蛋鸡卵泡发育及其表观遗传调控机制研究进展

doi:10.11843/j.issn.0366-6964.2023.09.003

摘要/Abstract

摘要： 家禽的繁殖性能、产蛋性能与卵泡的正常发育和排卵密切相关。家禽卵巢中大部分的卵泡在发育过程中发生闭锁,只有大约不到5%的卵泡可以从原始卵泡发育至成熟卵泡并排卵。鸡的卵泡发育主要受内在因素(激素和细胞因子等)和外在因素(营养水平等)调节。近来,越来越多的研究发现表观遗传也在卵泡发育中起着重要的调控作用。表观遗传学是指在DNA序列不发生改变的情况下,基因表达及表型产生可遗传的变化。因此,文章综述了蛋鸡卵泡发育的过程及主要影响因素,同时从DNA甲基化、组蛋白修饰、非编码RNA调控以及RNA修饰4个方面综述了表观遗传在卵泡发育中的可能调控机制,旨在为提高家禽生产性能提供一定的理论基础。

关键词: 蛋鸡, 卵泡发育, 影响因素, 表观遗传

Abstract: The reproductive performance and egg production performance of poultry is closely related to follicles development and ovulation. In poultry ovaries, less than 5% of follicles can develop from primordial follicle to mature follicle and ovulate, and most follicles become atresia during development. The development of follicles is influenced by intrinsic factors and extrinsic factors. Recently, many studies have found that epigenetic mechanism also plays an important role in the regulation of follicle development. Epigenetics is heritable changes in gene expression and phenotype without changing in the DNA sequence. Therefore, the review described the process of follicle development and the main influencing factors in follicle development in laying hens. Moreover, in this review, the possible epigenetics regulatory mechanisms including DNA methylation, histone modification, non-coding RNA regulation and RNA modification in follicle development were summarized. In conclusion, the review provides a theoretical basis for improving poultry production performance.

Key words: laying hens, follicle development, influence factors, epigenetics

中图分类号:

S831.3

茹盟, 曾文惠, 彭剑玲, 曾庆节, 殷超, 崔勇, 魏庆, 梁海平, 谢贤华, 黄建珍. 蛋鸡卵泡发育及其表观遗传调控机制研究进展[J]. 畜牧兽医学报, 2023, 54(9): 3613-3622.

RU Meng, ZENG Wenhui, PENG Jianling, ZENG Qingjie, YIN Chao, CUI Yong, WEI Qing, LIANG Haiping, XIE Xianhua, HUANG Jianzhen. Research Progress on Follicles Development of Hens and Its Epigenetic Regulatory Mechanism[J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(9): 3613-3622.

