昼夜节律与雌激素协同调控哺乳动物生殖的研究进展

doi:10.11843/j.issn.0366-6964.2023.05.001

Abstract

Abstract: The circadian system is an internal timer system in most mammals, as the main circadian clock, the hypothalamic suprachiasmatic nucleus (SCN) coordinates the timing of the organizational clock to align internal rhythms with environmental cycles. Cells in the SCN core are capable of receiving light signaling directly from intrinsically photosensitive retinal ganglion cells (ipRGCs), whose endogenous oscillations determine behavioral and physiological rhythms throughout the animal. Estrogen is capable of regulating a variety of biological processes of mammals, including but not limited to the circadian rhythmic behavior of the estrous cycle. Estrogen and SCN synergistically regulate GnRH secretion, LH peak, ovulation, and resulting in the regu-lation of the mammalian reproductive process. This paper reviews the recent research progress in the mutual regulation of estrogen and circadian rhythm in female mammals, including the phenomenon of estrogen secretion and circadian rhythm, the molecular link between estrogen and circadian rhythm, and their regulation mechanism on the reproduction of female mammals. These results can provide a reference for further exploration of the reproductive rhythm and hormone regulation mechanism of female mammals.

Key words: mammals, circadian rhythm, estrogen, SCN, reproduction regulation

CLC Number:

S811.4

WANG Wei, HE Xiaoyun, CHU Mingxing. Advances in the Regulation of Mammal Reproduction by the Interaction of Circadian Rhythm and Estrogens[J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(5): 1771-1781.

References 95

[1]	CHINNAPAIYAN S,DUTTA R K,DEVADOSS D,et al.Role of non-coding RNAs in lung circadian clock related diseases[J]. Int J Mol Sci,2020,21(8):3013.
[2]	ROSENWASSER A M,TUREK F W.Neurobiology of circadian rhythm regulation[J]. Sleep Med Clin,2022,17(2):141-150.
[3]	ZHANG W X,CHEN S Y,LIU C.Regulation of reproduction by the circadian rhythms[J]. Acta Physiol Sin,2016,68(6):799-808.
[4]	BASS J,LAZAR M A.Circadian time signatures of fitness and disease[J]. Science,2016,354(6315):994-999.
[5]	PHILPOTT J M,TORGRIMSON M R,HAROLD R L,et al.Biochemical mechanisms of period control within the mammalian circadian clock[J]. Semin Cell Dev Biol,2022,126:71-78.
[6]	HEWITT S C,KORACH K S.Estrogen receptors:new directions in the new millennium[J]. Endocr Rev,2018,39(5):664-675.
[7]	包莹莹.甘加型藏羊发情周期血浆E2动态变化规律及ERS在HPOA中的表达与分布[D].兰州:甘肃农业大学,2021.BAO Y Y.The dynamic variation of E2 in plasma and the distribution and expression of ERs in HPOA of Ganjia Tibetan sheep during estrus cycle[D].Lanzhou:Gansu Agricultural University,2021.(in Chinese)
[8]	贺小云,狄冉,胡文萍,等.绵羊季节性繁殖的神经内分泌研究进展[J].畜牧兽医学报,2018,49(1):18-25.HE X Y,DI R,HU W P,et al.Research progress on neuroendocrinology controlling sheep seasonal reproduction[J]. Acta Veterinaria et Zootechnica Sinica,2018,49(1):18-25.(in Chinese)
[9]	WEEMS P W,GOODMAN R L,LEHMAN M N.Neural mechanisms controlling seasonal reproduction:principles derived from the sheep model and its comparison with hamsters[J]. Front Neuroendocrinol,2015,37:43-51.
[10]	DARDENTE H,SIMONNEAUX V.GnRH and the photoperiodic control of seasonal reproduction:delegating the task to kisspeptin and RFRP-3[J]. J Neuroendocrinol,2022,34(5):e13124.
[11]	WILLIAMS III W P,KRIEGSFELD L J.Circadian control of neuroendocrine circuits regulating female reproductive function[J]. Front Endocrinol (Lausanne),2012,3:60.
