Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2018-0035
Animal Reproduction (AR)
Conference Paper

Follicular guidance for oocyte developmental competence

Satoshi Sugimura, Dulama Richani, Robert B. Gilchrist

Downloads: 4
Views: 1626

Abstract

The advancement of folliculogenesis is coincident with the sequential acquisition of oocyte developmental competence. In practical bovine/porcine ART, cumulus-oocyte complexes (COCs) aspirated from small antral follicles have low developmental competence relative to COCs from medium/large antral follicles, as evidenced by a poor capacity to support embryogenesis up to the blastocyst stage. This is in part because of incomplete differentiation of cumulus cells in small antral follicles, in particular under-developed functionality of EGF signalling. Gonadotrophins and oocyte-secreted paracrine factors cooperate to establish EGF receptor functionality in cumulus cells, which appears to be involved in the acquisition of oocyte developmental competence. Here we review the modification of follicular cumulus cells during antral folliculogenesis involved in oocyte developmental competence.

Keywords

cumulus cells, oocyte, oocyte secreted factors.

References

Caixeta ES, Ripamonte P, Franco MM, Junior JB, Dode MA. 2009. Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: an approach to identify marker genes for developmental competence. Reprod Fertil Dev, 21:655-664.

Chen J, Torcia S, Xie F, Lin CJ, Cakmak H, Franciosi F, Horner K, Onodera C, Song JS, Cedars MI, Ramalho-Santos M, Conti M. 2013. Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes. Nat Cell Biol, 15:1415-1423.

Cohen M, Matcovitch O, David E, Barnett-Itzhaki Z, Keren-Shaul H, Blecher-Gonen R, Jaitin DA, Sica A, Amit I, Schwartz M. 2014. Chronic exposure to TGFbeta1 regulates myeloid cell inflammatory response in an IRF7-dependent manner. EMBO J, 33:2906-2921.

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.

Diaz FJ, O'Brien MJ, Wigglesworth K, Eppig JJ. 2006. The preantral granulosa cell to cumulus cell transition in the mouse ovary: development of competence to undergo expansion. Dev Biol, 299:91-104.

Diaz FJ, Wigglesworth K, Eppig JJ. 2007. Oocytes are required for the preantral granulosa cell to cumulus cell transition in mice. Dev Biol, 305:300-311.

El-Hayek S, Demeestere I, Clarke HJ. 2014. Follicle-stimulating hormone regulates expression and activity of epidermal growth factor receptor in the murine ovarian follicle. Proc Natl Acad Sci USA, 111:16778-16783.

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, 93:47. doi: 10.1095/biolreprod.115.129569.

Eppig JJ, Schroeder AC, O'Brien MJ. 1992. Developmental capacity of mouse oocytes matured in vitro: effects of gonadotrophic stimulation, follicular origin and oocyte size. J Reprod Fertil, 95:119-127.

Erickson GF, Wang C, Hsueh AJ. 1979. FSH induction of functional LH receptors in granulosa cells cultured in a chemically defined medium. Nature, 279:336-338.

Garnett K, Wang J, Roy SK. 2002. Spatiotemporal expression of epidermal growth factor receptor messenger RNA and protein in the hamster ovary: follicle stage-specific differential modulation by follicle-stimulating hormone, luteinizing hormone, estradiol, and progesterone. Biol Reprod, 67:1593-1604.

Gebhardt KM, Feil DK, Dunning KR, Lane M, Russell DL. 2011. Human cumulus cell gene expression as a biomarker of pregnancy outcome after single embryo transfer. Fertil Steril, 96:47-52, e42.

Gilchrist RB, Thompson JG. 2007. Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology, 67:6-15.

Gilchrist RB. 2011. Recent insights into oocyte-follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reprod Fertil Dev, 23:23-31.

Gilchrist RB, Richani D. 2013. Somatic guidance for the oocyte. Dev Cell, 27:603-605.

Hatzirodos N, Hummitzsch K, Irving-Rodgers HF, Harland ML, Morris SE, Rodgers RJ. 2014a. Transcriptome profiling of granulosa cells from bovine ovarian follicles during atresia. BMC Genomics, 15:40. doi: 10.1186/1471-2164-15-40.

