Wang J, Liu S, Xie M, Chang H (2023) Integrated transcriptomics and metabolomics reveal protective effects on heart of hibernating Daurian ground squirrels. J Cell Physiol 238(11): 2724–2748. https://doi.org/10.1002/jcp.31123
- Крамарова ЛИ, Зиганшин РХ, Гахова ЭН (2009) Эндогенные гипометаболические-гипотермические факторы и их возможное применение для жизни в холоде. Биоорган химия 35(5): 597–609. [Kramarova LI, Ziganshin RKH, Gakhova EN (2009) Endogenous hypometabolic-hypothermic factors and their possible application to life in the cold. Bioorgan khimiya 35(5): 597–609. (In Russ)].
- Шевелев ОА, Петрова МВ, Менгисту ЭМ, Якименко ВА, Менжуренкова ДА, Колбаскина ИН, Жданова МА, Ходорович НА, Шевелева ЕО (2023) Механизмы низкотемпературных реабилитационных технологий. Естественная и искусственная гипотермия. Физич реабилитац мед, мед реабилитац 5(2): 141–156. [Shevelev OA, Petrova MV, Mengistu EM, Yakimenko VA, Menzhurenkova DA, Kolbaskina IN, Zhdanova MA, Khodorovich NA, Sheveleva YEO (2023) Mechanisms of low-temperature rehabilitation technologies. Natural and artificial hypothermia. Fiziches reabilitats med, med reabilitatsiya 5(2): 141–156. (In Russ)]. https://doi.org/10.36425/rehab345206
- Ruf T, Geiser F (2015) Daily torpor and hibernation in birds and mammals. Biol Rev Camb Philos Soc 90(3): 891–926. https://doi.org/10.1111/brv.12137
- Andrews MT (2019) Molecular interactions underpinning the phenotype of hibernation in mammals. J Exp Biol 222 (Pt 2). https://doi.org/10.1242/jeb.160606
- Ким АЕ, Ганапольский ВП, Головко КП, Шустов ЕБ (2022) Основные направления применения терапевтической гибернации в клинической и военной медицине (обзор литературы). Рос биомед исслед 7(3): 51–61. [Kim AYE, Ganapol'skiy VP, Golovko KP, Shustov YEB (2022) Main directions of therapeutic hibernation application in clinical and military medicine (literature review). Ross biomed issled 7(3): 51–61. (In Russ)].
- Ушаков ИБ, Комаревцев ВН, Сапецки НВ, Сапецкий АО, Тимофеев НН (2020) Теория ансамблей гибернации и возможности ее использования для обеспечения жизнедеятельности при экстремальных воздействиях. Вестн рос военно-мед акад 1(69): 119–123. [Ushakov IB, Komarevtsev VN, Sapetski NV, Sapetskiy AO, Timofeyev NN (2020) Hibernation ensemble theory and its potential use for life support under extreme impacts. Vestnik ross voyenno-med akad 1(69): 119–123. (In Russ)].
- Shi Z, Qin M, Huang L, Xu T, Chen Y, Hu Q, Peng S, Peng Z, Qu LN, Chen SG, Tuo QH, Liao DF, Wang XP, Wu RR, Yuan TF, Li YH, Liu XM (2021) Human torpor: translating insights from nature into manned deep space expedition. Biol Rev Camb Philos Soc 96(2): 642–672. https://doi.org/10.1111/brv.12671
- Wu CW, Storey KB (2016) Life in the cold: Links between mammalian hibernation and longevity. Biomol Concepts 7(1): 41–52. https://doi.org/10.1515/bmc-2015-0032
- Pan M (2018) Hibernation induction in non-hibernating species. Bioscience Horizons: The Int J Student Res 11. https://doi.org/10.1093/biohorizons/hzy002
- Zakharova NM, Tarahovsky YS, Komelina NP, Fadeeva IS, Kovtun AL (2021) Long-term pharmacological torpor of rats with feedback-controlled drug administration. Life Sci Space Res (Amst) 28: 18–21. https://doi.org/https://doi.org/10.1016/j.lssr.2020.11.002
- Шустов ЕБ, Капанадзе ГД, Фокин ЮВ, Матвеенко ЕЛ (2017) Методические особенности биомедицинских исследований влияния фармакологических средств на устойчивость организма к острой общей гипотермии. Биомедицина (3): 4–15. [SHustov EB, Kapanadze GD, Fokin YUV, Matveenko EL (2017) Methodical features of biomedical research of the influence of pharmacological agents on the resistance of the organism to acute general hypothermia. Biomedicina (3): 4–15. (In Russ)].
