Control of growth and development of preantral follicle: insights from in vitro culture
José Ricardo de Figueiredo, Laritza Ferreira de Lima, José Roberto Viana Silva, Regiane Rodrigues Santos
Abstract
The regulation of folliculogenesis involves a complex interaction among endocrine, paracrine and autocrine factors. The mechanisms involved in the initiation of the growth of the primordial follicle, i.e., follicular activation and the further growth of primary follicles up to the pre-ovulatory stage, are not well understood at this time. The present review focuses on the regulation and development of early stage (primordial, primary, and secondary) folliculogenesis highlighting the mechanisms of primordial follicle activation, growth of primary and secondary follicles and finally transition from secondary to tertiary follicles. We also discuss the importance of in vitro follicle culture for the understanding of folliculogenesis during the preantral phase. Studies suggest that follicular development from primordial to early antral stages is primarily controlled by intra-ovarian ligands but it can also be influenced by many extra-ovarian factors. The control of early folliculogenesis is, therefore, extremely complex because several ligands act through distinct signaling pathways that form sophisticated information networks responding to multiple, often opposing, stimuli. The balance among different stimuli determines follicular survival or death as well as quiescence or activation (growth). The distribution of the ligands and their corresponding receptors varies among follicular compartments and species, and significant changes in gene expression pattern among follicular categories have been reported. Knowing that follicular requirements during early folliculogenesis can be stage-specific and species-specific, in vitro culture studies offer an alternative to evaluate single and combined factors during a specific period of follicular development. Herewith we summarize the main findings obtained in vitro together with the mechanisms regulating folliculogenesis.
Keywords
References
Ackert CL, Gittens JE, O’Brien MJ, Eppig JJ, Kidder GM. 2001. Intercellular communication via connexin43 gap junctions is required for ovarian folliculogenesis in the mouse. Dev Biol, 233:258-270.
Adhikari D, Flohr G, Gorre N, Shen Y, Yang H, Lundin E, Lan Z, Gambello MJ, Liu K. 2009. Disruption of Tsc2 in oocytes leads to overactivation of the entire pool of primordial follicles. Mol Hum Reprod, 15:765-770.
Adhikari D, Zheng W, Shen Y, Gorre N, Hämäläinen T, Cooney AJ, Huhtaniemi I, Lan ZJ, Liu K. 2010. Tsc/mTORC1 signaling in oocytes governs the quiescence and activation of primordial follicles. Hum Mol Genet, 19:397-410.
Araujo VR, Gastal MO, Wischral A, Figueiredo JR, Gastal EL. 2014. In vitro development of bovine secondary follicles in two- and three-dimensional culture systems using vascular endothelial growth factor, insulin-like growth factor-1, and growth hormone. Theriogenology, 82:1246-1253.
Asadi-Azarbaijani B, Santos RR, Jahnukainen K, Braber S, van Duursen MBM, Toppari J, Saugstad OD, Nurmio M, Oskam IC. 2017. Developmental effects of imatinib mesylate on follicle assembly and early activation of primordial follicle pool in postnatal rat ovary. Reprod Biol, 17:25-33.
Atwood CS, Meethala SV. 2016. The spatiotemporal hormonal orchestration of human folliculogenesis, early embryogenesis and blastocyst implantation. Mol Cell Endocrinol, 430:33-48.
Bonnet A, Servin B, Mulsant P, Mandon-Pepin B. 2015. Spatio-temporal gene expression profiling during in vivo early ovarian folliculogenesis: integrated transcriptomic study and molecular signature of early follicular growth. PLoS One, 10:e0141482. doi: 10.1371/journal.pone.0141482.
Brito IR, Lima IM, Xu M, Shea LD, Woodruff TK, Figueiredo JR. 2014a. Three-dimensional systems for in vitro follicular culture: overview of alginate-based matrices. Reprod Fertil Dev, 26:915-930.
