Animal Reproduction (AR)
Animal Reproduction (AR)
Congress Paper

Intrafollicular barriers and cellular interactions during ovarian follicle development

Gabriella Mamede Andrade, Maite del Collado, Flávio Vieira Meirelles, Juliano Coelho da Silveira, Felipe Perecin

Downloads: 2
Views: 1663


Follicles are composed of different interdependent cell types including oocytes, cumulus, granulosa, and theca cells. Follicular cells and oocytes exchange signaling molecules from the beginning of the development of the primordial follicles until the moment of ovulation. The follicular structure transforms during folliculogenesis; barriers form between the germ and the somatic follicular cells, and between the somatic follicular cells. As such, communication systems need to adapt to maintain the exchange of signaling molecules. Two critical barriers are established at different stages of development: the zona pellucida, separating the oocyte and the cumulus cells limiting the communication through specific connections, and the antrum, separating subpopulations of follicular cells. In both situations, communication is maintained either by the development of specialized connections as transzonal projections or by paracrine signaling and trafficking of extracellular vesicles through the follicular fluid. The bidirectional communication between the oocytes and the follicle cells is vital for driving folliculogenesis and oogenesis. These communication systems are associated with essential functions related to follicular development, oocyte competence, and embryonic quality. Here, we discuss the formation of the zona pellucida and antrum during folliculogenesis, and their importance in follicle and oocyte development. Moreover, this review discusses the current knowledge on the cellular mechanisms such as the movement of molecules via transzonal projections, and the exchange of extracellular vesicles by follicular cells to overcome these barriers to support female gamete development. Finally, we highlight the undiscovered aspects related to intrafollicular communication among the germ and somatic cells, and between the somatic follicular cells and give our perspective on manipulating the above-mentioned cellular communication to improve reproductive technologies.


cellular communication, extracellular vesicles, granulosa cells, oocyte, ovarian follicle, transzonal projections


Akers JC, Gonda D, Kim R, Carter BS, Chen CC. 2013. Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J Neurooncol, 113:1-11.

Albertini DF, Barrett SL. 2004. The developmental origins of mammalian oocyte polarity. Semin Cell Dev Biol, 15, 599-606.

Albertini DF, Combelles CMH, Benecchi E, Carabatsos MJ. 2001. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction, 121:647-653.

Ambekar AS, Nirujogi RS, Srikanth SM, Chavan S, Kelkar DS, Hinduja I, Zaveri K, Prasad TSK, Harsha HC, Pandey A, Mukherjee S. 2013. Proteomic analysis of human follicular fluid: A new perspective towards understanding folliculogenesis. J Proteomics, 87:68-77.

Andrade G, Meirelles F, Perecin F, Silveira J. 2017a. Cellular and extracellular vesicular origins of miRNAs within the bovine ovarian follicle. Reprod Domest Anim, 52(6):1036-1045.

Andrade GM, da Silveira JC, Perrini C, Del Collado M, Gebremedhn S, Tesfaye D, Meirelles FV, Perecin F. 2017b. The role of the PI3K-Akt signaling pathway in the developmental competence of bovine oocytes. Plos One, 12.

Ávila ACFM, Andrade GM, Bridi A, Gimenes LU, Meirelles FV, Perecin F, da Silveira JC. 2019. Extracellular vesicles and its advances in female reproduction. Anim Reprod,16:31-38.

Baena V, Terasaki M. 2019. Three-dimensional organization of transzonal projections and other cytoplasmic extensions in the mouse ovarian follicle. Sci Rep, 9(1):1262.

Bleach ECL, Glencross RG, Feist SA, Groome NP, Knight PG. 2001. Plasma inhibin A in heifers: Relationship with follicle dynamics, gonadotropins, and steroids during the estrous cycle and after treatment with bovine follicular fluid. Biol Reprod, 64:743-752.

Bleil JD, Wassarman PM. 1980. Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte's zona pellucida. Dev Biol, 76:185-202.

BrawTal R, Yossefi S. 1997. Studies in vivo and in ivtro on the initiation of follicle growth in the bovine ovary. J Reprod Fertil, 109:165-171.

Buehr M. 1997. The primordial germ cells of mammals: Some current perspectives. Exp Cell Res, 232:194-207.

Byskov AG, Andersen CY, Nordholm L, Thogersen H, Xia GL, Wassmann O, Andersen JV, Guddal E, Roed T. 1995. Chemical-structure of sterols that activate oocyte meiosis. Nature, 374:559-562.

Carabatsos MJ, Elvin J, Matzuk MM, Albertini DF. 1998. Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev Biol, 204:373-384.

Cha K-Y, Barnes RB, Marrs RP, Lobo RA. 1986. Correlation of the bioactivity of luteinizing hormone in follicular fluid with oocyte maturity in the spontaneous cycle. Fertil Steril, 45:338-341.

Chakraborty P, Roy SK. 2017. Stimulation of primordial follicle assembly by estradiol-17 beta requires the action of bone morphogenetic protein-2 (BMP2). Sci Rep, 7(1):15581.

Clarke HJ. 2017. Regulation of germ cell development by intercellular signaling in the mammalian ovarian follicle. Wiley Interdisciplinary Reviews: Dev Biol, 7:e294. Doi: 10.1002/wdev.294.

Clarke HJ. 2018. History, origin, and function of transzonal projections: the bridges of communication between the oocyte and its environment. Anim Reprod, 15:215-223.

Combelles CMH, Carabatsos MJ, Kumar TR, Matzuk MM, Albertini DF. 2004. Hormonal control of somatic cell oocyte interactions during ovarian follicle development. Mol Reprod Dev, 69:347-355.

Conti M, Hsieh M, Zamah AM, Oh JS. 2012. Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Mol Cell Endocrinol, 356:65-73.

Crescitelli R, Lässer C, Szabo TG, Kittel A, Eldh M, Dianzani I, Buzás EI, Lötvall J. 2013. Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles, 2: eCollection 2013. Doi: 10.3402/jev.v2i0.20677.

da Silveira JC, Andrade GM, del Collado M, Sampaio RV, Sangalli JR, Silva LA, Pinaffi FVL, Jardim IB, Cesar MC, Nogueira MFG, Cesar ASM, Coutinho LL, Pereira RW, Perecin F, Meirelles FV. 2017. Supplementation with small-extracellular vesicles from ovarian follicular fluid during in ivtro production modulates bovine embryo development. Plos One, 12(6):e0179451. Doi: 10.1371/journal.pone.0179451.

da Silveira JC, de Andrade GM, Nogueira MFG, Meirelles FV, Perecin F. 2015a. Involvement of mirnas and cell-secreted vesicles in mammalian ovarian antral follicle development. Reprod Sci, 22:1474-1483.

da Silveira JC, Veeramachaneni DNR, Winger QA, Carnevale EM, Bouma GJ. 2012. Cell-Secreted Vesicles in Equine Ovarian Follicular Fluid Contain miRNAs and Proteins: A Possible New Form of Cell Communication Within the Ovarian Follicle. Biol Reprod, 86(3):71. Doi: 10.1095/biolreprod.111.093252.

da Silveira JC, Winger QA, Bouma GJ, Carnevale EM. 2015b. Effects of age on follicular fluid exosomal microRNAs and granulosa cell transforming growth factor-beta signalling during follicle development in the mare. Reprod Fertil Dev, 27:897-905.