- Ivanov KP, Arokina NK (2016) Maintenance of the Cardiovascular Function in a Deeply Cooled Homeothermic Organism by Physiological Methods without External Rewarming. Bull Exp Biol Med 160(4): 407–409. https://doi.org/10.1007/s10517-016-3182-z
- Арокина НК, Лучаков ЮИ, Зилов ВГ, Несмеянов АА (2019) Восстановление работы сердца у крыс и снижение температурного порога его остановки посредством искусственной вентиляции легких в условиях глубокой гипотермии. Вестн новых мед технол (1): 7–11. [Arokina NK, Luchakov YuI, Zilov VG, Nesmeyanov AA (2019) Influence of the apnea duration under deep hypothermia on restoring of the rats heart. Vestn novyh med tekhnol (1): 7–11. (In Russ)].
- Игнатьев ДА, Гордон РЯ, Патрушев ИВ, Попов ВИ (2012) Функциональное состояние головного мозга зимоспящих и незимоспящих при различных температурах животных. Успехи физиол наук 43(1): 48–74. [Ignat'yev DA, Gordon RYA, Patrushev IV, Popov VI (2012) Functional state of the brain of hibernating and non-hibernating animals at different temperatures. Uspekhi fiziol nauk 43(1): 48–74. (In Russ)].
- Меркулова ИА, Аветисян ЭА, Тереничева МА, Певзнер ДВ, Шахнович РМ (2020) Управляемая терапевтическая гипотермия при остановке сердца: сложные вопросы и нерешенные проблемы. Кардиология 60(2): 104–110. [Merkulova IA, Avetisyan EA, Terenicheva MA, Pevzner DV, Shakhnovich RM (2020) Therapeutic Hypothermia in a Cardiac Arrest: Complicated Questions and Unsolved Problems. Kardiologiya 60(2): 104–110. (In Russ)]. https://doi.org/10.18087/cardio.2020.2.n690
- Saigal S, Sharma JP, Dhurwe R, Kumar S, Gurjar M (2015) Targeted temperature management: Current evidence and practices in critical care. Indian J Crit Care Med 19(9): 537–546. https://doi.org/10.4103/0972-5229.164806
- Григорьев ЕВ, Шукевич ДЛ, Плотников ГП, Тихонов НС (2014) Терапевтическая гипотермия: возможности и перспективы. Клин мед 92(9): 9–16. [Grigor’ev EV, Shukevich DL, Plotnikov GP, Tikhonov NS (2014) Therapeutic Hypothermia: The Potential And Prospects. Klin med 92(9): 9–16. (In Russ)].
- Рябов ВВ, Вышлов ЕВ (2023) Терапевтическая гипотермия при остром инфаркте миокарда. Рос кардиол журн 28(7): 95–99. [Ryabov VV, Vyshlov YEV (2023) Therapeutic hypothermia in acute myocardial infarction. Russ J Cardiol 28(7): 95–99. (In Russ)]. https://doi.org/https://doi.org/10.15829/1560-4071-2023-5412
- Gocoł R, Hudziak D, Bis J, Mendrala K, Morkisz Ł, Podsiadło P, Kosiński S, Piątek J, Darocha T (2021) The Role of Deep Hypothermia in Cardiac Surgery. Int J Environ Res Public Health 18(13). https://doi.org/10.3390/ijerph18137061
- Bjertnæs LJ, Næsheim TO, Reierth E, Suborov EV, Kirov MY, Lebedinskii KM, Tveita T (2022) Physiological Changes in Subjects Exposed to Accidental Hypothermia: An Update. Front Med (Lausanne) 9: 824395. https://doi.org/10.3389/fmed.2022.824395
- Sato M, Kitaura K, Minami T, Matsumoto S, Fukuda M (2007) Hypothermia-related testicular toxicity of reserpine in mice. Exp Toxicol Pathol 59(3–4): 187–195. https://doi.org/10.1016/j.etp.2007.05.006
- Саяпина ИЮ, Целуйко СС, Лашин СА, Остронков ВС (2018) Функциональная морфология органов мужской репродуктивной системы при адаптации к низким температурам на фоне коррекции дигидрокверцетином. Благовещенск. ООО Типография. [Sayapina IYu, Celujko SS, Lashin SA, Ostronkov VS (2018) Functional morphology of organs of the male reproductive system during adaptation to low temperatures against the background of dihydroquercetin correction. Blagoveshchensk. OOO Tipografiya. (In Russ)].
- Blanco-Rodríguez J, Martínez-García C (1997) Mild hypothermia induces apoptosis in rat testis at specific stages of the seminiferous epithelium. J Androl 18(5): 535–539.
- Macdonald J, Harrison RG (1954) Effect of low temperatures on rat spermatogenesis. Fertil Steril 5(3): 205–216. https://doi.org/10.1016/s0015-0282(16)31621-1
- Зайцев ВА, Цепкова ГА, Говердовский ЮБ (2020) Репродуктивное здоровье мужчин в условиях воздействия сложного комплекса вредных профессиональных и экологических факторов. Врач 31(8): 45–53. [Zajcev VA, Cepkova GA, Goverdovskij YuB (2020) Male reproductive health under the influence of a complex set of harmful occupational and environmental factors. Vrach 31(8): 45–53. (In Russ)]. https://doi.org/10.29296/25877305-2020-08-07
- Фесенко МА, Голованева ГВ, Мителева ТЮ, Вуйцик ПА (2023) Влияние вредных производственных физических факторов на репродуктивное здоровье работников-мужчин. Мед труда и промышл экол 63(8): 528–536. [Fesenko MA, Golovaneva GV, Miteleva TYu, Vujcik PA (2023) The influence of harmful occupational physical factors on the male workers’ reproductive health. Med truda i promyshl ekol 63(8): 528–536. (In Russ)]. https://doi.org/10.31089/1026-9428-2023-63-8-528-536
- Nakamura M, Nonomura N, Namiki M, Okuyama A, Koh E, Kondoh N, Takeyama M, Kiyohara H, Fujioka H (1989) Temperature influence on human testicular function – optimal temperature for testicular macromolecular synthesis. Nihon Hinyokika Gakkai Zasshi 80(9): 1362–1366. https://doi.org/10.5980/jpnjurol1989.80.1362
- Xiao L, Wang Q, Ni H, Xu T, Cai X, Dai T, Wang L, Song C, Li Y, Li F, Meng T, Sheng H, Yu X, Zeng Q, Guo P, Zhang X (2024) Effects of temperature anomaly on sperm quality: A multi-center study of 33,234 men. Heliyon 10(5): e26765. https://doi.org/10.1016/j.heliyon.2024.e26765
- Zhou Y, Meng T, Wu L, Duan Y, Li G, Shi C, Zhang H, Peng Z, Fan C, Ma J, Xiong C, Bao W, Liu Y (2020) Association between ambient temperature and semen quality: A longitudinal study of 10 802 men in China. Environ Int 135: 105364. https://doi.org/10.1016/j.envint.2019.105364
- Barnes BM, Kretzmann M, Licht P, Zucker I (1986) The influence of hibernation on testis growth and spermatogenesis in the golden-mantled ground squirrel, Spermophilus lateralis. Biol Reprod 35(5): 1289–1297. https://doi.org/10.1095/biolreprod35.5.1289
- Gagnon MF, Lafleur C, Landry-Cuerrier M, Humphries MM, Kimmins S (2020) Torpor expression is associated with differential spermatogenesis in hibernating eastern chipmunks. Am J Physiol Regul Integr Comp Physiol 319(4): R455–R465. https://doi.org/10.1152/ajpregu.00328.2019
- Dou M, Lu C, Rao W (2022) Bioinspired materials and technology for advanced cryopreservation. Trends Biotechnol 40(1): 93–106. https://doi.org/10.1016/j.tibtech.2021.06.004
- Nemcova M, Seidlova V, Zukal J, Dundarova H, Bednarikova S, Pikula J (2023) Bat-derived cells use glucose as a cryoprotectant. J Therm Biol 115: 103652. https://doi.org/10.1016/j.jtherbio.2023.103652
- Захарова НМ (2023) Длиннохвостый суслик как модель патологических состояний. Теоретические и практические аспекты действия естественной и искусственной гипотермии на организм. Тез докл 2-й Всерос научн конф Махачкала. Изд-во ДГУ. 7. [Zaharova NM (2023) Long-tailed gopher as a model of pathological conditions. Theoretical and practical aspects of the effect of natural and artificial hypothermia on the organism. Theses of the report of the 2nd All-Rus scient conf Makhachkala. Publishing house DSU. 7. (In Russ)].