Brito IR, Silva CM, Duarte AB, Lima IM, Rodrigues GQ, Rossetto R, Sales AD, Lobo CH, Bernuci MP, Rosa-E-Silva AC, Campello CC, Xu M, Figueiredo JR. 2014b. Alginate hydrogel matrix stiffness influences the in vitro development of caprine preantral follicles. Mol Reprod Dev, 81:636-645.
Bromfield JJ, Sheldon IM. 2013. Lipopolysaccharide reduces the primordial follicle pool in the bovine ovarian cortex ex vivo and in the murine ovary in vivo. Biol Reprod, 88:98. doi: 10.1095/biolreprod.112.106914.
Cadenas J, Leiva-Revilla J, Vieira LA, Apolloni LB, Aguiar FLN, Alves BG, Lobo CH, Rodrigues APR, Apgar GA, Smitz J, Figueiredo JR, Maside C. 2017. Caprine ovarian follicle requirements differ between preantral and early antral stages after IVC in medium supplemented with GH and VEGF alone or in combination. Theriogenology, 87:321-332.
Campbell L, Trendell J, Spears N. 2013. Identification of cells migrating from the thecal layer of ovarian follicles. Cell Tissue Res, 353:189-194.
Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA. 2003. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science, 301(5630):215-218.
Celestino JJH, Lima-Verde IB, Bruno JB, Matos MHT, Chaves RN, Saraiva MVA, Silva CMG, Faustino LR, Rossetto R, Lopes CAP, Donato MAM, Peixoto CA, Campello CC, Silva JRV, Figueiredo JR. 2011. Steady-state level of bone morphogenetic protein-15 in goat ovaries and its influence on in vitro development and survival of preantral follicles. Mol Cell Endocrinol, 338:1-9.
Christensen AP, Peyrache E, Kaune H, Williams SA. 2017. Formation of multiple-oocyte follicles in culture. In vitro Cell Dev Biol Anim, 53:791-797.
Clarke HG, Hope SA, Byers S, Rodgers RJ. 2006. Formation of ovarian follicular fluid may be due to the osmotic potential of large glycosaminoglycans and proteoglycans. Reproduction, 132:119-131.
Dharma SJ, Modi DN, Nandedkar TD. 2009. Gene expression profiling during early folliculogenesis in the mouse ovary. Fertil Steril, 91:2025-2036.
Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. 1996. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature, 383:531-535.
Duarte AB, Chaves RN, Araújo VR, Celestino JJ, Silva GM, Lopes CA, Tavares LM, Campelo CC, Figueiredo JR. 2010. Follicular interactions affect the in vitro development of isolated goat preantral follicles. Zygote, 19:215-227.
Duarte AB, Araújo VR, Chaves RN, Silva GM, Magalhães-Padilha DM, Satrapa RA, Donato MA, Peixoto CA, Campello CC, Matos MH, Barros CM, Figueiredo JR. 2012. Bovine dominant follicular fluid promotes the in vitro development of goat preantral follicles. Reprod Fertil Dev, 24:490-500.
Erickson GF. 1983. Primary cultures of ovarian cells in serum-free medium as models of hormone-dependent differentiation. Mol Cell Endocrinol, 29:21-49.
Eriksen GV, Carlstedt I, Morgelin M, Uldbjerg N, Malmstrom A. 1999. Isolation and characterization of proteoglycans from human follicular fluid. Biochem J, 340:613-620.
Ernst EH, Grøndahl ML, Grund S, Hardy K, Heuck A, Sunde L, Franks S, Andersen CY, Villesen P, Lykke-Hartmann K. 2017. Dormancy and activation of human oocytes from primordial and primary follicles: molecular clues to oocyte regulation. Hum Reprod, 32:1684-1700.
Familiari G, Nottola SA, Motta PM. 1987. Focal cell contacts detected by rutheniumred, TritonX100 and saponin in the granulosa cells of mouse ovary. Tissue Cell, 19:207-215.
Figueiredo JR, Celestino JJH, Faustino LR, Rodrigues APR. 2011. In vitro culture of caprine preantral follicles: advances, limitations and prospects. Small Rumin Res, 98:92-195.