Dalanezi F, Destro F, Ferrazza R, García HM, Franchi F, Fontes P, Castilho A, Sartori R, Ferreira J. 2017. 183 Gene expression of in ivtro-maturated oocytes can be modulated by follicle exosomes from cows kept under thermoneutral or heat stress conditions. Reprod Fertil Dev, 29:200-200.

del Collado M, Andrade GM, Meirelles FV, da Silveira JC, Perecin F. 2018. Contributions from the ovarian follicular environment to oocyte function. Anim Reprod, 15:261-270.

del Collado M, da Silveira JC, Sangalli JR, Andrade GM, Sousa L, Silva LA, Meirelles FV, Perecin F. 2017. Fatty acid binding protein 3 and transzonal projections are involved in lipid accumulation during in ivtro maturation of bovine oocytes. Sci Rep, 7:2645. Doi:10.1038/s41598-017-02467-9

Di Pietro C. 2016. Exosome-mediated communication in the ovarian follicle. Journal of Assisted Reproduction and Genetics, 33:303-311.

Diez-Fraile A, Lammens T, Tilleman K, Witkowski W, Verhasselt B, De Sutter P, Benoit Y, Espeel M, D'Herde K. 2014. Age-associated differential microRNA levels in human follicular fluid reveal pathways potentially determining fertility and success of in ivtro fertilization. Hum Fertil, 17:90-98.

Dong JW, Albertini DF, Nishimori K, Kumar TR, Lu NF, Matzuk MM. 1996. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature, 383:531-535.

Dvořák M, Tesařík J. 1980. Ultrastructure of human ovarian follicles, Biology of the Ovary, Springer, pp.121-137.

El-Hayek S, Clarke HJ. 2015. Follicle-stimulating hormone increases gap junctional communication between somatic and germ-line follicular compartments during murine oogenesis. Biol Reprod, 93(2):47. Doi: 10.1095/biolreprod.115.129569.

El-Hayek S, Yang Q, Abbassi L, FitzHarris G, Clarke HJ. 2018. Mammalian oocytes locally remodel follicular architecture to provide the foundation for germline-soma communication. Curr Biol, 28(7):1124-1131.

Ellsworth L, Balmaceda J, Schenken RS, Silverman A, Prihoda T, Asch R. 1984. Human chorionic gonadotropin and steroid concentrations in human follicular fluid in relation to follicle size and oocyte maturity in stimulated ovarian cycles. Acta Eur Fertil, 15:343-346.

Enien W, Chantler E, Seif M, Elstein M. 1998. Human ovarian granulosa cells and follicular fluid indices: the relationship to oocyte maturity and fertilization in ivtro. Human Reprod, 13:1303-1306.

Eppig JJ. 2001. Oocyte control of ovarian follicular development and function in mammals. Reproduction, 122:829-838.

Eppig JJ. 2018. Reproduction: oocytes call, granulosa cells connect. Curr Biol, 28:R354-R356.

Eppig JJ, Pendola FL, Wigglesworth K, Pendola JK. 2005. Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: Amino acid transport. Biol Reprod, 73:351-357.

Eppig JJ, Wigglesworth K, Pendola F, Hirao Y, 1997. Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biol Reprod, 56:976-984.

Erickson B. 1966. Development and senescence of the postnatal bovine ovary. J Anim Sci, 25:800-805.

Erickson GF, Shimasaki S. 2001. The physiology of folliculogenesis: the role of novel growth factors. Fertil Steril, 76:943-949.

Fair T, Hulshof SCJ, Hyttel P, Greve T, Boland M. 1997. Oocyte ultrastructure in bovine primordial to early tertiary follicles. Anat Embryol, 195:327-336.

Fayezi S, Darabi M, Nouri M, Rahimipour A, Mehdizadeh A. 2014. Analysis of follicular fluid total phospholipids in women undergoing in-vitro fertilisation. J Obstet Gynaecol, 34:259-262. Florman HM, Ducibella T. 2006. Fertilization in mammals. Knobil and Neill’s physiology of Reproduction, 3:55-112.

Fortune JE. 1994. Ovarian follicular-growth and development in mammals. Biol Reprod, 50:225-232.