- Bouma HR, Verhaag EM, Otis JP, Heldmaier G, Swoap SJ, Strijkstra AM, Henning RH, Carey HV (2012) Induction of torpor: Mimicking natural metabolic suppression for biomedical applications. J Cell Physiol 227(4): 1285–1290. https://doi.org/10.1002/jcp.22850
- Gritsyna YV, Grabarskaya MA, Mikhailova GZ, Popova SS, Bobyleva LG, Ermakov AM, Zakharova NM, Vikhlyantsev IM (2022) Differential Expression of Titin and Obscurin mRNA in Striated Muscles of the Long-Tailed Ground Squirrel Urocitellus undulatus. J Evol Biochem Physiol 58(5): 1332–1340. https://doi.org/10.1134/S0022093022050052
- Stancic A, Jankovic A, Korac A, Cirovic D, Otasevic V, Storey KB, Korac B (2018) A lesson from the oxidative metabolism of hibernator heart: Possible strategy for cardioprotection. Comp Biochem Physiol B Biochem Mol Biol 219-220: 1–9. https://doi.org/10.1016/j.cbpb.2018.02.004
- Berg von Linde M, Arevström L, Fröbert O (2015) Insights from the Den: How Hibernating Bears May Help Us Understand and Treat Human Disease. Clin Transl Sci 8(5): 601–605. https://doi.org/10.1111/cts.12279
- Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83(4): 1153–1181. https://doi.org/10.1152/physrev.00008.2003
- Jorban A, Lunenfeld E, Huleihel M (2024) Effect of Temperature on the Development of Stages of Spermatogenesis and the Functionality of Sertoli Cells In vitro. Int J Mol Sci 25(4). https://doi.org/10.3390/ijms25042160
- Durairajanayagam D, Agarwal A, Ong C (2015) Causes, effects and molecular mechanisms of testicular heat stress. Reprod Biomed Online 30(1): 14–27. https://doi.org/10.1016/j.rbmo.2014.09.018
- Robinson BR, Netherton JK, Ogle RA, Baker MA (2023) Testicular heat stress, a historical perspective and two postulates for why male germ cells are heat sensitive. Biol Rev Camb Philos Soc 98(2): 603–622. https://doi.org/10.1111/brv.12921
- Zhang Z, Short RV, Meehan T, De Kretser DM, Renfree MB, Loveland KL (2004) Functional analysis of the cooled rat testis. J Androl 25(1): 57–68. https://doi.org/10.1002/j.1939-4640.2004.tb02759.x
- Саяпина ИЮ, Огородникова ТЛ (2013) Репродуктивная функция семенников крыс после семидневной адаптации к низким температурам по данным морфологического анализа. Научн журн КубГАУ 89(05): 316–328. [Sayapina IYU, Ogorodnikova TL (2013) Reproductive function of the rat testis after 7-day adaptation to low temperatures, according to the morphological analysis. Nauchn zhurn KuBGAU 89(05): 316–328. (In Russ)].
- Саяпина ИЮ (2011) Количественный анализ функциональной активности семенника крыс при окислительном стрессе, индуцированном адаптацией к низким температурам. Вестн новых мед технол 18(2): 155–157. [Sayapina IYU (2011) The quantitative analysis of functional activity of rat testicles at an oxidative stress induced by the adaptation to low temperatures. Vestn novykh med tekhnol 18(2): 155–157. (In Russ)].
- Barnes B (1996) Relationships between hibernation and reproduction in male ground squirrels. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the Cold: Tenth Int Hibernation Sympos. Armidale, Aust. Univ N-Engl Press. 71–80.
- Bieber C, Ruf (2004) Seasonal Timing of Reproduction and Hibernation in the Edible Dormouse (Glis glis). In: Barnes BM (ed) Life in the Cold Evolution, Mechanism, Adaptation and Application Fairbanks, Alaska, USA. Instit Arctic Biol, Univer Alaska. 113–125.