[12]	WALTON J C,BUMGARNER J R,NELSON R J.Sex differences in circadian rhythms[J]. Cold Spring Harb Perspect Biol,2022,14(7):a039107.
[13]	ALVORD V M,KANTRA E J,PENDERGAST J S.Estrogens and the circadian system[J]. Semin Cell Dev Biol,2022,126:56-65.
[14]	CLEMENS A M,LENSCHOW C,BEED P,et al.Estrus-cycle regulation of cortical inhibition[J]. Curr Biol,2019,29(4):605-615.e6.
[15]	KUMRO F G,SMITH F M,YALLOP M J,et al. Short communication:simultaneous measurements of estrus behavior and plasma concentrations of estradiol during estrus in lactating and nonlactating dairy cows[J]. J Dairy Sci,2021,104(2):2445-2454.
[16]	LASSER J,MATZHOLD C,EGGER-DANNER C,et al.Integrating diverse data sources to predict disease risk in dairy cattle-a machine learning approach[J]. J Anim Sci,2021,99(11):skab294.
[17]	SILVA C C,CORTÉS G D,JAVIER C Y,et al.A neural circadian signal essential for ovulation is generated in the suprachiasmatic nucleus during each stage of the oestrous cycle[J]. Exp Physiol,2020,105(2):258-269.
[18]	EVERETT J W,SAWYER C H.A 24-hour periodicity in the "LH-release apparatus" of female rats,disclosed by barbiturate sedation[J]. Endocrinology,1950,47(3):198-218.
[19]	STETSON M H,WATSON-WHITMYRE M,DIPINTO M N,et al.Daily luteinizing hormone release in ovariectomized hamsters:effect of barbiturate blockade[J]. Biol Reprod,1981,24(1):139-144.
[20]	HASTINGS M H,MAYWOOD E S,BRANCACCIO M.Generation of circadian rhythms in the suprachiasmatic nucleus[J]. Nat Rev Neurosci,2018,19(8):453-469.
[21]	STEPHAN F K,ZUCKER I.Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions[J]. Proc Natl Acad Sci U S A,1972,69(6):1583-1586.
[22]	RALPH M R,FOSTER R G,DAVIS F C,et al.Transplanted suprachiasmatic nucleus determines circadian period[J]. Science, 1990,247(4945):975-978.
[23]	程满,余爽,李娟,等.视交叉上核在昼夜节律中的作用[J].生命科学,2015,27(11):1380-1385.CHENG M,YU S,LI J,et al.The role of the suprachiasmatic nucleus in circadian rhythm generation[J]. Chinese Bulletin of Life Sciences,2015,27(11):1380-1385.(in Chinese)
[24]	BEGEMANN K,NEUMANN A M,OSTER H.Regulation and function of extra-SCN circadian oscillators in the brain[J]. Acta Physiol (Oxf),2020,229(1):e13446.
[25]	ABDALLA O H M H,MASCARENHAS B,CHENG H Y M.Death of a protein:the role of E3 ubiquitin ligases in circadian rhythms of mice and flies[J]. Int J Mol Sci, 2022,23(18):10569.
[26]	SCIARRA F,FRANCESCHINI E,CAMPOLO F,et al.Disruption of circadian rhythms:a crucial factor in the etiology of infertility[J]. Int J Mol Sci,2020,21(11):3943.
[27]	MERKLINGER-GRUCHALA A,ELLISON P T,LIPSON S F,et al.Low estradiol levels in women of reproductive age having low sleep variation[J]. Eur J Cancer Prev,2008,17(5):467-472.
[28]	王子昕,宋佳怡,夏天.昼夜节律紊乱对女性卵巢功能的影响[J].国际生殖健康/计划生育杂志,2022,41(4):317-321.WANG Z X,SONG J Y,XIA T.Effect of circadian rhythm disorder on ovarian function[J]. Journal of International Reproductive Health/Family Planning,2022,41(4):317-321.(in Chinese)
[29]	ASTIZ M,HEYDE I,OSTER H.Mechanisms of communication in the mammalian circadian timing system[J]. Int J Mol Sci, 2019, 20(2):343.
