Rewarding Conversation Between Oocyte and Cumulus Cells Directs the Process of Folliculogenesis
Abstract
The process of folliculogenesis needs a balanced environment to create a mature oocyte that is expected to have characteristics in order to form the ability of a healthy fertilisation. Previous studies have been focused on endocrine effects of hypothalamic–pituitary system on ovarian functions. Influences of this system have been studied for many years. Besides of extra-ovarian factors, recent studies have focused on intraovarian factors which forms the relationship between oocyte and cumulus cells. It has been shown that even the maturity of antral follicule and oocyte has been effected from this communication. These factors which takes part at process of folliculogenesis, were shown to be efficient even at the success of assisted reproductive technologies. We studied general lines of this conversation based on main research articles that continue to be relevant at this topic.
References
Juengel J, McNatty K. The role of proteins of the transforming growth factor-β superfamily in the intraovarian regulation of follicular development. Human reproduction update. 2005;11(2):144-61.
Knight PG, Glister C. TGF-β superfamily members and ovarian follicle development. Reproduction. 2006;132(2):191-206.
Chang H-M, Qiao J, Leung PC. Oocyte–somatic cell interactions in the human ovary—novel role of bone morphogenetic proteins and growth differentiation factors. Human reproduction update. 2016;23(1):1-18.
Steptoe PC, Edwards RG. Birth after reimplantation of a human embryo. Lancet. 1978;2(8085):366.
Lin D, Ran J, Zhu S, Quan S, Ye B, Yu A, et al. Effect of GOLPH3 on cumulus granulosa cell apoptosis and ICSI pregnancy outcomes. Scientific Reports. 2017;7(1):7863.
Wigglesworth K, Lee K-B, O’Brien MJ, Peng J, Matzuk MM, Eppig JJ. Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammalian oocytes. Proceedings of the National Academy of Sciences. 2013;110(39):E3723-E9.
Raman RS, Chan PJ, Corselli JU, Patton WC, Jacobson JD, Chan SR, et al. Comet assay of cumulus cell DNA status and the relationship to oocyte fertilization via intracytoplasmic sperm injection. Human Reproduction. 2001;16(5):831-5.
Sanfins A, Rodrigues P, Albertini DF. GDF-9 and BMP-15 direct the follicle symphony. Journal of assisted reproduction and genetics. 2018:1-10.
Belli M, Shimasaki S. Molecular Aspects and Clinical Relevance of GDF9 and BMP15 in Ovarian Function. Vitamins and hormones. 2018;107:317-48.
Da Broi M, Giorgi V, Wang F, Keefe D, Albertini D, Navarro P. Influence of follicular fluid and cumulus cells on oocyte quality: clinical implications. Journal of assisted reproduction and genetics. 2018;35(5):735-51.
Li Y, Li R-Q, Ou S-B, Zhang N-F, Ren L, Wei L-N, et al. Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reproductive Biology and Endocrinology. 2014;12(1):81.
Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocrine reviews. 1996;17(2):121-55.
de Castro FC, Cruz MHC, Leal CLV. Role of growth differentiation factor 9 and bone morphogenetic protein 15 in ovarian function and their importance in mammalian female fertility—A review. Asian-Australasian journal of animal sciences. 2016;29(8):1065.
McNatty KP, Juengel JL, Reader KL, Lun S, Myllymaa S, Lawrence SB, et al. Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants. Reproduction. 2005;129(4):481-7.
Peng J, Li Q, Wigglesworth K, Rangarajan A, Kattamuri C, Peterson RT, et al. Growth differentiation factor 9: bone morphogenetic protein 15 heterodimers are potent regulators of ovarian functions. Proceedings of the National Academy of Sciences. 2013;110(8):E776-E85.
Abir R, Ben-Haroush A, Melamed N, Felz C, Krissi H, Fisch B. Expression of bone morphogenetic proteins 4 and 7 and their receptors IA, IB, and II in human ovaries from fetuses and adults. Fertility and sterility. 2008;89(5):1430-40.
Erickson GF, Shimasaki S. The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reproductive Biology and Endocrinology. 2003;1(1):9.
Wagner DO, Sieber C, Bhushan R, Börgermann JH, Graf D, Knaus P. BMPs: from bone to body morphogenetic proteins. American Association for the Advancement of Science; 2010.
Yoshino O, McMahon HE, Sharma S, Shimasaki S. A unique preovulatory expression pattern plays a key role in the physiological functions of BMP-15 in the mouse. Proceedings of the National Academy of Sciences. 2006;103(28):10678-83.
Su Y-Q, Sugiura K, Wigglesworth K, O'Brien MJ, Affourtit JP, Pangas SA, et al. Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development. 2008;135(1):111-21.
Falck B. Site of production of oestrogen in rat ovary as studied in micro‐transplants. Acta Physiologica Scandinavica. 1960;47(4):1-101.