- Vasilieva NA, Tikhonova NB, Savinetskaya LE, Kuznetsova EV (2024) Female hormonal profiles and vaginal cytology in a ground squirrel species with prolonged hibernation. Mammal Biol 104(1): 55–67. https://doi.org/10.1007/s42991-023-00387-y
- Barnes BM (1986) Annual cycles of gonadotropins and androgens in the hibernating golden-mantled ground squirrel. Gen Comp Endocrinol 62(1): 13–22. https://doi.org/10.1016/0016-6480(86)90089-4
- Dai Pra R, Mohr SM, Merriman DK, Bagriantsev SN, Gracheva EO (2022) Ground squirrels initiate sexual maturation during hibernation. Curr Biol 32(8): 1822-8.e4. https://doi.org/10.1016/j.cub.2022.02.032
- Han Y, Zhan J, Xu Y, Zhang F, Yuan Z, Weng Q (2017) Proliferation and apoptosis processes in the seasonal testicular development of the wild Daurian ground squirrel (Citellus dauricus Brandt, 1844). Reprod Fertil Dev 29(9): 1680–1688. https://doi.org/10.1071/rd16063
- Li Q, Zhang F, Zhang S, Sheng X, Han X, Weng Q, Yuan Z (2015) Seasonal expression of androgen receptor, aromatase, and estrogen receptor alpha and beta in the testis of the wild ground squirrel (Citellus dauricus Brandt). Eur J Histochem 59(1): 2456. https://doi.org/10.4081/ejh.2015.2456
- Dutourné B, Saboureau M (1983) An endocrine and histophysiological study of the testicular annual cycle in the hedgehog (Erinaceus europaeus L.). Gen Comp Endocrinol 50(2): 324–332. https://doi.org/10.1016/0016-6480(83)90233-2
- Reznik-Schüller H, Reznik G (1973) Comparative histometric investigations of the testicular function of European hamsters (Cricetus cricetus) with and without hibernation. Fertil Steril 24(9): 698–705. https://doi.org/10.1016/s0015-0282(16)39915-0
- Saboureau M, Dutourné B (1981) The reproductive cycle in the male hedgehog (Erinaceus europaeus L.): A study of endocrine and exocrine testicular functions. Reprod Nutr Dev 21(1): 109–126. https://doi.org/10.1051/rnd:19810110
- Zhang H, Sheng X, Hu X, Li X, Xu H, Zhang M, Li B, Xu M, Weng Q, Zhang Z, Taya K (2010) Seasonal changes in spermatogenesis and immunolocalization of cytochrome P450 17alpha-hydroxylase/c17-20 lyase and cytochrome P450 aromatase in the wild male ground squirrel (Citellus dauricus Brandt). J Reprod Dev 56(3): 297–302. https://doi.org/10.1262/jrd.09-078t
- Wang J, Wang Y, Zhu M, Zhang F, Sheng X, Zhang H, Han Y, Yuan Z, Weng Q (2017) Seasonal expression of luteinizing hormone receptor and follicle stimulating hormone receptor in testes of the wild ground squirrels (Citellus dauricus Brandt). Acta Histochem 119(7): 727–732. https://doi.org/10.1016/j.acthis.2017.09.004
- Strauss A, Hoffmann IE, Vielgrader H, Millesi E (2008) Testis development and testosterone secretion in captive European ground squirrels before, during, and after hibernation. Acta Theriol 53(1): 47–56. https://doi.org/10.1007/BF03194278
- Williams CT, Barnes BM, Buck CL (2016) Integrating physiology, behavior, and energetics: Biologging in a free-living arctic hibernator. Comp Biochem Physiol A Mol Integr Physiol 202: 53–62. https://doi.org/10.1016/j.cbpa.2016.04.020
- Barnes BM, Kretzmann M, Zucker I, Licht P (1988) Plasma androgen and gonadotropin levels during hibernation and testicular maturation in golden-mantled ground squirrels. Biol Reprod 38(3): 616–622. https://doi.org/10.1095/biolreprod38.3.616
- Wang Z, Wang MD, Wang XC, Chen L, Li LF, Jiang LN, Xu JH, Kai D (2024) High levels of mitochondrial dynamics, autophagy, and apoptosis contribute to stable testicular status in hibernating Daurian ground squirrels. Comp Biochem Physiol A Mol Integr Physiol 297: 111705. https://doi.org/10.1016/j.cbpa.2024.111705
- Siutz C, Franceschini C, Millesi E (2016) Sex and age differences in hibernation patterns of common hamsters: adult females hibernate for shorter periods than males. J Comp Physiol B 186(6): 801–811. https://doi.org/10.1007/s00360-016-0995-z
- Vekhnik VA, Ruf T, Bieber C (2022) A Review on the Edible dormouse reproduction (Glis glis Linnaeus, 1766). J Wildlife and Biodiversity 6 (Special issue): 24–45. https://doi.org/https://doi.org/10.5281/zenodo.7338112
- Richter MM, Barnes BM, O'Reilly KM, Fenn AM, Buck CL (2017) The influence of androgens on hibernation phenology of free-living male arctic ground squirrels. Horm Behav 89: 92–97. https://doi.org/10.1016/j.yhbeh.2016.12.007
- Bushberg DM, Holmes WG (1985) Sexual Maturation in Male Belding’s Ground Squirrels: Influence of Body Weight. Biol Reproduct 33(2): 302–308. https://doi.org/10.1095/biolreprod33.2.302
- Darrow JM, Yogev L, Goldman BD (1987) Patterns of reproductive hormone secretion in hibernating Turkish hamsters. Am J Physiol Regul Integrat Compar Physiol 253(2): R329–R336. https://doi.org/10.1152/ajpregu.1987.253.2.R329
- Holekamp KE, Talamantes F (1991) Seasonal variation in circulating testosterone and oestrogens of wild-caught California ground squirrels (Spermophilus beecheyi). J Reprod Fertil 93(2): 415–425. https://doi.org/10.1530/jrf.0.0930415
- Barnes BM, Licht P, Zucker I (1987) Temperature dependence of in vitro androgen production in testes from hibernating ground squirrels, Spermophilus lateralis. Canad J Zool 65(12): 3020–3023. https://doi.org/10.1139/z87-457
- Duffy BM, Staples JF (2022) Arousal from Torpor Increases Oxidative Damage in the Hibernating Thirteen-Lined Ground Squirrel (Ictidomys tridecemlineatus). Physiol Biochem Zool 95(3): 229–238. https://doi.org/10.1086/719931
- Orr AL, Lohse LA, Drew KL, Hermes-Lima M (2009) Physiological oxidative stress after arousal from hibernation in Arctic ground squirrel. Comp Biochem Physiol A Mol Integr Physiol 153(2): 213–221. https://doi.org/10.1016/j.cbpa.2009.02.016
- Tøien Ø, Drew KL, Chao ML, Rice ME (2001) Ascorbate dynamics and oxygen consumption during arousal from hibernation in Arctic ground squirrels. Am J Physiol Regul Integr Comp Physiol 281(2): R572–R583. https://doi.org/10.1152/ajpregu.2001.281.2.R572
- Антонова ЕП, Илюха ВА, Сергина СН (2015) Антиоксидантная защита у зимоспящих млекопитающих. Принципы эколог 4(2): 4–20. [Antonova EP, Ilyukha VA, Sergina SN (2015) Antioxidant defense system in hibernating mammals. Principy èkologii 4(2): 4–20. (In Russ)]. https://doi.org/10.15393/j1.art.2015.3962
- Klichkhanov NK, Nikitina ER, Shihamirova ZM, Astaeva MD, Chalabov SI, Krivchenko AI (2021) Erythrocytes of Little Ground Squirrels Undergo Reversible Oxidative Stress During Arousal From Hibernation. Front Physiol 12: 730657. https://doi.org/10.3389/fphys.2021.730657
- Божедомов ВА, Торопцева МВ, Ушакова ИВ, Спориш ЕА, Ловыгина НА, Липатова НА (2011) Активные формы кислорода и репродуктивная функция мужчин: фундаментальные и клинические аспекты (обзор литературы). Андрология и генитал хирург (3): 10–16. [Bozhedomov VA, Toroptseva MV, Ushakova IV, Sporish YEA, Lovygina NA, Lipatova NA (2011) Reactive oxygen species and the reproductive function of men: Basic and clinical aspects (review). Androlog i genital khirurg (3): 10–16. (In Russ)].
- Takalani NB, Monageng EM, Mohlala K, Monsees TK, Henkel R, Opuwari CS (2023) Role of oxidative stress in male infertility. Reprod Fertil 4(3). https://doi.org/10.1530/raf-23-0024
- Wu PY, Scarlata E, O'Flaherty C (2020) Long-Term Adverse Effects of Oxidative Stress on Rat Epididymis and Spermatozoa. Antioxidants (Basel) 9(2). https://doi.org/10.3390/antiox9020170
- Rouble AN, Hefler J, Mamady H, Storey KB, Tessier SN (2013) Anti-apoptotic signaling as a cytoprotective mechanism in mammalian hibernation. Peer J 1: e29. https://doi.org/10.7717/peerj.29
- Sato T, Sugiyama T, Sekijima T (2023) Mating in the cold. Prolonged sperm storage provides opportunities for forced copulation by male bats during winter. Front Physiol 14: 1241470. https://doi.org/10.3389/fphys.2023.1241470
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