[30]	BOS N P A,MIRMIRAN M.Circadian rhythms in spontaneous neuronal discharges of the cultured suprachiasmatic nucleus[J]. Brain Res, 1990,511(1):158-162.
[31]	FATEHI M,ZIDICHOUSKI J A,KOMBIAN S B,et al.17β-estradiol attenuates excitatory neuro-transmission and enhances the excitability of rat parabrachial neurons in vitro[J]. J Neurosci Res,2006,84(3):666-674.
[32]	PETERFI Z,CHURCHILL L,HAJDU I,et al.Fos-immunoreactivity in the hypothalamus:dependency on the diurnal rhythm,sleep,gender,and estrogen[J]. Neuroscience,2004,124(3):695-707.
[33]	FATEHI M,FATEHI-HASSANABAD Z.Effects of 17 β -estradiol on neuronal cell excitability and neurotransmission in the suprachiasmatic nucleus of rat[J]. Neuropsychopharmacology,2008,33(6):1354-1364.
[34]	肖义军,钟磊发.哺乳动物昼夜节律的调控及其分子机制[J].生物学通报,2018,53(5):2-4.XIAO Y J,ZHONG L F.The regulation of the circadian rhythm of mammals and their molecular mechanisms[J]. Bulletin of Biology, 2018,53(5):2-4.(in Chinese)
[35]	MIRSKY H P,LIU A C,WELSH D K,et al.A model of the cell-autonomous mammalian circadian clock[J]. Proc Natl Acad Sci U S A,2009,106(27):11107-11112.
[36]	PATKE A,YOUNG M W,AXELROD S.Molecular mechanisms and physiological importance of circadian rhythms[J]. Nat Rev Mol Cell Biol,2020,21(2):67-84.
[37]	VAN DER HORST G T J,MUIJTJENS M,KOBAYASHI K,et al.Mammalian Cry 1 and Cry 2 are essential for maintenance of circadian rhythms[J]. Nature,1999,398(6728):627-630.
[38]	PREITNER N,DAMIOLA F,LUIS-LOPEZ-MOLINA,et al.The orphan nuclear receptor REV-ERBα controls circadian transcription within the positive limb of the mammalian circadian oscillator[J]. Cell,2002,110(2):251-260.
[39]	SATO T K,PANDA S,MIRAGLIA L J,et al.A functional genomics strategy reveals rora as a component of the mammalian circadian clock[J]. Neuron,2004,43(4):527-537.
[40]	钮嘉辉,王小伟,尤启冬.选择性雌激素受体下调剂研究进展[J].药学进展,2019,43(4):282-292.NIU J H,WANG X W,YOU Q D,et al.Advances in the development of selective estrogen receptor down-regulators[J]. Progress in Pharmaceutical Sciences,2019,43(4):282-292.(in Chinese)
[41]	O'LONE R,FRITH M C,KARLSSON E K,et al.Genomic targets of nuclear estrogen receptors[J]. Mol Endocrinol,2004, 18(8):1859-1875.
[42]	HELDRING N,PIKE A,ANDERSSON S,et al.Estrogen receptors:how do they signal and what are their targets[J]. Physiol Rev,2007,87(3):905-931.
[43]	SANTOLLO J,DANIELS D.Multiple estrogen receptor subtypes influence ingestive behavior in female rodents[J]. Physiol Behav,2015,152:431-437.
[44]	HATCHER K M,ROYSTON S E,MAHONEY M M.Modulation of circadian rhythms through estrogen receptor signaling[J]. Eur J Neurosci,2020,51(1):217-228.
[45]	GERY S,VIRK R K,CHUMAKOV K,et al.The clock gene Per 2 links the circadian system to the estrogen receptor[J]. Oncogene, 2007,26(57):7916-7920.
[46]	DAS M,WEBSTER N J G.Obesity,cancer risk,and time-restricted eating[J]. Cancer Metastasis Rev,2022,41(3):697-717.
[47]	NAKAMURA T J,SELLIX M T,MENAKER M,et al.Estrogen directly modulates circadian rhythms of PER 2 expression in the uterus[J]. Am J Physiol Endocrinol Metab,2008,295(5):E1025-E1031.