Hatzirodos N, Irving-Rodgers HF, Hummitzsch K, Harland ML, Morris SE, Rodgers RJ. 2014b. Transcriptome profiling of granulosa cells of bovine ovarian follicles during growth from small to large antral sizes. BMC Genomics, 15:24. doi: 10.1186/1471-2164-15-24.

Hendriksen PJ, Vos PL, Steenweg WN, Bevers MM, Dieleman SJ. 2000. Bovine follicular development and its effect on the in vitro competence of oocytes. Theriogenology, 53:11-20.

Honda K, Yanai H, Negishi H, Asagiri M, Sato M, Mizutani T, Shimada N, Ohba Y, Takaoka A, Yoshida N, Taniguchi T. 2005. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature, 434:772-777.

Hsieh M, Lee D, Panigone S, Horner K, Chen R, Theologis A, Lee DC, Threadgill DW, Conti M. 2007. Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol Cell Biol, 27:1914-1924.

Ilha GF, Rovani MT, Gasperin BG, Antoniazzi AQ, Goncalves PB, Bordignon V, Duggavathi R. 2015. Lack of FSH support enhances LIF-STAT3 signaling in granulosa cells of atretic follicles in cattle. Reproduction, 150:395-403.

Irving-Rodgers HF, Harland ML, Sullivan TR, Rodgers RJ. 2009. Studies of granulosa cell maturation in dominant and subordinate bovine follicles: novel extracellular matrix focimatrix is co-ordinately regulated with cholesterol side-chain cleavage CYP11A1. Reproduction, 137:825-834.

Li HJ, Sutton-McDowall ML, Wang X, Sugimura S, Thompson JG, Gilchrist RB. 2016. Extending prematuration with cAMP modulators enhances the cumulus contribution to oocyte antioxidant defence and oocyte quality via gap junctions. Hum Reprod, 31:810-821.

Lonergan P, Monaghan P, Rizos D, Boland MP, Gordon I. 1994. Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol Reprod Dev, 37:48-53.

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

 

Mottershead DG, Sugimura S, Al-Musawi SL, Li JJ, Richani D, White MA, Martin GA, Trotta AP, Ritter LJ, Shi J, Mueller TD, Harrison CA, Gilchrist RB. 2015. Cumulin, an oocyte-secreted heterodimer of the transforming growth factor-beta family, is a potent activator of granulosa cells and improves oocyte quality. J Biol Chem, 290:24007-24020.

Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M. 2004. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science, 303:682-684.

Prochazka R, Srsen V, Nagyova E, Miyano T, Flechon JE. 2000. Developmental regulation of effect of epidermal growth factor on porcine oocyte-cumulus cell complexes: nuclear maturation, expansion, and F-actin remodeling. Mol Reprod Dev, 56:63-73.

Prochazka R, Kalab P, Nagyova E. 2003. Epidermal growth factor-receptor tyrosine kinase activity regulates expansion of porcine oocyte-cumulus cell complexes in vitro. Biol Reprod, 68:797-803

Prochazka R, Blaha M, Nemcova L. 2012. Signaling pathways regulating FSH- and amphiregulin-induced meiotic resumption and cumulus cell expansion in the pig. Reproduction, 144:535-546.

Richani D, Gilchrist RB. 2018. The epidermal growth factor network: role in oocyte growth, maturation and developmental competence. Hum Reprod Update, 24:1-14.

Ritter LJ, Sugimura S, Gilchrist RB. 2015. Oocyte induction of EGF responsiveness in somatic cells is associated with the acquisition of porcine oocyte developmental competence. Endocrinology, 156:2299-2312.

Roy SK. 1993. Epidermal growth factor and transforming growth factor-beta modulation of follicle-stimulating hormone-induced deoxyribonucleic acid synthesis in hamster preantral and early antral follicles. Biol Reprod, 48:552-557.

Russell DL, Gilchrist RB, Brown HM, Thompson JG. 2016. Bidirectional communication between cumulus cells and the oocyte: old hands and new players? Theriogenology, 86:62-68.