参考文献

[1] KRALIK G,KRALIK Z.Poultry products enriched with nutricines have beneficial effects on human health[J].Med Glas (Zenica),2017,14(1):1-7.
[2] JOHNSON A L.Regulation of follicle differentiation by gonadotropins and growth factors[J].Poult Sci,1993,72(5):867-873.
[3] 张俊楠,孙志华,徐桂云.家禽卵泡发育与调控机制研究进展[J].中国家禽, 2021,43(5):1-7.
ZHANG J N,SUN Z H,XU G Y.Research progress on development and regulatory mechanism of poultry follicles[J].China Poultry, 2021, 43(5):1-7.(in Chinese)
[4] 李桂明.热应激影响蛋鸡等级前卵泡发育的机理研究[D].泰安:山东农业大学,2020.
LI G M.Studies on mechanisms of prehierarchical follicle development affected by heat stress in laying hens[D].Taian:Shandong Agricultural University,2020.(in Chinese)
[5] GURAYA S S,CHALANA R K.Morphology of the post-ovulatory follicle of house sparrow[J].Acta Biol Acad Sci Hung,1976, 27(4):261-267.
[6] ONAGBESAN O,BRUGGEMAN V,DECUYPERE E.Intra-ovarian growth factors regulating ovarian function in avian species:a review[J]. Anim Reprod Sci,2009,111(2-4):121-140.
[7] LIN X,LIU X T,GUO C Q,et al.Promotion of the prehierarchical follicle growth by postovulatory follicles involving PGE₂-EP2 signaling in chickens[J].J Cell Physiol,2018,233(11):8984-8995.
[8] HRABIA A,SOCHA J K,SECHMAN A.Involvement of matrix metalloproteinases (MMP-2,-7,-9) and their tissue inhibitors (TIMP-2,-3) in the regression of chicken postovulatory follicles[J].Gen Comp Endocrinol,2018,260:32-40.
[9] JOHNSON A L,WOODS D C.Dynamics of avian ovarian follicle development:cellular mechanisms of granulosa cell differentiation[J].Gen Comp Endocrinol,2009,163(1-2):12-17.
[10] 林欣.蛋鸡退化卵泡衰退的机制及其功能的研究[D].杭州:浙江大学,2018.
LIN X.Degradation and functions of the regressed ovarian follicles in the laying chicken[D].Hangzhou:Zhejiang University,2018.(in Chinese)
[11] MA Y F,YAO J W,ZHOU S,et al.Enhancing effect of FSH on follicular development through yolk formation and deposition in the low-yield laying chickens[J].Theriogenology,2020,157:418-430.
[12] LIN X,MA Y F,QIAN T F,et al.Basic fibroblast growth factor promotes prehierarchical follicle growth and yolk deposition in the chicken[J].Theriogenology,2019,139:90-97.
[13] GHANEM K,JOHNSON A L.Proteome profiling of chicken ovarian follicles immediately before and after cyclic recruitment[J]. Mol Reprod Dev,2021,88(8):571-583.
[14] GHANEM K,JOHNSON A L.Relationship between cyclic follicle recruitment and ovulation in the hen ovary[J].Poult Sci,2019, 98(7):3014-3021.
[15] DONG J,GUO C Q,ZHOU S,et al.Leukemia inhibitory factor prevents chicken follicular atresia through PI3K/AKT and Stat3 signaling pathways[J].Mol Cell Endocrinol,2022,543:111550.
[16] JIANG B Y,CAO B L,ZHOU Z C,et al.Characterization of chicken α_2a-adrenoceptor:molecular cloning,functional analysis,and its involvement in ovarian follicular development[J].Genes (Basel),2022,13(7):1113.
[17] STEPHENS C S,HILL-RICCIUTI A,FRANCOEUR L,et al.Feeding level is associated with altered liver transcriptome and follicle selection in hen[J].Biol Reprod,2022,106(5):943-952.
[18] SHEN M M,LI T T,ZHANG G X,et al.Dynamic expression and functional analysis of circRNA in granulosa cells during follicular development in chicken[J].BMC Genomics,2019,20(1):96.
[19] SHEN M,LI T,FENG Y,et al.Exploring the expression and preliminary function of chicken regulator of G protein signalling 3(RGS3) gene in follicular development[J].Br Poult Sci,2022,63(5):613-620.
[20] ZHOU J W,PENG X W,MEI S Q.Autophagy in ovarian follicular development and atresia[J].Int J Biol Sci,2019,15(4):726-737.