[48]	XIAO L Y,CHANG A K,ZANG M X,et al.Induction of the CLOCK gene by E2-ERα signaling promotes the proliferation of breast cancer cells[J]. PLoS One,2014,9(5):e95878.
[49]	肖利云.雌激素-雌激素受体α信号调控 CLOCK 表达的机理[D].大连:大连理工大学,2014.XIAO L Y.The mechanism of E2-ERα signal regulating the expression of CLOCK[D].Dalian:Dalian University of Technology, 2014.(in Chinese)
[50]	JUNIOR R P,DE ALMEIDA CHUFFA L G,SIM?O V A,et al.Melatonin regulates the daily levels of plasma amino acids, acylcarnitines,biogenic amines,sphingomyelins,and hexoses in a xenograft model of triple negative breast cancer[J]. Int J Mol Sci, 2022, 23(16):9105.
[51]	潘霄汝,赵玉磊,杨玉花,等.雌激素对体外培养人毛乳头细胞生物钟基因表达的影响[J].临床皮肤科杂志,2019, 48(9):539-544.PAN X R,ZHAO Y L,YANG Y H,et al.Effect of estrogen on expression of circadian clock genes in human dermal papilla cells in vitro[J]. Journal of Clinical Dermatology,2019,48(9):539-544.(in Chinese)
[52]	CAI W,RAMBAUD J,TEBOUL M,et al.Expression levels of estrogen receptor β are modulated by components of the molecular clock[J]. Mol Cell Biol,2008,28(2):784-793.
[53]	HOFFMAN A E,YI C H,ZHENG T Z,et al.CLOCK in breast tumorigenesis:genetic,epigenetic,and transcriptional profiling analyses[J]. Cancer Res,2010,70(4):1459-1468.
[54]	SRINIVASAN V,SMITS M,SPENCE W,et al.Melatonin in mood disorders[J]. World J Biol Psychiatry,2006,7(3):138-151.
[55]	WIIK A,GLENMARK B,EKMAN M,et al.Oestrogen receptor β is expressed in adult human skeletal muscle both at the mRNA and protein level[J]. Acta Physiol Scand,2003,179(4):381-387.
[56]	LI S,WANG M,AO X,et al.CLOCK is a substrate of SUMO and sumoylation of CLOCK upregulates the transcriptional activity of estrogen receptor-α[J]. Oncogene,2013,32(41):4883-4891.
[57]	HAN Z J,FENG Y H,GU B H,et al.The post-translational modification,SUMOylation,and cancer (review)[J]. Int J Oncol,2018, 52(4):1081-1094.
[58]	DAI W,XIE S Q,CHEN C Y,et al.Ras sumoylation in cell signaling and transformation[J]. Semin Cancer Biol,2021,76:301-309.
[59]	赵淑琴.褪黑素介导的生物钟基因 Cry 对双峰驼雌二醇分泌的影响[D].兰州:甘肃农业大学,2020.ZHAO S Q.Effect of melatonin-mediated circadian clock genes Cry on estradiol secretion of Bactrian camel[D].Lanzhou:Gansu Agricultural University,2020.(in Chinese)
[60]	NAKAMURA T J,SHINOHARA K,FUNABASHI T,et al.Effect of estrogen on the expression of Cry 1 and Cry 2 mRNAs in the suprachiasmatic nucleus of female rats[J]. Neurosci Res,2001,41(3):251-255.
[61]	张森,谭建华.大鼠发情周期中主要生殖激素的变化[J].动物医学进展,2005,26(12):1-6.ZHANG S,TAN J H.Change of reproductive hormones at oestrous cycle stage in rat[J]. Progress in Veterinary Medicine,2005, 26(12):1-6.(in Chinese)
[62]	KRIEGSFELD L J,SILVER R,GORE A C,et al.Vasoactive intestinal polypeptide contacts on gonadotropin-releasing hormone neurones increase following puberty in female rats[J]. J Neuroendocrinol,2002,14(9):685-690.