Sasseville M, Ritter LJ, Nguyen TM, Liu F, Mottershead DG, Russell DL, Gilchrist RB. 2010. Growth differentiation factor 9 signaling requires ERK1/2 activity in mouse granulosa and cumulus cells. J Cell Sci, 123:3166-3176.

Scaramuzzi RJ, Baird DT, Campbell BK, Driancourt MA, Dupont J, Fortune JE, Gilchrist RB, Martin GB, McNatty KP, McNeilly AS, Monget P, Monniaux D, Viñoles C, Webb R. 2011. Regulation of folliculogenesis and the determination of ovulation rate in ruminants. Reprod Fertil Dev, 23:444-467.

Shimada M, Hernandez-Gonzalez I, Gonzalez- Robayna I, Richards JS. 2006. Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol, 20:1352-1365.

Singh B, Rutledge JM, Armstrong DT. 1995. Epidermal growth factor and its receptor gene expression and peptide localization in porcine ovarian follicles. Mol Reprod Dev, 40:391-399.

Sirard MA, Picard L, Dery M, Coenen K, Blondin P. 1999. The time interval between FSH administration and ovarian aspiration influences the development of cattle oocytes. Theriogenology, 51:699-708.

Su YQ, Sugiura K, Li Q, Wigglesworth K, Matzuk MM, Eppig JJ. 2010. Mouse oocytes enable LH-induced maturation of the cumulus-oocyte complex via promoting EGF receptor-dependent signaling. Mol Endocrinol, 24:1230-1239.

Sugimura S, Kobayashi S, Hashiyada Y, Ohtake M, Kaneda M, Yamanouchi T, Matsuda H, Aikawa Y, Watanabe S, Nagai T, Kobayashi E, Konishi K, Imai K. 2012. Follicular growth-stimulated cows provide favorable oocytes for producing cloned embryos. Cell Reprogram, 14:29-37.

Sugimura S, Ritter LJ, Sutton-McDowall ML, Mottershead DG, Thompson JG, Gilchrist RB. 2014. Amphiregulin co-operates with bone morphogenetic protein 15 to increase bovine oocyte developmental competence: effects on gap junction-mediated metabolite supply. Mol Hum Reprod, 20:499-513.

Sugimura S, Ritter LJ, Rose RD, Thompson JG, Smitz J, Mottershead DG, Gilchrist RB. 2015. Promotion of EGF receptor signaling improves the quality of low developmental competence oocytes. Dev Biol, 403:139-149.

Sugimura S, Kobayashi N, Okae H, Yamanouchi T, Matsuda H, Kojima T, Yajima A, Hashiyada Y, Kaneda M, Sato K, Imai K, Tanemura K, Arima T, Gilchrist RB. 2017. Transcriptomic signature of the follicular somatic compartment surrounding an oocyte with high developmental competence. Sci Rep, 7:6815. doi: 10.1038/s41598-017-07039-5.

Thibault C. 1977. Hammond memorial lecture. Are follicular maturation and oocyte maturation independent proccesses? J Reprod Fertil, 51:1-15.

Thomas FH, Wilson H, Silvestri A, Fraser HM. 2008. Thrombospondin-1 expression is increased during follicular atresia in the primate ovary. Endocrinology, 149:185-192.

Vanderhyden BC, Caron PJ, Buccione R, Eppig JJ. 1990. Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev Biol, 140:307-317.

Wang WB, Levy DE, Lee CK. 2011. STAT3 negatively regulates type I IFN-mediated antiviral response. J Immunol, 187:2578-2585.

Wathlet S, Adriaenssens T, Segers I, Verheyen G, Van de Velde H, Coucke W, Ron El R, Devroey P, Smitz J. 2011. Cumulus cell gene expression predicts better cleavage-stage embryo or blastocyst development and pregnancy for ICSI patients. Hum Reprod, 26:1035-1051.

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, 92:23. doi: 10.1095/biolreprod.114.121756.

5b8e8a8d0e8825c135dd6777 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections