哺乳动物原始卵泡形成与发育的研究进展

doi:10.11843/j.issn.0366-6964.2020.03.002

Abstract

Abstract: In most female mammals, the migration of primordial germ cells, germ cells meiosis, and breakdown of germ cell nests are regarded as the 3 critical processes for the formation of early primordial follicles. In addition, there are some special factors and signaling pathways regulating the formation and development of primordial follicles. However, the reproductive ability of a female is determined by the size and reserve capacity of her primordial follicle pool. This review summarizes the factors and signaling pathways involved in the formation and development of primordial follicles, with the aim of understanding the cellular and molecular mechanisms and providing research ideas for maintaining the primordial follicle pool and promoting primordial follicle activation.

Key words: mammal, ovary, primordial follicle, formation and development, signaling pathway

CLC Number:

S821.3

YANG Meixia, ZHANG Yufang, TANG Yaru, ZHANG Hongliang, WANG Shuilian. Research Progresses on the Formation and Development of Primordial Follicles in Mammals[J]. Acta Veterinaria et Zootechnica Sinica, 2020, 51(3): 417-425.

References 67

[1]	WANG C, ZHOU B, XIA G. Mechanisms controlling germline cyst breakdown and primordial follicle formation[J]. Cell Mol Life Sci, 2017, 74(14):2547-2566.
[2]	WEAR H M,MCPIKE M J,WATANABE K H.From primordial germ cells to primordial follicles:a review and visual representation of early ovarian development in mice[J].J Ovarian Res,2016,9(1):36.
[3]	SARRAJ M A, DRUMMOND A E. Mammalian foetal ovarian development:consequences for health and disease[J]. Reproduction, 2012, 143(2):151-163.
[4]	DE SOUSA LOPES S M C,HAYASHI K,SURANI M A.Proximal visceral endoderm and extraembryonic ectoderm regulate the formation of primordial germ cell precursors[J].BMC Dev Biol,2007,7:140.
[5]	KANAMORI M,OIKAWA K,TANEMURA K,et al.Mammalian germ cell migration during development,growth,and homeostasis[J]. Reprod Med Biol,2019,18(3):247-255.
[6]	ARA T,NAKAMURA Y,EGAWA T,et al.Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine,stromal cell-derived factor-1(SDF-1)[J].Proc Natl Acad Sci USA,2003,100(9):5319-5323.
[7]	MOLYNEAUX K A,ZINSZNER H,KUNWAR P S,et al.The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival[J].Development,2003,130(18):4279-4286.
[8]	CANTÚ A V,ALTSHULER-KEYLIN S,LAIRD D J.Discrete somatic niches coordinate proliferation and migration of primordial germ cells via Wnt signaling[J].J Cell Biol,2016,214(2):215-229.
[9]	MCLAREN A.Meiosis and differentiation of mouse germ cells[J].Symp Soc Exp Biol,1984,38:7-23.
[10]	EDSON M A,NAGARAJA A K,MATZUK M M.The mammalian ovary from genesis to revelation[J].Endocr Rev,2009, 30(6):624-712.
[11]	BALTUS A E,MENKE D B,HU Y C,et al.In germ cells of mouse embryonic ovaries,the decision to enter meiosis precedes premeiotic DNA replication[J].Nat Genet,2006,38(12):1430-1434.
[12]	QIU X H,LI M L,LI N,et al.Maternal diabetes impairs the initiation of meiosis in murine female germ cells[J].Mol Med Rep,2017,16(4):5189-5194.
[13]	WANG Y J,TENG Z,LI G,et al.Cyclic AMP in oocytes controls meiotic prophase I and primordial folliculogenesis in the perinatal mouse ovary[J].Development,2015,142(2):343-351.
[14]	FENG Y M,LIANG G J,PAN B,et al.Notch pathway regulates female germ cell meiosis progression and early oogenesis events in fetal mouse[J].Cell Cycle,2014,13(5):782-791.
[15]	KIM S M,YOKOYAMA T,NG D,et al.Retinoic acid-stimulated ERK1/2 pathway regulates meiotic initiation in cultured fetal germ cells[J].PLoS One,2019,14(11):e0224628.
[16]	LIANG G J,ZHANG X F,WANG J J,et al.Activin A accelerates the progression of fetal oocytes throughout meiosis and early oogenesis in the mouse[J].Stem Cells Dev,2015,24(20):2455-2465.
[17]	ZHANG H Q,ZHANG X F,ZHANG L J,et al.Fetal exposure to bisphenol A affects the primordial follicle formation by inhibiting the meiotic progression of oocytes[J].Mol Biol Rep,2012,39(5):5651-5657.
[18]	ELKOUBY Y M,MULLINS M C.Coordination of cellular differentiation,polarity,mitosis and meiosis-new findings from early vertebrate oogenesis[J].Dev Biol,2017,430(2):275-287.
[19]	PEPLING M E,SPRADLING A C.Female mouse germ cells form synchronously dividing cysts[J].Development, 1998, 125(17):3323-3328.
[20]	PEPLING M E,SPRADLING A C.Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles[J]. Dev Biol,2001,234(2):339-351.
[21]	TINGEN C,KIM A,WOODRUFF T K.The primordial pool of follicles and nest breakdown in mammalian ovaries[J].Mol Hum Reprod,2009,15(12):795-803.
[22]	XU J X,GRIDLEY T.Notch2 is required in somatic cells for breakdown of ovarian germ-cell nests and formation of primordial follicles[J].BMC Biol,2013,11:13.
[23]	TROMBLY D J,WOODRUFF T K,MAYO K E.Suppression of Notch signaling in the neonatal mouse ovary decreases primordial follicle formation[J].Endocrinology,2009,150(2):1014-1024.
[24]	CHEN C L,FU X F,WANG L Q,et al.Primordial follicle assembly was regulated by notch signaling pathway in the mice[J].Mol Biol Rep,2014,41(3):1891-1899.
[25]	VANORNY D A,PRASASYA R D,CHALPE A J,et al.Notch signaling regulates ovarian follicle formation and coordinates follicular growth[J].Mol Endocrinol,2014,28(4):499-511.
[26]	YORK J P,REN Y A,ZENG J,et al.Growth arrest specific 2(GAS2) is a critical mediator of germ cell cyst breakdown and folliculogenesis in mice[J].Sci Rep,2016,6:34956.
[27]	HUANG K,WANG Y,ZHANG T,et al.JAK signaling regulates germline cyst breakdown and primordial follicle formation in mice[J].Biol Open,2018,7(1):bio029470.
[28]	NIU W B,WANG Y,WANG Z P,et al.JNK signaling regulates E-cadherin junctions in germline cysts and determines primordial follicle formation in mice[J].Development,2016,143(10):1778-1787.
[29]	XU J J,HUANG J J,PAN Q J,et al.Gestational diabetes promotes germ cell cCyst breakdown and primordial follicle formation in newborn mice via the AKT signaling pathway[J].PLoS One,2019,14(4):e0215007.
[30]	CHEN Y,JEFFERSON W N,NEWBOLD R R,et al.Estradiol,progesterone,and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo[J].Endocrinology,2007,148(8):3580-3590.
[31]	LEI L,JIN S Y,MAYO K E,et al.The interactions between the stimulatory effect of follicle-stimulating hormone and the inhibitory effect of estrogen on mouse primordial folliculogenesis[J].Biol Reprod,2010,82(1):13-22.
[32]	MU X Y,LIAO X G,CHEN X M,et al.DEHP exposure impairs mouse oocyte cyst breakdown and primordial follicle assembly through estrogen receptor-dependent and independent mechanisms[J].J Hazard Mater,2015,298:232-240.
[33]	KARAVAN J R,PEPLING M E.Effects of estrogenic compounds on neonatal oocyte development[J].Reprod Toxicol,2012, 34(1):51-56.
[34]	MAKKER A,GOEL M M,MAHDI A A.PI3K/PTEN/Akt and TSC/mTOR signaling pathways,ovarian dysfunction,and infertility:an update[J].J Mol Endocrinol,2014,53(3):R103-R118.
[35]	VADLAKONDA L,DASH A,PASUPULETI M,et al.The paradox of Akt-mTOR interactions[J].Front Oncol,2013,3:165.
[36]	ZHENG W J,NAGARAJU G,LIU Z L,et al.Functional roles of the phosphatidylinositol 3-kinases (PI3Ks) signaling in the mammalian ovary[J].Mol Cell Endocrinol,2012,356(1-2):24-30.
[37]	ZHOU S,YAN W,SHEN W,et al.Low expression of SEMA6C accelerates the primordial follicle activation in the neonatal mouse ovary[J].J Cell Mol Med,2018,22(1):486-496.
[38]	SOBINOFF A P,NIXON B,ROMAN S D,et al.Staying alive:PI3K pathway promotes primordial follicle activation and survival in response to 3MC-induced ovotoxicity[J].Toxicol Sci,2012,128(1):258-271.
[39]	ADHIKARI D,RISAL S,LIU K,et al.Pharmacological inhibition of mTORC1 prevents over-activation of the primordial follicle pool in response to elevated PI3K signaling[J].PLoS One,2013,8(1):e53810.
[40]	ZHOU L Y,XIE Y Q,LI S,et al.Rapamycin prevents cyclophosphamide-induced over-activation of primordial follicle pool through PI3K/Akt/mTOR signaling pathway in vivo[J].J Ovarian Res,2017,10(1):56.
[41]	JANG H,LEE O H,LEE Y,et al.Melatonin prevents cisplatin-induced primordial follicle loss via suppression of PTEN/AKT/FOXO3a pathway activation in the mouse ovary[J].J Pineal Res,2016,60(3):336-347.
[42]	GROSBOIS J,DEMEESTERE I.Dynamics of PI3K and Hippo signaling pathways during in vitro human follicle activation[J]. Hum Reprod,2018,33(9):1705-1714.
[43]	BEZERRA M É S,BARBERINO R S,MENEZES V G,et al.Insulin-like growth factor-1(IGF-1) promotes primordial follicle growth and reduces DNA fragmentation through the phosphatidylinositol 3-kinase/protein kinase B (PI3K/AKT) signalling pathway[J].Reprod Fertil Dev,2018,30(11):1503-1513.
[44]	VANORNY D A,MAYO K E.The role of Notch signaling in the mammalian ovary[J].Reproduction,2017,153(6):R187-R204.
[45]	TERAUCHI K J,SHIGETA Y,IGUCHI T,et al.Role of Notch signaling in granulosa cell proliferation and polyovular follicle induction during folliculogenesis in mouse ovary[J].Cell Tissue Res,2016,365(1):197-208.
[46]	WANG L Q,LIU J C,CHEN C L,et al.Regulation of primordial follicle recruitment by cross-talk between the Notch and phosphatase and tensin homologue (PTEN)/AKT pathways[J].Reprod Fertil Dev,2016,28(6):700-712.
[47]	GUO M,ZHANG H,BIAN F H,et al.P4 down-regulates Jagged2 and Notch1 expression during primordial folliculogenesis[J]. Front Biosci (Elite Ed),2012,4:2631-2644.
[48]	REISS K,SAFTIG P.The "A Disintegrin and Metalloprotease" (ADAM) family of sheddases:physiological and cellular functions[J]. Semin Cell Dev Biol,2009,20(2):126-137.
[49]	FENG L Z,WANG Y J,CAI H,et al.ADAM10-Notch signaling governs the recruitment of ovarian pregranulosa cells and controls folliculogenesis in mice[J].J Cell Sci,2016,129(11):2202-2212.
[50]	MANOVA K,HUANG E J,ANGELES M,et al.The expression pattern of the c-kit ligand in gonads of mice supports a role for the c-kit receptor in oocyte growth and in proliferation of spermatogonia[J].Dev Biol,1993,157(1):85-99.
[51]	JONES R L,PEPLING M E.KIT signaling regulates primordial follicle formation in the neonatal mouse ovary[J].Dev Biol,2013,382(1):186-197.
[52]	PARROTT J A,SKINNER M K.Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis[J].Endocrinology,1999,140(9):4262-4271.
[53]	HUTT K J,MCLAUGHLIN E A,HOLLAND M K.KIT/KIT ligand in mammalian oogenesis and folliculogenesis:roles in rabbit and murine ovarian follicle activation and oocyte growth[J].Biol Reprod,2006,75(3):421-433.
[54]	GOUGEON A,DELANGLE A,AROUCHE N,et al.Kit ligand and the somatostatin receptor antagonist,BIM-23627,stimulate in vitro resting follicle growth in the neonatal mouse ovary[J].Endocrinology,2010,151(3):1299-1309.
[55]	CAVALCANTE A Y P,GOUVEIA B B,BARBERINO R S,et al.Kit ligand promotes the transition from primordial to primary follicles after in vitro culture of ovine ovarian tissue[J].Zygote,2016,24(4):578-582.
[56]	KNAPCZYK-STWORA K,GRZESIAK M,DUDA M,et al.Effect of flutamide on folliculogenesis in the fetal porcine ovary-regulation by Kit ligand/c-Kit and IGF1/IGF1R systems[J].Anim Reprod Sci,2013,142(3-4):160-167.
[57]	PEARSON G,ROBINSON F,GIBSON T B,et al.Mitogen-Activated Protein (MAP) kinase pathways:regulation and physiological functions[J]. Endocr Rev,2001,22(2):153-183.
[58]	DAVIS R J.Signal transduction by the JNK group of MAP kinases[J].Cell,2000,103(2):239-252.
[59]	ZHENG L P,ZHANG D L,HUANG J,et al.Proto-oncogene c-erbB2 initiates rat primordial follicle growth via PKC and MAPK pathways[J].Reprod Biol Endocrinol,2010,8:66.
[60]	ZHAO Y,ZHANG Y,LI J,et al.MAPK3/1 participates in the activation of primordial follicles through mTORC1-KITL signaling[J]. J Cell Physiol,2018,233(1):226-237.
[61]	ROSS S,HILL C S.How the Smads regulate transcription[J].Int J Biochem Cell Biol,2008,40(3):383-408.
[62]	DING X Y,ZHANG X L,MU Y L,et al.Effects of BMP4/SMAD signaling pathway on mouse primordial follicle growth and survival via up-regulation of Sohlh2 and c-kit[J].Mol Reprod Dev,2013,80(1):70-78.
[63]	XIANG C,LI J,HU L L,et al.Hippo signaling pathway reveals a spatio-temporal correlation with the size of primordial follicle pool in mice[J].Cell Physiol Biochem,2015,35(3):957-968.
[64]	HU L L,SU T,LUO R C,et al.Hippo pathway functions as a downstream effector of AKT signaling to regulate the activation of primordial follicles in mice[J].J Cell Physiol,2019,234(2):1578-1587.
[65]	DICKINSON R E,MYERS M,DUNCAN W C.Novel regulated expression of the SLIT/ROBO pathway in the ovary:possible role during luteolysis in women[J].Endocrinology,2008,149(10):5024-5034.
[66]	DICKINSON R E,HRYHORSKYJ L,TREMEWAN H,et al.Involvement of the SLIT/ROBO pathway in follicle development in the fetal ovary[J].Reproduction,2010,139(2):395-407.
[67]	BERTOLDO M J,BERNARD J,DUFFARD N,et al.Inhibitors of c-Jun phosphorylation impede ovine primordial follicle activation[J].Mol Hum Reprod,2016,22(5):338-349.

Research Progresses on the Formation and Development of Primordial Follicles in Mammals

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References 67

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	TIAN Qihui, ZHANG Liang, LONG Yali. Study on the Effect of Astragalus on Proliferation of Bone Marrow Mesenchymal Stem Cells in Anoxic Microenvironment based on PI3K-AKT Signal Pathway [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(1): 346-354.
[2]	HAN Kunliang, LAN Wei, HU Xin, CUI Yadong, KONG Xiangfeng. Effects of Compound Chinese Herb Ultrafine Powder on Antioxidant Ability and Related Gene Expression in Laying Hens [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(9): 3784-3792.
[3]	LI Yuexin, LIU Aiju, MA Xiaofei, ZHENG Zhong, HU Boxin, ZHI Yunxia, TIAN Shujun. Effect of TGFβR1 on the Function of Sheep Granulosa Cells Mediated by TGF-β/Smad Signaling Pathway [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(8): 3335-3347.
[4]	ZHANG Peng, WANG Mingxiu, JING Kemin, PENG Wei, TIAN Yuan, LI Yuqian, FU Changqi, SHU Shi, ZHONG Jincheng, CAI Xin. Abnormal Expression of FGFs/FGFRs and Their Mediated Signaling Pathway Genes Affect the Proliferative Activity of Undifferentiated Spermatogonia in Cattleyak [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(7): 2886-2897.
[5]	XU Tiantian, ZHANG Tongtong, WANG Meng, WANG Xin. Transcription Factor Foxq1 Affects the Proliferation of Hair Follicle Stem Cells in Cashmere Goats via WNT/β-catenin Signaling Pathway [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(6): 2653-2661.
[6]	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.
[7]	CHEN Yongping, KOU Yuhong, JIAO Wenjing, HOU Xiaoyu, FAN Honggang. Effect of Coenzyme Q10 on LPS-induced Acute Lung Injury in Mice [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(4): 1730-1741.
[8]	LIAO Weili, ZHANG Xiaoke, ZENG Jianhua, YANG Linfang, LI Shuo, HU Mengting, GUO Yixuan, CHEN Zanmou, ZHANG Hao, LI Jiaqi, YUAN Xiaolong. Associations between FOXL2 Polymorphism and Several Important Economic Traits in Liangguang Spotted Pigs [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(3): 956-965.
[9]	ZHANG Chengcheng, SUN Jiahao, WANG Xiuling, ZHANG Xiaorong, WU Yantao. Beclin1 Interacts with the Nonstructural Protein NS5A of CSFV and Promotes Virus Proliferation [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(2): 715-725.
[10]	REN Xiujuan, KANG Decuo, SU Shaofeng, LIN Yanan, LI Yajing, DU Ming, BAI Dongyi, LI Bei, ZHAO Yiping, DUGARJAVIIN Manglai. Comparison of Immune Gene Expression between Mongolian Horse and Thoroughbred [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(12): 5020-5032.
[11]	LUO Ju, MAO Jiani, XIA Yinzhao, YANG Zhenguo. Regulation of circRNAs on Mammalian Intestinal Barrier Function [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(11): 4439-4448.
[12]	XING Wenwen, QI Nannan, LI Mengxuan, LIU Jiying. Research Progress on the Mechanism of YY1 and Its Role in the Regulation of Animal Reproduction [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(10): 4040-4049.
[13]	ZHAO Yaya, CHANG Jiang, JU Ning, LUO Yulong. Mechanism of Plant Polyphenols Addition in Diet Regulating Meat Color Stability [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(1): 36-47.
[14]	LIU Lihua, ZHONG Zhenyu, ZHENG Yujie, WANG Xin. lncRNA EPB41L4A-AS Inhibits the Proliferation of Bovine Mammary Epithelial Cells by Regulating the Expression of ErbB3 Gene [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(7): 2152-2159.
[15]	ZHANG Yuchen, LEI Yaping, NONG Bidan, PANG Xiaomin, ZHANG Miaomiao, LIU Xiaoli, GU Changqin, ZHANG Wanpo, CHENG Guofu, HU Xueying. Pathological Observation on the Ovary of Laying Ducks after Natural Infection with Duck Tembusu Virus [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(7): 2326-2332.