[21] BHARDWAJ J K,PALIWAL A,SARAF P,et al.Role of autophagy in follicular development and maintenance of primordial follicular pool in the ovary[J].J Cell Physiol,2022,237(2):1157-1170.
[22] LEOPARDO N P,VELAZQUEZ M E,CORTASA S,et al.A dual death/survival role of autophagy in the adult ovary of Lagostomus maximus (Mammalia-Rodentia)[J].PLoS One,2020,15(5):e0232819.
[23] GAWRILUK T R,HALE A N,FLAWS J A,et al.Autophagy is a cell survival program for female germ cells in the murine ovary[J].Reproduction,2011,141(6):759-765.
[24] WU G,LI C Y,TAO J L,et al.FSH mediates estradiol synthesis in hypoxic granulosa cells by activating glycolytic metabolism through the HIF-1α-AMPK-GLUT1 signaling pathway[J].J Biol Chem,2022,298(5):101830.
[25] MA L Z,ZHENG Y X,TANG X R,et al.miR-21-3p inhibits autophagy of bovine granulosa cells by targeting VEGFA via PI3K/AKT signaling[J].Reproduction,2019,158(5):441-452.
[26] MAGGI R,CARIBONI A M,MARELLI M M,et al.GnRH and GnRH receptors in the pathophysiology of the human female reproductive system[J].Hum Reprod Update,2016,22(3):358-381.
[27] PRASTIYA R A,MADYAWATI S P,SARI S Y,et al.Effect of follicle-stimulating hormone and luteinizing hormone levels on egg-laying frequency in hens[J].Vet World,2022,15(12):2890-2895.
[28] TENA-SEMPERE M.Ghrelin and reproduction:ghrelin as novel regulator of the gonadotropic axis[J].Vitam Horm,2007, 77:285-300.
[29] NAVARRO V M.Metabolic regulation of kisspeptin-the link between energy balance and reproduction[J].Nat Rev Endocrinol, 2020,16(8):407-420.
[30] CHRISTOFFERSEN B Ø,SANCHEZ-DELGADO G,JOHN L M,et al.Beyond appetite regulation:targeting energy expenditure, fat oxidation,and lean mass preservation for sustainable weight loss[J].Obesity (Silver Spring),2022,30(4):841-857.
[31] 李敬.circEML1通过gga-miR-449a/IGF2BP3轴调控蛋鸡卵泡颗粒细胞类固醇激素合成和分泌的分子机制[D].郑州:河南农业大学,2022:131.
LI J.circEML1 modulates steroid synthesis and secretion of hen's follicular granulosa cells via targeting the gga-miR-449a/IGF2BP3 axis[D].Zhengzhou:Henan Agricultural University,2022:131.(in Chinese)
[32] 李琴,王启贵.TGF-β家族成员调控家禽卵泡发育的研究进展及展望[J].中国家禽,2019,41(19):1-5.
LI Q,WANG Q G.The role of TGF-β family members in avian follicle development[J].China Poultry,2019,41(19):1-5.(in Chinese)
[33] ZHOU S,MA Y F,YAO J W,et al.TGF-β1-induced collagen promotes chicken ovarian follicle development via an intercellular cooperative pattern[J].Cell Biol Int,2021,45(6):1336-1348.
[34] 陈林,李刚,徐光明,等.表皮生长因子影响家禽卵泡发育机制的研究进展[J].中国畜牧杂志,2022,58(12):41-46.
CHEN L,LI G,XU G M,et al.Research progress on the mechanism of epidermal growth factor (EGF) affecting follicle development in poultry[J].Chinese Journal of Animal Science,2022,58(12):41-46.(in Chinese)
[35] ONAGBESAN O,BRUGGEMAN V,DECUYPERE E.Intra-ovarian growth factors regulating ovarian function in avian species:a review[J].Anim Reprod Sci,2009,111(2-4):121-140.
[36] BERMUDEZ B,ISHII T,WU Y H,et al.Energy balance and bone health:a nutrient availability perspective[J].Curr Osteoporos Rep,2023,21(1):77-84.
[37] WALZEM R L,CHEN S E.Obesity-induced dysfunctions in female reproduction:lessons from birds and mammals[J].Adv Nutr,2014,5(2):199-206.
[38] YAO Y,WANG H H,YANG Y,et al.Dehydroepiandrosterone activates the GPER-mediated AMPK signaling pathway to alleviate the oxidative stress and inflammatory response in laying hens fed with high-energy and low-protein diets[J].Life Sci,2022, 308:120926.
[39] ZHANG Q L,WANG Y,LIU J S,et al.Effects of hypercaloric diet-induced hyperinsulinemia and hyperlipidemia on the ovarian follicular development in mice[J].J Reprod Dev,2022,68(3):173-180.
[40] VARLAMOV O.Western-style diet,sex steroids and metabolism[J].Biochim Biophys Acta (BBA):Mol Basis Dis,2017,1863(5):1147-1155.
[41] LU J,LI Y F,QU L,et al.Effects of energy-restricted feeding during rearing on sexual maturation and reproductive performance of Rugao layer breeders[J].Poult Sci,2021,100(8):101225.
[42] LI G M,LIU L P,YIN B,et al.Heat stress decreases egg production of laying hens by inducing apoptosis of follicular cells via activating the FasL/Fas and TNF-α systems[J].Poult Sci,2020,99(11):6084-6093.
[43] 李先强,王家乡,吴艳,等.遮光诱导的氧化应激对蛋鸡卵泡发育的影响[J].中国畜牧杂志,2022,58(4):188-194.
LI X Q,WANG J X,WU Y,et al.Effects of oxidative stress induced by shading on follicle development in laying hens[J].Chinese Journal of Animal Science,2022,58(4):188-194.(in Chinese)
[44] CAO X H,GUO L Y,ZHOU C M,et al.Effects of N-acetyl-l-cysteine on chronic heat stress-induced oxidative stress and inflammation in the ovaries of growing pullets[J].Poult Sci,2023,102(1):102274.
[45] GONNELLA F,KONSTANTINIDOU F,DI BERARDINO C,et al.A systematic review of the effects of high-fat diet exposure on oocyte and follicular quality:a molecular point of view[J].Int J Mol Sci,2022,23(16):8890.
[46] CHEN Z Y,ZHANG Y.Role of mammalian DNA methyltransferases in development[J].Annu Rev Biochem,2020,89:135-158.
[47] WEIZMAN N F,WYSE B A,MONTBRIAND J,et al.Cannabis significantly alters DNA methylation of the human ovarian follicle in a concentration-dependent manner[J].Mol Hum Reprod,2022,28(7):gaac022.
[48] LIU Y N,QIN Y,WU B,et al.DNA methylation in polycystic ovary syndrome:emerging evidence and challenges[J].Reprod Toxicol,2022,111:11-19.
[49] QU F,WANG F F,YIN R,et al.A molecular mechanism underlying ovarian dysfunction of polycystic ovary syndrome:hyperandrogenism induces epigenetic alterations in the granulosa cells[J].J Mol Med (Berl),2012,90(8):911-923.
[50] SANG Q,LI X,WANG H J,et al.Quantitative methylation level of the EPHX1 promoter in peripheral blood DNA is associated with polycystic ovary syndrome[J].PLoS One,2014,9(2):e88013.
[51] LI S X,ZHU D Y,DUAN H M,et al.Differential DNA methylation patterns of polycystic ovarian syndrome in whole blood of Chinese women[J].Oncotarget,2017,8(13):20656-20666.
[52] KANWAL R,GUPTA K,GUPTA S.Cancer epigenetics:an introduction[M]//VERMA M.Cancer Epigenetics.New York:Humana Press,2015:3-25.
[53] 薛倩,李国辉,殷建玫,等.鸡繁殖性能近交衰退相关CpG岛差异甲基化基因的筛选[J].畜牧兽医学报,2021,52(4):943-953.
XUE Q,LI G H,YIN J M,et al.Screening of genes with differential methylated CpG island related to inbreeding depression of chicken reproduction[J].Acta Veterinaria et Zootechnica Sinica,2021,52(4):943-953.(in Chinese)
[54] ZHAO J B,PAN H B,LIU Y,et al.Interacting networks of the hypothalamic-pituitary-ovarian axis regulate layer hens performance[J].Genes (Basel),2023,14(1):141.
[55] BARUA A,BAHR J M.Ovarian cancer:applications of chickens to humans[J].Annu Rev Anim Biosci,2022,10:241-257.
[56] ROY S,SINHA N,HUANG B B,et al.Jumonji Domain-containing protein-3(JMJD3/Kdm6b) is critical for normal ovarian function and female fertility[J].Endocrinology,2022,163(5):bqac047.
[57] STRAHL B D,ALLIS C D.The language of covalent histone modifications[J].Nature,2000,403(6765):41-45.
[58] LAVOIE H A.Epigenetic control of ovarian function:the emerging role of histone modifications[J].Mol Cell Endocrinol,2005, 243(1-2):12-18.
[59] LI D Y,NING C Y,ZHANG J M,et al.Dynamic transcriptome and chromatin architecture in granulosa cells during chicken folliculogenesis[J].Nat Commun,2022,13(1):131.
[60] YE Q H,ZENG X F,WANG S,et al.Butyrate drives the acetylation of histone H3K9 to activate steroidogenesis through PPARγ and PGC1α pathways in ovarian granulosa cells[J].FASEB J,2021,35(2):e21316.
[61] SHEN H J,XU W Q,LAN F.Histone lysine demethylases in mammalian embryonic development[J].Exp Mol Med,2017,49(4):e325.
[62] SHEN H J,XU W Q,LAN F.Histone lysine demethylases in mammalian embryonic development[J].Exp Mol Med,2017,49(4):e325.
[63] XIONG X R,ZHANG X J,YANG M Z,et al.Oocyte-specific knockout of histone lysine demethylase KDM2a compromises fertility by blocking the development of follicles and oocytes[J].Int J Mol Sci,2022,23(19):12008.
[64] LIU Y,KONG F,WANG W Y,et al.Low estrogen level in aged mice leads to abnormal oogenesis affecting the quality of surrounded nucleolus-type immature oocytes[J].Reprod Fertil Dev,2022,34(15):991-1001.
[65] HE C F,WANG K X,GAO Y Y,et al.Roles of noncoding RNA in reproduction[J].Front Genet,2021,12:777510.
[66] ZHANG J B,XU Y X,LIU H L,et al.MicroRNAs in ovarian follicular atresia and granulosa cell apoptosis[J].Reprod Biol Endocrinol,2019,17(1):9.
[67] SONG J Y,MA X C,LI F X,et al.Exposure to multiple pyrethroid insecticides affects ovarian follicular development via modifying microRNA expression[J].Sci Total Environ,2022,828:154384.
[68] WU N,GAUR U,ZHU Q,et al.Expressed microRNA associated with high rate of egg production in chicken ovarian follicles[J]. Anim Genet,2017,48(2):205-216.
[69] KANG L,CUI X X,ZHANG Y J,et al.Identification of miRNAs associated with sexual maturity in chicken ovary by Illumina small RNA deep sequencing[J].BMC Genomics,2013,14:352.
[70] WU X,ZHANG N,LI J,et al.gga-miR-449b-5p regulates steroid hormone synthesis in laying hen ovarian granulosa cells by targeting the IGF2BP3 gene[J].Animals (Basel),2022,12(19):2710.
[71] WAN T,SUN H T,MAO Z L,et al.Vitamin D deficiency inhibits microRNA-196b-5p which regulates ovarian granulosa cell hormone synthesis,proliferation,and apoptosis by targeting RDX and LRRC17[J].Ann Transl Med,2021,9(24):1775.
[72] WANG Y,GUO Z Y,ZI C,et al.CircRNA expression in chicken granulosa cells illuminated with red light[J].Poult Sci,2022, 101(4):101734.
[73] 陈亚楠,李瑞梅,陈晓丽,等.长链非编码RNA与卵泡发育相关性的研究进展[J].生殖医学杂志,2020,29(12):1677-1681.
CHEN Y N,LI R M,CHEN X L,et al.Research progress of correlation between LncRNAs and follicle development[J].Journal of Reproductive Medicine,2020,29(12):1677-1681.(in Chinaese).
[74] PENG Y D,CHANG L,WANG Y Q,et al.Genome-wide differential expression of long noncoding RNAs and mRNAs in ovarian follicles of two different chicken breeds[J].Genomics,2019,111(6):1395-1403.
[75] ZHOU X F,HE Y T,PAN X C,et al.DNMT1-mediated lncRNA IFFD controls the follicular development via targeting GLI1 by sponging miR-370[J].Cell Death Differ,2023,30(2):576-588.
[76] MU H B,CAI S Y,WANG X F,et al.RNA binding protein IGF2BP1 meditates oxidative stress-induced granulosa cell dysfunction by regulating MDM2 mRNA stability in an m⁶A-dependent manner[J].Redox Biol,2022,57:102492.
[77] FAN Y,ZHANG C S,ZHU G Y.Profiling of RNA N6-methyladenosine methylation during follicle selection in chicken ovary[J].Poult Sci,2019,98(11):6117-6124.
[78] GUO S K,WANG X D,CAO M L,et al.The transcriptome-wide N6-methyladenosine (m⁶A) map profiling reveals the regulatory role of m⁶A in the yak ovary[J].BMC Genomics,2022,23(1):358.
[79] CAO Z B,ZHANG D D,WANG Y Q,et al.Identification and functional annotation of m6A methylation modification in granulosa cells during antral follicle development in pigs[J].Anim Reprod Sci,2020,219:106510.