Hutt KJ, Albertini DF. An oocentric view of folliculogenesis and embryogenesis. Reproductive biomedicine online. 2007;14(6):758-64.
Erickson GF, Shimasaki S. The role of the oocyte in folliculogenesis. Trends in Endocrinology & Metabolism. 2000;11(5):193-8.
Matzuk MM, Burns KH, Viveiros MM, Eppig JJ. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science. 2002;296(5576):2178-80.
Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Human reproduction update. 2008;14(2):159-77.
Su Y-Q, Sugiura K, Eppig JJ, editors. Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Seminars in reproductive medicine; 2009: © Thieme Medical Publishers.
Dias F, Khan M, Adams G, Sirard M, Singh J. Granulosa cell function and oocyte competence: super-follicles, super-moms and super-stimulation in cattle. Animal reproduction science. 2014;149(1-2):80-9.
Shi Y, Massagué J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. cell. 2003;113(6):685-700.
Miyazono K, Kusanagi K, Inoue H. Divergence and convergence of TGF‐β/BMP signaling. Journal of cellular physiology. 2001;187(3):265-76.
Mueller TD, Nickel J. Promiscuity and specificity in BMP receptor activation. FEBS letters. 2012;586(14):1846-59.
Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature. 2003;425(6958):577.
Moore RK, Otsuka F, Shimasaki S. Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. Journal of Biological Chemistry. 2003;278(1):304-10.
Mazerbourg S, Klein C, Roh J, Kaivo-Oja N, Mottershead DG, Korchynskyi O, et al. Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5. Molecular Endocrinology. 2004;18(3):653-65.
Vitt UA, Mazerbourg S, Klein C, Hsueh AJ. Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biology of reproduction. 2002;67(2):473-80.
Mazerbourg S, Hsueh AJ. Genomic analyses facilitate identification of receptors and signalling pathways for growth differentiation factor 9 and related orphan bone morphogenetic protein/growth differentiation factor ligands. Human reproduction update. 2006;12(4):373-83.
Lintern-Moore S, Moore G. The initiation of follicle and oocyte growth in the mouse ovary. Biology of reproduction. 1979;20(4):773-8.
Skinner MK. Regulation of primordial follicle assembly and development. Human reproduction update. 2005;11(5):461-71.
Huang Z, Wells D. The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome. Molecular human reproduction. 2010;16(10):715-25.
Makowski L, Caspar D, Phillips W, Goodenough D. Gap junction structures: Analysis of the x-ray diffraction data. The Journal of cell biology. 1977;74(2):629-45.
Mehlmann LM, Jones TL, Jaffe LA. Meiotic arrest in the mouse follicle maintained by a Gs protein in the oocyte. Science. 2002;297(5585):1343-5.
Richard FJ, Tsafriri A, Conti M. Role of phosphodiesterase type 3A in rat oocyte maturation. Biology of reproduction. 2001;65(5):1444-51.
Norris RP, Ratzan WJ, Freudzon M, Mehlmann LM, Krall J, Movsesian MA, et al. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development. 2009;136(11):1869-78.
Vaccari S, Weeks JL, Hsieh M, Menniti FS, Conti M. Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biology of reproduction. 2009;81(3):595-604.
Sugiura K, Su Y-Q, Diaz FJ, Pangas SA, Sharma S, Wigglesworth K, et al. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development. 2007;134(14):2593-603.
Nagashima T, Li Q, Clementi C, Lydon JP, DeMayo FJ, Matzuk MM. BMPR2 is required for postimplantation uterine function and pregnancy maintenance. The Journal of clinical investigation. 2013;123(6):2539-50.
Takebayashi K, Takakura K, Wang H-Q, Kimura F, Kasahara K, Noda Y. Mutation analysis of the growth differentiation factor-9 and-9B genes in patients with premature ovarian failure and polycystic ovary syndrome. Fertility and sterility. 2000;74(5):976-9.
Crispi S, Piccolo MT, D'avino A, Donizetti A, Viceconte R, Spyrou M, et al. Transcriptional profiling of endometriosis tissues identifies genes related to organogenesis defects. Journal of cellular physiology. 2013;228(9):1927-34.
Dube JL, Wang P, Elvin J, Lyons KM, Celeste AJ, Matzuk MM. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Molecular endocrinology. 1998;12(12):1809-17.
Incerti B, Dong J, Borsani G, Matzuk MM. Structure of the mouse growth/differentiation factor 9 gene. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research. 1994;1222(1):125-8.
Mottershead DG, Sugimura S, Al-Musawi SL, Li J-J, Richani D, White MA, et al. Cumulin, an oocyte-secreted heterodimer of the transforming growth factor-β family, is a potent activator of granulosa cells and improves oocyte quality. Journal of Biological Chemistry. 2015;290(39):24007-20.