[63]	方溪.VIP刺激大鼠离体下丘脑释放GnRH[J].国外医学妇产科学分册,1988(5):304.FANG X.VIP stimulates GnRH release from isolated hypothalamus of rats[J]. Journal of International Obstetrics and Gynecology,1988(5):304.(in Chinese)
[64]	PIET R,DUNCKLEY H,LEE K,et al.Vasoactive intestinal peptide excites GnRH neurons in male and female mice[J]. Endocrinology, 2016,157(9):3621-3630.
[65]	WILLIAMS III W P,JARJISIAN S G,MIKKELSEN J D,et al.Circadian control of kisspeptin and a gated GnRH response mediate the preovulatory luteinizing hormone surge[J]. Endocrinology,2011,152(2):595-606.
[66]	STEVENSON H,BARTRAM S,CHARALAMBIDES M M,et al.Kisspeptin-neuron control of LH pulsatility and ovulation[J]. Front Endocrinol (Lausanne),2022,13:951938.
[67]	GU G B,SIMERLY R B.Projections of the sexually dimorphic anteroventral periventricular nucleus in the female rat[J]. J Comp Neurol,1997,384(1):142-164.
[68]	MILLER B H,OLSON S L,LEVINE J E,et al.Vasopressin regulation of the proestrous luteinizing hormone surge in wild-type and Clock mutant mice[J]. Biol Reprod,2006,75(5):778-784.
[69]	骆倩倩.下丘脑弓状核kisspeptin/kiss1r系统对生殖发育及青春期启动的作用[D].滨州:滨州医学院,2016.LUO Q Q.The role of kisspeptin/kiss1r system on reproductive development and puberty onset expressed in the arcuate nucleus of hypothalamus[D].Binzhou:Binzhou Medical University,2016.(in Chinese)
[70]	BELCHETZ P E,PLANT T M,NAKAI Y,et al.Hypophysial responses to continuous and intermittent delivery of hypothalamic gonadotropin-releasing hormone[J]. Science,1978,202(4368):631-633.
[71]	PLANT T M.60 YEARS OF NEUROENDOCRINOLOGY:the hypothalamo-pituitary-gonadal axis[J]. J Endocrinol,2015,226(2):T41-T54.
[72]	EIDEN L E,HERNÁNDEZ V S,JIANG S Z,et al.Neuropeptides and small-molecule amine transmitters:cooperative signaling in the nervous system[J]. Cell Mol Life Sci,2022,79(9):492.
[73]	WIEGAND S J,TERASAWA E,BRIDSON W E,et al.Effects of discrete lesions of preoptic and suprachiasmatic structures in the female rat.Alterations in the feedback regulation of gonadotropin secretion[J]. Neuroendocrinology,1980,31(2):147-157.
[74]	GRAY G D,SÖDERSTEN P,TALLENTIRE D,et al.Effects of lesions in various structures of the suprachiasmatic-preoptic region on LH regulation and sexual behavior in female rats[J]. Neuroendocrinology,1978,25(3):174-191.
[75]	ROBERTSON J L,CLIFTON D K,DE LA IGLESIA H O,et al.Circadian regulation of Kiss 1 neurons:implications for timing the preovulatory gonadotropin-releasing hormone/luteinizing hormone surge[J]. Endocrinology,2009,150(8):3664-3671.
[76]	MURR S M,GESCHWIND I I,BRADFORD G E.Plasma LH and FSH during different oestrous cycle conditions in mice[J]. J Reprod Fertil,1973,32(2):221-230.
[77]	PADILLA S L,PEREZ J G,BEN-HAMO M,et al.Kisspeptin neurons in the arcuate nucleus of the hypothalamus orchestrate circadian rhythms and metabolism[J]. Curr Biol,2019,29(4):592-604.e4.
[78]	MCQUILLAN H J,HAN S Y,CHEONG I,et al.GnRF pulse generator activity across the estrous cycle of female mice[J]. Endocrinology, 2019,160(6):1480-1491.
[79]	IRWIG M S,FRALEY G S,SMITH J T,et al.Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KISS- 1 mRNA in the male rat[J]. Neuroendocrinology,2004,80(4):264-272.
[80]	MERENESS A L,MURPHY Z C,SELLIX M T.Developmental programming by androgen affects the circadian timing system in female mice[J]. Biol Reprod,2015,92(4):88.
[81]	SEN A,HOFFMANN H M.Role of core circadian clock genes in hormone release and target tissue sensitivity in the reproductive axis[J]. Mol Cell Endocrinol,2020,501:110655.
[82]	KENNAWAY D J,BODEN M J,VARCOE T J.Circadian rhythms and fertility[J]. Mol Cell Endocrinol,2012,349(1):56-61.
[83]	CHASSARD D,BUR I,POIREL V J,et al.Evidence for a putative circadian kiss-clock in the hypothalamic AVPV in female mice[J]. Endocrinology,2015,156(8):2999-3011.
[84]	BITTMAN E L.Circadian function in multiple cell types is necessary for proper timing of the preovulatory LH surge[J]. J Biol Rhythms,2019,34(6):622-633.
[85]	TSUTSUMI R,WEBSTER N J G.GnRH pulsatility,the pituitary response and reproductive dysfunction[J]. Endocr J,2009,56(6):729-737.
[86]	CHU A,ZHU L,BLUM I D,et al.Global but not gonadotrope-specific disruption of Bmal 1 abolishes the luteinizing hormone surge without affecting ovulation[J]. Endocrinology,2013,154(8):2924-2935.
[87]	CALLEJO J,JÁUREGUI M T,VALLS C,et al.Heterotopic ovarian transplantation without vascular pedicle in syngeneic lewis rats:six-month control of estradiol and follicle-stimulating hormone concentrations after intraperitoneal and subcutaneous implants[J]. Fertil Steril,1999,72(3):513-517.
[88]	FAHRENKRUG J,GEORG B,HANNIBAL J,et al.Diurnal rhythmicity of the clock genes Per 1 and Per 2 in the rat ovary[J]. Endocrinology,2006,147(8):3769-3776.
[89]	YOSHIKAWA T,SELLIX M,PEZUK P,et al.Timing of the ovarian circadian clock is regulated by gonadotropins[J]. Endocrinology,2009,150(9):4338-4347.
[90]	DUTTA R K,CHINNAPAIYAN S,RASMUSSEN L,et al.A neutralizing aptamer to TGFBR2 and miR-145 antagonism rescue cigarette smoke-and TGF-β-mediated CFTR expression[J]. Mol Ther,2019,27(2):442-455.
[91]	SUN E,SHI Y H.MicroRNAs:small molecules with big roles in neurodevelopment and diseases[J]. Exp Neurol,2015,268:46-53.
[92]	CHENG H Y,PAPP J W,VARLAMOVA O,et al.Microrna modulation of circadian-clock period and entrainment[J]. Neuron, 2007,54(5):813-829.
[93]	WANG W,HE X Y,DI R,et al.Transcriptome analysis revealed long non-coding RNAs associated with mRNAs in sheep thyroid gland under different photoperiods[J]. Genes (Basel),2022,13(4):606.
[94]	HE X Y,DI R,GUO X F,et al.Transcriptomic changes of photoperiodic response in the hypothalamus were identified in ovariectomized and estradiol-treated sheep[J]. Front Mol Biosci,2022,9:848144.
[95]	COON S L,MUNSON P J,CHERUKURI P F,et al.Circadian changes in long noncoding RNAs in the pineal gland[J]. Proc Natl Acad Sci U S A,2012,109(33):13319-13324.

Advances in the Regulation of Mammal Reproduction by the Interaction of Circadian Rhythm and Estrogens

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References 95

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	SHEN Yingchao, DAVSHILT Toli, REN Hong, WANG Xisheng, TIAN Shuyue, DU Ming, DUGARJAVIIN Manglai, BOU Gerelchimeg. Differential Expression of Oocyte Development-related Hormone and Growth Factor Receptors in Equine Expanded and Compact Cumulus-oocyte Complexes [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(9): 3735-3744.
[2]	XU Chunlin, CAO Yuzhu, XIA Tian, JIA Qihui, WANG Dandan, ZHENG Hang, TIAN Yadong, KANG Xiangtao, JIANG Ruirui, LIU Xiaojun, LI Hong. Biological Characteristics and Expression Regulation of Chicken Microsomal Triglyceride Transfer Protein Like Gene [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(9): 2900-2911.
[3]	DING Ziqiang, GE Wenbo, DUAN Hongwei, LÜ Jianshu, ZENG Jianlin, WANG Wenjuan, NIU Tian, ZHANG Yong, ZHAO Xingxu, HU Junjie. Dihydrotestosterone Affects Sheep Uterine Function through Regulating Progesterone, Oestrogen and Apoptosis [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(9): 2993-3005.
[4]	TANG Ziwen, CHENG Huaqin, LIU Dongju, PHAGMO Droma, YANG Xue, LI Jian, YIN Shi. The Protective Effect of Proanthocyanidins on Oxidative Damage of Yak Granulosa Cells Induced by Zearalenone [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(9): 3006-3017.
[5]	WANG Qianmei, YUAN Ligang, LI Chengye, YANG Hongzao, CHEN Shaoyu. Distribution of Sex Hormone Receptors in Cryptorchidism and Normal Testes of Ziwuling Black Goat [J]. Acta Veterinaria et Zootechnica Sinica, 2020, 51(6): 1455-1465.
[6]	YANG Yue, GUO Zeming, HAN Haoshu, LI Weitian, GAO Ting, WANG Xintong, CHEN Yaoxing. Effect of Acute Sleep Deprivation on Melatonin Level of Plasma and Clock Gene Expression of Hypothalamus in Mice [J]. Acta Veterinaria et Zootechnica Sinica, 2020, 51(10): 2609-2612.
[7]	WEI Yuanyuan, CUI Yuqing, HAN Chao, ZHONG Xiuhui, BAO Yongzhan, SHI Wanyu. Reproductive Injury Effects of Bisphenol A Exposure during Pregnancy on Offspring Adult Females [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(7): 1466-1474.
[8]	HE Xiaoyun, LIU Qiuyue, CHU Mingxing. Advances in miRNA Regulating Mammalian Follicular Development and Oocyte Maturation [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(11): 2175-2185.
[9]	ZHANG Cui, CHEN Weina, LI Junliang, GU Shukai, XU Da, LI Dongjie, LI Shijie. Abnormal Expression of LINC24065 in Somatic Cell Nuclear Transfer Cattle [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(1): 44-51.
[10]	ZHANG Yan-yan, PENG Hui, XIAO Tian-fang. Research Progress of Trophectoderm Development of Early Embryo in Mammals [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(10): 2080-2085.
[11]	JING Xiao-yan, ZHANG Cai-xia, SONG Yan-fang, LIU Dong-yu, LIU Di, YANG Xiu-qin. Trans-splicing and Its Roles in Mammals [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(10): 2070-2079.
[12]	LI Ting, MA Ai-tuan, LIU Yue-qin, GAO Kun, ZHANG Ji-wei, ZHANG Ying-jie. Effects of Inhibin on the Secretion of Estrogen, Progesterone and Expressions of Related Genes in Sheep Granulosa Cells [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2017, 48(9): 1648-1653.
[13]	LI Tao-tao, MA You-ji, ZHAO Xing-xu. Research Progress on Reproduction Regulation of SOX9 Gene in Male Mammals [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2017, 48(6): 971-978.
[14]	TIAN Fang-yuan, WANG Tai-an, LI Yan-min, LI Cui-cui, MA Zheng, KANG Xiang-tao, TIAN Ya-dong, LIU Xiao-jun. Cloning and Expression Characteristics of MOGAT and DGAT Genes in Chicken (Gallus gallus) [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2017, 48(2): 214-224.
[15]	GAN Mai-lin, YANG Da-hong, TAN Ya, YANG Qiong, PU Hong-zhou, ZHANG Shun-hua, ZHU Li. The Study of Influence of Environment on Transgenerational Inheritance of DNA Methylation in Mammals [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2017, 48(12): 2225-2231.