Galloway SM, McNatty KP, Cambridge LM, Laitinen MPE, Juengel JL, Jokiranta TS, McLaren RJ, Luiro K, Dodds KG, Montgomery GW, Beattie AE, Davis GH, Ritvos O. 2000. Mutations in an oocyte-derived growth factor gene (bmp15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet, 25:279-283
Gosden RG, Byattsmith JG. 1986. Oxygen concentration gradient across the ovarian follicular epithelium - model, predictions and implications. Hum Reprod, 1:65-68.
Gupta PSP, Nandi S, Ravindranatha BM, Sarma PV. 2002. In vitro culture of buffalo (Bubalus bubalis) preantral follicles. Theriogenology, 57:1839-1854.
Gutierrez CG, Ralph JH, Telfer EE, Wilmut I, Webb R. 2000. Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol Reprod, 62:1322-1328.
Hornick JE, Duncan FE, Shea LD, Woodruff TK. 2012. Isolated primate primordial follicles require a rigid physical environment to survive and grow in vitro. Hum Reprod, 27:1801-1810.
Hsueh AJ, Kawamura K, Cheng Y, Fauser BC. 2015. Intraovarian control of early folliculogenesis. Endocr Rev, 36:1-24.
Hu Y, Yuan DZ, Wu Y, Yu LL, Xu LZ, Yue LM, Liu L, Xu WM, Qiao XY, Zeng RJ, Yang ZL, Yin WY, Ma YX, Nie Y. 2017. Bisphenol A initiates excessive premature activation of primordial follicles in mouse ovaries via the PTEN signaling pathway. Reprod Sci, 25:609-620.
Hunter T. 2000. Cell, signaling-2000 and beyond. Cell Press, 100:113-127.
Ikeda Y, Hasegawa A, Tsubamoto H, Wakimoto Y, Kumamoto K, Shibahara H. 2016. Effects of gremlin-2 on the transition of primordial follicles during early folliculogenesis in the human ovary. Eur J Obstet Gynecol Reprod Biol, 203:72-77.
Irving-Rodgers HF, Harland ML, Rodgers RJ. 2004. A novel basal lamina matrix of the stratified epithelium of the ovarian follicle. Matrix Biol, 23:207-217.
Jiang C, Diao F, Sang YJ, Xu N, Zhu RL, Wang XX, Chen Z, Tao WW, Yao B, Sun HX, Huang XX, Xue B, Li CJ. 2017. GGPP-mediated protein geranylgeranylation in oocyte is essential for the establishment of oocyte-granulosa cell communication and primary-secondary follicle transition in mouse ovary. PLoS Genet, 13:e1006535. doi: 10.1371/journal.pgen.1006535.
Jimenez CR, Araújo VR, Penitente-Filho JM, Azevedo JL, Silveira RG, Torres CAA. 2016. The base medium affects ultrastructure and survival of bovine preantral follicles cultured in vitro. Theriogenology, 85:1019-1029.
John GB, Gallardo TD, Shirley LJ, Castrillon DH. 2008. Foxo3 is a PI3K dependent molecular switch controlling the initiation of oocyte growth. Dev Biol, 32:197-204.
Juengel JL, Hudson NL, Heath DA, Smith P, Reader KL, Lawrence SB, O’Connel, Laitinen MP, Cranfield M, Groome NP, Ritvos O, McNatty KP. 2002. Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol Reprod, 67:1777-1789.
Kawamura A, Cheng Y, Suzuki N, Deguchi M, Sato Y, Takae S, Chi-hong Ho, Kawamura N, Tamura M, Hashimoto S, Sugishita Y, Morimoto Y, Hosoi Y, Yoshioka N, Ishizuka B, Hsueh AJ. 2013. Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc Natl Acad Sci USA, 110:17474-17479.
Kumar TR, Low MJ, Matzuk MM. 1998. Genetic rescue of follicle-stimulating hormone beta-deficient mice. Endocrinology, 139:3289-3295.
Li R, Phillips DM, Mather JP. 1995. Activin promotes ovarian follicle development in vitro. Endocrinology, 136:849-856.
Liu L, Rajareddy S, Reddy P, Jagarlamudi K, Du C, Shen Y, Guo Y, Boman K, Lundin E, Ottander U, Selstam G, Liu K. 2007. Phosphorylation and inactivation of glycogen synthase kinase-3 by soluble kit ligand in mouse oocytes during early follicular development. J Mol Endocrinol, 38:137-146.
Liu X, Qiao P, Jiang A, Jiang J, Han H, Wang L, Ren C. 2015. Paracrine regulation of steroidogenesis in theca cells by granulosa cells derived from mouse preantral follicles. Biomed Res Int, 2015:925691. doi.org/10.1155/2015/925691
Maehama T, Dixon JE. 1998. The tumor suppressor, PTEN/ MMAC1, dephosphorylates the lipid second messenger, phospha- tidylinositol 3, 4, 5-trisphosphate. J Biol Chem, 273:13375-13378.
Magalhães-Padilha DM, Geisler-Lee J, Wischral A, Gastal MO, Fonseca GR, Eloy YR, Geisler M, Figueiredo JR, Gastal EL. 2013. Gene expression
during early folliculogenesis in goats using microarray analysis. Biol Reprod, 89:19. doi: 10.1095/biolreprod. 112.106096.
McArthur ME, Irving-Rodgers HF, Byers S, Rodgers RJ. 2000. Identification and immunolocalization of decorin, versican, perlecan, nidogen, and chondroitin sulfate proteoglycans in bovine small-antral ovarian follicles. Biol Reprod, 63:913-924.
McLaughlin EA; McIver SC. 2009. Awakening the oocyte: controlling primordial follicle development. Reproduction, 137:1-11.
McMahon HE, Hashimoto O, Mellon PL, Shimasaki S. 2008. Oocyte-specific overexpression of mouse bone morphogenetic protein-15 leads to accelerated folliculogenesis and an early onset of acyclicity in transgenic mice. Endocrinology, 149:2807-2815.
McNatty KP, Galloway SM, Wilson T, Smith P, Hudson NL, O'Connell A, Bibby AH, Heath DA, Davis GH, Hanrahan JP, Juengel JL. 2005. Physiological effects of major genes affecting ovulation rate in sheep. Genet Sel Evol, 37:S25-38.
Mora JM, Fenwick MA, Castle L, Baithun M, Ryder TA, Mobberley M, Carzaniga R, Franks S, Hardy K. 2012. Characterization and significance of adhesion and junction-related proteins in mouse ovarian follicles. Biol Reprod, 86:153. doi: 10.1095/biolreprod.111.096156.
Novella-Maestre E, Herraiz S, Rodríguez-Iglesias B, Díaz-García C, Pellicer A. 2015. Short-term PTEN inhibition improves in vitro activation of primordial follicles, preserves follicular viability, and restores AMH levels in cryopreserved ovarian tissue from cancer patients. PLoS One, 10:e0127786. doi: 10.1371/ journal.pone.0127786.
Paes VM, Vieira LA, Correia HHV, Sa NAR, Moura AAA, Sales AD, Rodrigues APR, Magalhães-Padilha DM, Santos FW, Apgar GA, Campello CC, Camargo LSA, Figueiredo JR. 2016. Effect of heat stress on the survival and development of in vitro cultured bovine preantral follicles and on in vitro maturation of cumulus-oocyte complex. Theriogenology, 86:994-1003.
Parrott JA, Skinner MK. 2000. Kit ligand actions on ovarian stromal cells: effects on theca cell recruitment and steroid production. Mol Reprod Dev, 55:55-64.
Pires ES, Hlavin C, Macnamara E, Ishola-Gbenla K, Doerwaldt C, Chamberlain C, Klotz K, Herr AK, Khole A, Chertihin O, Curnow E, Feldman SH, Mandal A, Shetty J, Flickinger C, Herr JC. 2013. SAS1B protein [ovastacin] shows temporal and spatial restriction to oocytes in several eutherian orders and initiates translation at the primary to secondary follicle transition. Dev Dyn, 242:1405-1426.
Princivalle M, Hasan S, Hosseini G, Agostini AI. 2001. Anticoagulant heparan sulfate proteoglycans expression in the rat ovary peaks in preovulatory granulosa cells. Glycobiology, 11:183-194.
Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hämäläinen T, Peng SL, Lan ZJ, Cooney AJ, Huhtaniemi I, Liu K. 2008. Oocyte-specific deletion of PTEN causes premature activation of the primordial follicle pool. Science, 319:611-613.
Richards JS, Pangas SA. 2010. The ovary: basic biology and clinical implications. J Clin Invest, 120:963-972.
Rodgers RJ, Irving-Rodgers HF. 2010. Formation of the ovarian follicular antrum and follicular fluid. Biol Reprod, 82:1021-1029.
Roness H, Kalich-Philosoph L, Meirow D. 2014. Prevention of chemotherapy-induced ovarian damage: possible roles for hormonal and non-hormonal attenuating agents. Hum Reprod Update, 20:759-774.
Santos RR, Schoevers EJ, Wu X, Roelen BAJ, Fink-Gremmels J. 2015. The protective effect of follicular fluid against the emerging mycotoxins alternariol and beauvericin. World Mycotoxin J, 8:445-450.
Silva JRV, van den Hurk R, Matos MHT, Santos RR, Pessoa C, Moraes MO, Figueiredo JR. 2004. Influences of FSH and EGF on primordial follicles during in vitro culture of caprine ovarian cortical tissue. Theriogenology, 61:1691-1704.
Silva JRV, van den Hurk R, Figueiredo JR. 2016. Ovarian follicle development in vitro and oocyte competence: advances and challenges for farm animals. Domest Anim Endocrinol, 55:123-135.
Simon AM, Goodenough DA, Li E, Paul DL. 1997. Female infertility in mice lacking connexin 37. Nature, 385(6616):525-529.
Spears N, De Bruin JP, Gosden RG. 1996. The establishment of follicular dominance in co-cultured mouse ovarian follicles. J Reprod Fertil, 106:1-6.
Sun X, Su Y, He Y, Zhang J, Liu W, Zhang H, Hou Z, Liu J, Li J. 2005. New strategy for in vitro activation of primordial follicles with mTOR and PI3K stimulators. Cell Cycle, 14:721-731.
Tran H, Brunet A, Griffith EC, Greenberg ME. 2003. The many forks in FOXO's Road. Sci STKE, (172):RE5. doi: 10.1126/stke.2003.172.re5.
Vasconcelos GL, Saraiva MV, Costa JJ, Passos MJ, Silva AW, Rossi RO, Portela AM, Duarte AB, Magalhães-Padilha DM, Campelo CC, Figueiredo JR, van den Hurk R, Silva JR. 2013. Effects of growth differentiation factor-9 and FSH on in vitro development, viability and mRNA expression in bovine preantral follicles. Reprod Fertil Dev, 25:1194-1203.
Wang C, Roy SK. 2010. Expression of E-cadherin and N-cadherin in perinatal hamster ovary: possible involvement in primordial follicle formation and regulation by follicle-stimulating hormone. Endocrinology, 151:2319-2330.
Wu J, Emery BR, Carrell DT. 2001. In vitro growth, maturation, fertilization, and embryonic development of oocytes from porcine preantral follicles. Biol Reprod, 64:375-381.
Yoshida H, Takakura N, Kataoka H, Kunisada T, Okamura H, Nishikawa SI. 1997. Stepwise requirement of c-kit tyrosine kinase in mouse ovarian follicle development. Dev Biol, 184:122-137.
Young JM, McNeilly AS. 2010. Theca: the forgotten cell of the ovarian follicle. Reproduction, 140:489-504.
Zhao Y, Zhang Y, Li J, Zheng N, Xu X, Yang J, Xia G, Zhang M. 2018. MAPK3/1 participates in the activation of primordial follicles through mTORC1-KITL signaling. J Cell Physiol, 233:226-237.
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