Freitas C, Neto AC, Matos L, Silva E, Ribeiro A, Silva-Carvalho JL, Almeida H. 2017. Follicular Fluid redox involvement for ovarian follicle growth. J Ovarian Res, 10(1):44. Doi: 10.1186/s13048-017-0342-3.

Gilchrist RB, Luciano AM, Richani D, Zeng HT, Wang X, De Vos M, Sugimura S, Smitz J, Richard FJ, Thompson JG. 2016. Oocyte maturation and quality: role of cyclic nucleotides. Reproduction, 152:R143-R157.

Gilchrist RB, Ritter LJ, Armstrong DT. 2004. Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci, 82-3:431-446.

Girard A, Dufort I, Douville G, Sirard MA. 2015. Global gene expression in granulosa cells of growing, plateau and atretic dominant follicles in cattle. Reprod Biol Endocrinol, 13:17. Doi: 10.1186/s12958-015-0010-7.

Guo J, Shi LY, Gong XH, Jiang MJ, Yin YX, Zhang XY, Yin H, Li H, Emori C, Sugiura K, Eppig JJ, Su YQ. 2016. Oocyte-dependent activation of MTOR in cumulus cells controls the development and survival of cumulus-oocyte complexes. J Cell Sci, 129:3091-3103.

Gupta SK. 2015. Role of zona pellucida glycoproteins during fertilization in humans. J Reprod Immunol, 108:90-97.

Gutierrez CG, Ralph JH, Telfer EE, Wilmut I, Webb R. 2000. Growth and antrum formation of bovine preantral follicles in long-term culture in ivtro. Biol Reprod, 62:1322-1328.

Hennet ML, Combelles CMH. 2012. The antral follicle: a microenvironment for oocyte differentiation. Int J Dev Biol, 56:819-831.

Hillier SG. 2009. Paracrine support of ovarian stimulation. Mol Hum Reprod, 15:843-850.

Hung W-T, Hong X, Christenson LK, McGinnis LK. 2015. Extracellular vesicles from bovine follicular fluid support cumulus expansion. Biol Reprod, 93(5):117. Doi: 10.1095/biolreprod.115.13297.

Hung W-T, Navakanitworakul R, Khan T, Zhang P, Davis JS, McGinnis LK, Christenson LK. 2017. Stage-specific follicular extracellular vesicle uptake and regulation of bovine granulosa cell proliferation. Biol Reprod, 97(4):644-655.

Hyttel P, Fair T, Callesen H, Greve T. 1997. Oocyte growth, capacitation and final maturation in cattle. Theriogenology, 47:23-32.

Jaffe LA, Egbert JR. 2017. Regulation of mammalian oocyte meiosis by intercellular communication within the ovarian follicle. Ann Rev Physiol, 79:237-260.

Keefe D, Tran P, Pellegrini C, Oldenbourg R. 1997. Polarized light microscopy and digital image processing identify a multilaminar structure of the hamster zona pellucida. Hum Reprod, 12:1250-1252.

Kerr JB, Myers M, Anderson RA. 2013. The dynamics of the primordial follicle reserve. Reproduction, 146:R205-R215.

Knight PG, Glister, C, 2006. TGF-beta superfamily members and ovarian follicle development. Reproduction, 132:191-206.

Leroy J, Vanholder T, Delanghe JR, Opsomer G, Van Soom A, Bols PEJ, de Kruif A. 2004. Metabolite and ionic composition of follicular fluid from different-sized follicles and their relationship to serum concentrations in dairy cows. Anim Reprod Sci, 80:201-211.

Li R, Albertini DF. 2013. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol, 14:141-152.

Lodde V, Franciosi F, Tessaro I, Modina SC, Luciano AM. 2013. Role of gap junction-mediated communications in regulating large-scale chromatin configuration remodeling and embryonic developmental competence acquisition in fully grown bovine oocyte. J Assist Reprod Genet, 30:1219-1226.

Macaulay AD, Gilbert I, Caballero J, Barreto R, Fournier E, Tossou P, Sirard MA, Clarke HJ, Khandjian EW, Richard FJ, Hyttel P, Robert C. 2014. The gametic synapse: rna transfer to the bovine oocyte. Biol Reprod, 91(4):90. doi: 10.1095/biolreprod.114.119867.

Macaulay AD, Gilbert I, Scantland S, Fournier E, Ashkar F, Bastien A, Saadi HAS, Gagne D, Sirard MA, Khandjian EW, Richard FJ, Hyttel P, Robert C. 2016. Cumulus cell transcripts transit to the bovine oocyte in preparation for maturation. Biol Reprod, 94(1):16. Doi: 10.1095/biolreprod.114.127571.

Machtinger R, Rodosthenous RS, Adir M, Mansour A, Racowsky C, Baccarelli AA, Hauser R. 2017. Extracellular microRNAs in follicular fluid and their potential association with oocyte fertilization and embryo quality: an exploratory study. J Assist Reprod Genet, 34:525-533.

Martinez RM, Liang LM, Racowsky C, Dioni L, Mansur A, Adir M, Bollati V, Baccarelli AA, Hauser R, Machtinger R. 2018. Extracellular microRNAs profile in human follicular fluid and IVF outcomes.Sci Rep, 8(1):17036. Doi: 10.1038/s41598-018-35379-3.

Mathivanan S, Ji H, Simpson RJ. 2010. Exosomes: Extracellular organelles important in intercellular communication. J Proteomics,73:1907-1920.

Matzuk MM, Burns KH, Viveiros MM, Eppig JJ2002. Intercellular communication in the mammalian ovary: Oocytes carry the conversation. Science, 296:2178-2180.

McLaughlin M, Bromfield JJ, Albertini DF, Telfer EE. 2010. Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles. Mol Hum Reprod, 16:644-653.

Meeker JD, Missmer SA, Altshul L, Vitonis AF, Ryan L, Cramer DW, Hauser R. 2009. Serum and follicular fluid organochlorine concentrations among women undergoing assisted reproduction technologies. Environ Health, 8:32. Doi: 10.1186/1476-069X-8-32.

Mendoza C, Ruiz-Requena E, Ortega E, Cremades N, Martinez F, Bernabeu R, Greco E, Tesarik J. 2002. Follicular fluid markers of oocyte developmental potential. Hum Reprod, 17:1017-1022.

Mihm A, Bleach ECL. 2003. Endocrine regulation of ovarian antral follicle development in cattle. Anim Reprod Sci, 78:217-237.

Mobarak H, Heidarpour M, Lolicato F, Nouri M, Rahbarghazi R, Mahdipour M. 2019. Physiological impact of extracellular vesicles on female reproductive system; highlights to possible restorative effects on female age-related fertility. Biofactors, 45(3):293-303.

Modliński JA. 1970. The role of the zona pellucida in the development of mouse eggs in vivo. J Embryol Exp Morphol, 23:539-547.

Monniaux D. 2016. Driving folliculogenesis by the oocyte-somatic cell dialog: Lessons from genetic models. Theriogenology, 86:41-53.

Motta PM, Makabe S, Nottola SA. 1997. The ultrastructure of human reproduction .1. The natural history of the female germ cell: origin, migration and differentiation inside the developing ovary. Hum Reprod Update, 3:281-295.

Navakanitworakul R, Hung WT, Gunewardena S, Davis JS, Chotigeat W, Christenson LK. 2016. characterization and small RNA content of extracellular vesicles in follicular fluid of developing bovine antral follicles. Sci Rep, 6:25486. Doi: 10.1038/srep25486.

O'Gorman A, Wallace M, Cottell E, Gibney MJ, McAuliffe FM, Wingfield M, Brennan L. 2013. Metabolic profiling of human follicular fluid identifies potential biomarkers of oocyte developmental competence. Reproduction, 146:389-395.

Paulini F, Silva RC, Rolo J, Lucci CM. 2014. Ultrastructural changes in oocytes during folliculogenesis in domestic mammals. J Ovarian Res, 7:102. Doi: 10.1186/s13048-014-0102-6.

Pepling ME. 2012. Follicular assembly: mechanisms of action. Reproduction, 143:139-149.

Revelli A, Delle Piane L, Casano S, Molinari E, Massobrio M, Rinaudo P. 2009. Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics. Reprod Biol Endocrinol, 7:40. Doi: 10.1186/1477-7827-7-40.

Rodgers RJ, Irving-Rodgers HF. 2010. Formation of the ovarian follicular antrum and follicular fluid. Biol Reprod, 82:1021-1029.

Rodrigues TA, Tuna KM, Alli AA, Tribulo P, Hansen P, Koh J, Paula-Lopes F. 2019. Follicular fluid exosomes act on the bovine oocyte to improve oocyte competence to support development and survival to heat shock. Reprod Fertil Dev, 31(5):888-897. Doi: 10.1071/RD18450.

Rodriguez KF, Farin CE. 2004. Developmental capacity of bovine cumulus oocyte complexes after transcriptional inhibition of germinal vesicle breakdown. Theriogenology, 61:1499-1511.

Russe I. 1983. Oogenesis in cattle and sheep. Bibl Anat, 24:77-92.

Sanfins A, Rodrigues P, Albertini DF. 2018. GDF-9 and BMP-15 direct the follicle symphony. J Assist Reprod Genet, 35:1741-1750.

Sang Q, Yao ZY, Wang H, Feng RZ, Wang HJ, Zhao XZ, Xing QH, Jin L, He L, Wu LQ, Wang L. 2013. Identification of microRNAs in human follicular fluid: characterization of microRNAs that govern steroidogenesis in ivtro and are associated with polycystic ovary syndrome in vivo. J Clin Endocrinol Metab, 98:3068-3079.

Santonocito M, Vento M, Guglielmino MR, Battaglia R, Wahlgren J, Ragusa M, Barbagallo D, Borzi P, Rizzari S, Maugeri M, Scollo P, Tatone C, Valadi H, Purrello M, Di Pietro C. 2014. Molecular characterization of exosomes and their microRNA cargo in human follicular fluid: bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation. Fertil Steril, 102:1751-U1590.

Scantland S, Tessaro I, Macabelli CH, Macaulay AD, Cagnone G, Fournier E, Luciano AM, Robert C. 2014. The adenosine salvage pathway as an alternative to mitochondrial production of ATP in maturing mammalian oocytes. Biol Reprod, 91(3):75. Doi: 10.1095/biolreprod.114.120931.

Shaaker M, Rahimipour A, Nouri M, Khanaki K, Darabi M, Farzadi L, Shahnazi V, Mehdizadeh A. 2012. Fatty acid composition of human follicular fluid phospholipids and fertilization rate in assisted reproductive techniques. Iran Biomed J, 16:162-168.

Smith MF, McIntush EW, Smith GW, 1994. Mechanisms Associated With Corpus-Luteum Development. J Anim Sci, 72:1857-1872.

Sohel MMH, Hoelker M, Noferesti SS, Salilew-Wondim D, Tholen E, Looft C, Rings F, Uddin MJ, Spencer TE, Schellander K, Tesfaye D. 2013. Exosomal and non-exosomal transport of extra-cellular micrornas in follicular fluid: implications for bovine oocyte developmental competence. Plos One, 8(11):e78505. Doi: 10.1371/journal.pone.0078505.

Soto-Heras S, Paramio M-T, Thompson JG. 2019. Effect of pre-maturation with C-type natriuretic peptide and 3-isobutyl-1-methylxanthine on cumulus-oocyte communication and oocyte developmental competence in cattle. Anim Reprod Sci, 202:49-57.

Suchanek E, Simunic V, Macas E, Kopjar B, Grizelj V. 1988. Prostaglandin F2α, progesterone and estradiol concentrations in human follicular fluid and their relation to success of in ivtro fertilization. Eur J Obstet Gynecol Reprod Biol, 28:331-339.

Sun YC, Sun XF, Dyce PW, Shen W, Chen H. 2017. The role of germ cell loss during primordial follicle assembly: a review of current advances. Int J Biol Sci, 13:449-457.

Taylor DD, Gercel-Taylor C. 2013. The origin, function, and diagnostic potential of RNA within extracellular vesicles present in human biological fluids. Front Genet, 4:142. Doi: 10.3389/fgene.2013.00142.

Thomas RE, Armstrong DT, Gilchrist RB. 2004. Bovine cumulus cell-oocyte gap junctional communication during in ivtro maturation in response to manipulation of cell-specific cyclic adenosine 3 ',5 '-monophosophate levels. Biol Reprod, 70:548-556.

Tilly JL. 2001. Commuting the death sentence: How oocytes strive to survive. Nat Rev Mol Cell Biol, 2:838-848.

van Niel G, D'Angelo G, Raposo G. 2018. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol, 19:213-228.

vandenHurk R, Bevers MM, Beckers JF. 1997. In-vivo and in-vitro development of preantral follicles. Theriogenology, 47:73-82.

Wallace M, Cottell E, Gibney MJ, McAuliffe FM, Wingfield M, Brennan L. 2012. An investigation into the relationship between the metabolic profile of follicular fluid, oocyte developmental potential, and implantation outcome. Fertil Steril, 97(5):1078-1084.e1-8. Doi: 10.1016/j.fertnstert.2012.01.122.

Wang C, Roy SK. 2007. Development of primordial follicles in the hamster: Role of estradiol-17 beta. Endocrinology, 148:1707-1716.

Wang Y, Lv C, Huang H-L, Zeng M-H, Yi D-J, Tan H-J, Peng T-L, Yu W-X, Deng H-W, Xiao H-M. 2019. Influence of mouse defective zona pellucida in folliculogenesis on apoptosis of granulosa cells and developmental competence of oocytes. Biol Reprod. Doi: 10.1093/biolre/ioz093.

Wang YY, Sun YC, Sun XF, Cheng SF, Li B, Zhang XF, De Felici M, Shen W. 2017. Starvation at birth impairs germ cell cyst breakdown and increases autophagy and apoptosis in mouse oocytes. Cell Death Dis, 8(2):e2613. Doi: 10.1038/cddis.2017.3.

Wassarman PM. 1999. Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell, 96:175-183.

Wassarman PM, Litscher ES. 2012. Influence of the zona pellucida of the mouse egg on folliculogenesis and fertility. Int J Dev Biol, 56(10-12):833-9. Doi: 10.1387/ijdb.120136pw.

Wassarman PM, Litscher ES. 2013. Biogenesis of the Mouse Egg's Extracellular Coat, the Zona Pellucida. Gametogenesis, 102:243-266.

Wigglesworth K, Lee KB, Emori C, Sugiura K, Eppig JJ. 2015. Transcriptomic diversification of developing cumulus and mural granulosa cells in mouse ovarian follicles. Biol Reprod, 92(1):23. Doi: 10.1095/biolreprod.114.121756.

Yang XK, Zhou Y, Peng S, Wu L, Lin HY, Wang SY, Wang HM. 2012. Differentially expressed plasma microRNAs in premature ovarian failure patients and the potential regulatory function of mir-23a in granulosa cell apoptosis. Reproduction, 144:235-244.

Zuckerman S. 1951. The number of oocytes in the mature ovary. Recent Prog Horm Res, 6:63-109.

5d52ba940e8825d24cdaee82 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections