Acta Veterinaria et Zootechnica Sinica ›› 2020, Vol. 51 ›› Issue (3): 417-425.doi: 10.11843/j.issn.0366-6964.2020.03.002
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YANG Meixia, ZHANG Yufang, TANG Yaru, ZHANG Hongliang*, WANG Shuilian*
Received:
2019-10-08
Online:
2020-03-25
Published:
2020-03-20
CLC Number:
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.
[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. |
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