Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 9/2017

01-09-2017 | Reproductive Physiology and Disease

Age-related expression of TGF beta family receptors in human cumulus oophorus cells

Authors: A. Ribeiro, C. Freitas, L. Matos, A. Gouveia, F. Gomes, J. L. Silva Carvalho, H. Almeida

Published in: Journal of Assisted Reproduction and Genetics | Issue 9/2017

Login to get access

Abstract

Purpose

During ovarian follicle growth, local cellular interactions are essential for oocyte quality acquisition and successful fertilization. While cumulus cells (CCs) nurture oocytes, they also deliver oocyte-secreted factors (OSFs) that activate receptors on CCs. We hypothesized that disturbance of those interactions contributes to age-related lower reproductive success in women submitted to assisted reproductive technology treatments.

Methods

Women aged 27–48, without recognized personal reproductive disorder, were enrolled in the study and divided in <35- and ≥35-year-old groups. CCs collected upon follicle aspiration were processed for immunocytochemistry and RNA extraction. The expression patterns of OSF receptors BMPR2, ALK 4, ALK5, and activin receptor-like kinase (ALK6) were studied.

Results

Independently of age, receptors were found mostly in the cell periphery. The quantitative assay revealed that in older women, BMPR2, ALK 4, and ALK6 were all significantly decreased, whereas ALK5 was slightly increased.

Conclusions

Female age imparts an effect on the expression of OSF receptors in CCs. The findings indicate that reproductive aging affects the local regulation of signaling pathways mediated by BMPR2, ALK6, and ALK4 receptor activation, suggesting their joint involvement.
Literature
1.
go back to reference Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev. 1996;17(2):121–55.CrossRefPubMed Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev. 1996;17(2):121–55.CrossRefPubMed
2.
go back to reference Yoo SW, Savchev S, Sergott L, Rezai T, Lopez MF, Von Wald T, Eaton JL, Reindollar R, Usheva A. A large network of interconnected signaling pathways in human ovarian follicles is supported by the gene expression activity of the granulosa cells. Reprod Sci. 2011;18(5):476–84.CrossRefPubMed Yoo SW, Savchev S, Sergott L, Rezai T, Lopez MF, Von Wald T, Eaton JL, Reindollar R, Usheva A. A large network of interconnected signaling pathways in human ovarian follicles is supported by the gene expression activity of the granulosa cells. Reprod Sci. 2011;18(5):476–84.CrossRefPubMed
3.
go back to reference Erickson GF, Shimasaki S. The role of the oocyte in folliculogenesis. Trends Endocrinol Metab. 2000;11:193.CrossRefPubMed Erickson GF, Shimasaki S. The role of the oocyte in folliculogenesis. Trends Endocrinol Metab. 2000;11:193.CrossRefPubMed
4.
go back to reference Makabe S, Naguro T, Stallone T. Oocyte–follicle cell interactions during ovarian follicle development, as seen by high resolution scanning and transmission electron microscopy in humans. Microsc Res Tech. 2006;69:436–49.CrossRefPubMed Makabe S, Naguro T, Stallone T. Oocyte–follicle cell interactions during ovarian follicle development, as seen by high resolution scanning and transmission electron microscopy in humans. Microsc Res Tech. 2006;69:436–49.CrossRefPubMed
5.
go back to reference Matzuk MM, Burns KH, Viveiros MM, Eppig JJ. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science. 2002;296(5576):2178–80.CrossRefPubMed Matzuk MM, Burns KH, Viveiros MM, Eppig JJ. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science. 2002;296(5576):2178–80.CrossRefPubMed
6.
go back to reference Juengel JL, McNatty KP. The role of proteins of the transforming growth factor-b superfamily in the intraovarian regulation of follicular development. Hum Reprod Update. 2005;11(2):144–16.CrossRef Juengel JL, McNatty KP. The role of proteins of the transforming growth factor-b superfamily in the intraovarian regulation of follicular development. Hum Reprod Update. 2005;11(2):144–16.CrossRef
7.
go back to reference Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature. 1996;383:531–5.CrossRefPubMed Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature. 1996;383:531–5.CrossRefPubMed
8.
go back to reference Carabatsos MJ, Elvin J, Matzuk MM, Albertini DF. Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev Biol. 1998;204:373–84.CrossRefPubMed Carabatsos MJ, Elvin J, Matzuk MM, Albertini DF. Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev Biol. 1998;204:373–84.CrossRefPubMed
9.
go back to reference Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, Prasad SV, Skinner SS, Dunbar BS, Dube JL, Celeste AJ, Matzuk MM. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol. 2001;15:854–66.CrossRefPubMed Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, Prasad SV, Skinner SS, Dunbar BS, Dube JL, Celeste AJ, Matzuk MM. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol. 2001;15:854–66.CrossRefPubMed
10.
go back to reference Moore RK, Otsuka F, Shimasaki S. Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. J Biol Chem. 2003;278:304–10.CrossRefPubMed Moore RK, Otsuka F, Shimasaki S. Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. J Biol Chem. 2003;278:304–10.CrossRefPubMed
11.
go back to reference 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. Hum Reprod Update. 2006;12(4):373–83.CrossRefPubMed 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. Hum Reprod Update. 2006;12(4):373–83.CrossRefPubMed
12.
go back to reference Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update. 2008;14(2):159–77.CrossRefPubMed Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update. 2008;14(2):159–77.CrossRefPubMed
13.
go back to reference Li Q, Agno JE, Edson MA, Nagaraja AK, Nagashima T, Matzuk MM. Transforming growth factor β receptor type 1 is essential for female reproductive tract integrity and function. PLoS Genet. 2011;7(10):e1002320.CrossRefPubMedPubMedCentral Li Q, Agno JE, Edson MA, Nagaraja AK, Nagashima T, Matzuk MM. Transforming growth factor β receptor type 1 is essential for female reproductive tract integrity and function. PLoS Genet. 2011;7(10):e1002320.CrossRefPubMedPubMedCentral
14.
go back to reference Peng J, Li Q, Wigglesworth K, Rangarajan A, Kattamuri C, Peterson RT, Eppig JJ, Thompson TB, Matzuk MM. Growth differentiation factor 9:bone morphogenetic protein 15 heterodimers are potent regulators of ovarian functions. Proc Natl Acad Sci U S A. 2013 Feb 19;110(8):E776–85.CrossRefPubMedPubMedCentral Peng J, Li Q, Wigglesworth K, Rangarajan A, Kattamuri C, Peterson RT, Eppig JJ, Thompson TB, Matzuk MM. Growth differentiation factor 9:bone morphogenetic protein 15 heterodimers are potent regulators of ovarian functions. Proc Natl Acad Sci U S A. 2013 Feb 19;110(8):E776–85.CrossRefPubMedPubMedCentral
15.
go back to reference Mottershead DG, 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. J Biol Chem. 2015;290(39):24007–20.CrossRefPubMedPubMedCentral Mottershead DG, 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. J Biol Chem. 2015;290(39):24007–20.CrossRefPubMedPubMedCentral
16.
go back to reference Russell DL, et al. Bidirectional communication between cumulus cells and the oocyte: old hands and new players? Theriogenology. 2016;86(1):62–8.CrossRefPubMed Russell DL, et al. Bidirectional communication between cumulus cells and the oocyte: old hands and new players? Theriogenology. 2016;86(1):62–8.CrossRefPubMed
17.
go back to reference Sutton-McDowall ML, Gilchrist RB, Thompson JG. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction. 2010;139(4):685–95.CrossRefPubMed Sutton-McDowall ML, Gilchrist RB, Thompson JG. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction. 2010;139(4):685–95.CrossRefPubMed
18.
go back to reference Tatemoto H, Sakurai N, Muto N. Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol Reprod. 2000;63:805–10.CrossRefPubMed Tatemoto H, Sakurai N, Muto N. Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol Reprod. 2000;63:805–10.CrossRefPubMed
19.
go back to reference Matos L, Stevenson D, Gomes F, Silva-Carvalho JL, Almeida H. Superoxide dismutase expression in human cumulus oophorus cells. Mol Hum Reprod. 2009;15(7):411–9.CrossRefPubMed Matos L, Stevenson D, Gomes F, Silva-Carvalho JL, Almeida H. Superoxide dismutase expression in human cumulus oophorus cells. Mol Hum Reprod. 2009;15(7):411–9.CrossRefPubMed
20.
go back to reference Tanghe S, Van Soom A, Nauwynck H, Coryn M, de Kruif A. Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev. 2002;61(3):414–24.CrossRefPubMed Tanghe S, Van Soom A, Nauwynck H, Coryn M, de Kruif A. Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev. 2002;61(3):414–24.CrossRefPubMed
21.
go back to reference Assou S, Anahory T, Pantesco V, Le Carrour T, Pellestor F, Klein B, Reyftmann L, Dechaud H, De Vos J, Samir H. The human cumulus–oocyte complex gene-expression profile. Hum Reprod. 2006;21:1705–19.CrossRefPubMedPubMedCentral Assou S, Anahory T, Pantesco V, Le Carrour T, Pellestor F, Klein B, Reyftmann L, Dechaud H, De Vos J, Samir H. The human cumulus–oocyte complex gene-expression profile. Hum Reprod. 2006;21:1705–19.CrossRefPubMedPubMedCentral
22.
go back to reference Assou S, Haouzi D, Mahmoud K, Aouacheria A, Guillemin Y, Pantesco V, Rème T, Dechaud H, De Vos J, Hamamah S. A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study. Mol Hum Reprod. 2008;14(12):711–9.CrossRefPubMed Assou S, Haouzi D, Mahmoud K, Aouacheria A, Guillemin Y, Pantesco V, Rème T, Dechaud H, De Vos J, Hamamah S. A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study. Mol Hum Reprod. 2008;14(12):711–9.CrossRefPubMed
23.
go back to reference Huang Z, Wells D. The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome. Mol Hum Reprod. 2010;16(10):715–25.CrossRefPubMed Huang Z, Wells D. The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome. Mol Hum Reprod. 2010;16(10):715–25.CrossRefPubMed
24.
go back to reference Li Y, Li R-Q, Song-Bang O, Zhang N-F, Ren L, Wei L-N, Zhang Q-X, Yang D-Z. Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reprod Biol Endocrinol. 2014;12:81.CrossRefPubMedPubMedCentral Li Y, Li R-Q, Song-Bang O, Zhang N-F, Ren L, Wei L-N, Zhang Q-X, Yang D-Z. Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reprod Biol Endocrinol. 2014;12:81.CrossRefPubMedPubMedCentral
25.
go back to reference Alviggi C, Humaidan P, Howles CM, Tredway D, Hillier SG. Biological versus chronological ovarian age: implications for assisted reproductive technology. Reprod Biol Endocrinology. 2009;7:101.CrossRef Alviggi C, Humaidan P, Howles CM, Tredway D, Hillier SG. Biological versus chronological ovarian age: implications for assisted reproductive technology. Reprod Biol Endocrinology. 2009;7:101.CrossRef
26.
go back to reference Hansen KR, Knowlton NS, Thyer AC, Charleston JS, Soules MR, Klein NA. A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Hum Reprod. 2008;23:699–708.CrossRefPubMed Hansen KR, Knowlton NS, Thyer AC, Charleston JS, Soules MR, Klein NA. A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Hum Reprod. 2008;23:699–708.CrossRefPubMed
28.
go back to reference Schwartz D, Mayaux MJ. Female fecundity as a function of age: results of artificial insemination in 2193 nulliparous women with azoospermic husbands. Federation CECOS. N Engl J Med. 1982;306(7):404–6.CrossRefPubMed Schwartz D, Mayaux MJ. Female fecundity as a function of age: results of artificial insemination in 2193 nulliparous women with azoospermic husbands. Federation CECOS. N Engl J Med. 1982;306(7):404–6.CrossRefPubMed
29.
go back to reference Kupka MS, Ferraretti AP, de Mouzon J, Erb K, D’Hooghe T, Castilla JA, Calhaz-Jorge C, De Geyter C, Goossens V. European IVF-Monitoring Consortium, for the European Society of Human Reproduction and Embryology. Assisted reproductive technology in Europe, 2010: results generated from European registers by ESHRE†. Hum Reprod. 2014;29(10):2099–113.CrossRefPubMed Kupka MS, Ferraretti AP, de Mouzon J, Erb K, D’Hooghe T, Castilla JA, Calhaz-Jorge C, De Geyter C, Goossens V. European IVF-Monitoring Consortium, for the European Society of Human Reproduction and Embryology. Assisted reproductive technology in Europe, 2010: results generated from European registers by ESHRE†. Hum Reprod. 2014;29(10):2099–113.CrossRefPubMed
30.
go back to reference Centers for Disease Control and Prevention. American Society for Reproductive Medicine, Society for Assisted Reproductive Technology. In: Assisted reproductive technology national summary report. Atlanta (GA): US Dept of Health and Human Services; 2014. p. 2016. Centers for Disease Control and Prevention. American Society for Reproductive Medicine, Society for Assisted Reproductive Technology. In: Assisted reproductive technology national summary report. Atlanta (GA): US Dept of Health and Human Services; 2014. p. 2016.
32.
go back to reference Broekmans FJ, Knauff EA, teVelde ER, Macklon NS, Fauser BC. Female reproductive ageing: current knowledge and future trends. Trends Endocrinol Metab. 2007;18(2):58–65.CrossRefPubMed Broekmans FJ, Knauff EA, teVelde ER, Macklon NS, Fauser BC. Female reproductive ageing: current knowledge and future trends. Trends Endocrinol Metab. 2007;18(2):58–65.CrossRefPubMed
33.
go back to reference Rattanachaiyanont M, Leader A, Léveillé MC. Lack of correlation between oocyte-corona-cumulus complex morphology and nuclear maturity of oocytes collected in stimulated cycles for intracytoplasmic sperm injection. Fertil Steril. 1999;71(5):937–40.CrossRefPubMed Rattanachaiyanont M, Leader A, Léveillé MC. Lack of correlation between oocyte-corona-cumulus complex morphology and nuclear maturity of oocytes collected in stimulated cycles for intracytoplasmic sperm injection. Fertil Steril. 1999;71(5):937–40.CrossRefPubMed
34.
go back to reference Ebner T, Moser M, Shebl O, Sommergruber M, Yaman C, Tews G. Blood clots in the cumulus-oocyte complex predict poor oocyte quality and post-fertilization development. Reprod BioMed Online. 2008;16(6):801–7.CrossRefPubMed Ebner T, Moser M, Shebl O, Sommergruber M, Yaman C, Tews G. Blood clots in the cumulus-oocyte complex predict poor oocyte quality and post-fertilization development. Reprod BioMed Online. 2008;16(6):801–7.CrossRefPubMed
35.
go back to reference Albertini DF, Combelles CM, Benecchi EH, Mary CJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001;121:647–53.CrossRefPubMed Albertini DF, Combelles CM, Benecchi EH, Mary CJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001;121:647–53.CrossRefPubMed
36.
go back to reference Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction. 2001;122(6):829–38.CrossRefPubMed Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction. 2001;122(6):829–38.CrossRefPubMed
37.
go back to reference Galloway SM, McNatty KP, Cambridge LM, Laitinen MP, Juengel JL, Jokiranta TS, McLaren RJ, Luiro K, Dodds KG, Montgomery GW, et al. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet. 2000;25:279–83.CrossRefPubMed Galloway SM, McNatty KP, Cambridge LM, Laitinen MP, Juengel JL, Jokiranta TS, McLaren RJ, Luiro K, Dodds KG, Montgomery GW, et al. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet. 2000;25:279–83.CrossRefPubMed
38.
go back to reference Silva JRV, van den Hurk R, Van Tol HTA, Rolen BAJ, Figueiredo JR. Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), and BMP receptors in the ovaries of goats. Mol Reprod Devel. 2005;70:11–9.CrossRefPubMed Silva JRV, van den Hurk R, Van Tol HTA, Rolen BAJ, Figueiredo JR. Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), and BMP receptors in the ovaries of goats. Mol Reprod Devel. 2005;70:11–9.CrossRefPubMed
39.
go back to reference Bodensteiner KJ, Clay CM, Moeller CL, Sawyer HR. Molecular cloning of the ovine growth/differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries. Biol Reprod. 1999;60(2):381–6.CrossRefPubMed Bodensteiner KJ, Clay CM, Moeller CL, Sawyer HR. Molecular cloning of the ovine growth/differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries. Biol Reprod. 1999;60(2):381–6.CrossRefPubMed
40.
go back to reference Aaltonen J, Laitinen MP, Vuojolainen K, Jaatinen R, Horelli-Kuitunen N, Seppa L, Louhio H, Tuuri T, Sjoberg J, Butzow R, Hovata O, Dale L, Ritvos O. Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J Clin Endocrinol Metab. 1999;84:2744–275.PubMed Aaltonen J, Laitinen MP, Vuojolainen K, Jaatinen R, Horelli-Kuitunen N, Seppa L, Louhio H, Tuuri T, Sjoberg J, Butzow R, Hovata O, Dale L, Ritvos O. Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J Clin Endocrinol Metab. 1999;84:2744–275.PubMed
41.
go back to reference Teixeira Filho FL, Baracat EC, Lee TH, Suh CS, Matsui M, Chang RJ, Shimasaki S, Erickson GF. Aberrant expression of growth differentiation factor-9 in oocytes of women with polycystic ovary syndrome. J Clin Endocrinol Metab. 2002;87:1337–44.CrossRefPubMed Teixeira Filho FL, Baracat EC, Lee TH, Suh CS, Matsui M, Chang RJ, Shimasaki S, Erickson GF. Aberrant expression of growth differentiation factor-9 in oocytes of women with polycystic ovary syndrome. J Clin Endocrinol Metab. 2002;87:1337–44.CrossRefPubMed
42.
go back to reference Margulis S, Abir R, Felz C, Nitke S, Krissi H, Fisch B. Bone morphogenetic protein 15 expression in human ovaries from fetuses, girls, and women. Fertil Steril. 2009;92(5):1666–73.CrossRefPubMed Margulis S, Abir R, Felz C, Nitke S, Krissi H, Fisch B. Bone morphogenetic protein 15 expression in human ovaries from fetuses, girls, and women. Fertil Steril. 2009;92(5):1666–73.CrossRefPubMed
43.
go back to reference Sun RZ, Lei L, Cheng L, Jin ZF, Zu SJ, Shan ZY, Wang ZD, Zhang JX, Liu ZH. Expression of GDF-9, BMP-15 and their receptors in mammalian ovary follicles. J Mol Histol. 2010;41(6):325–32.CrossRefPubMed Sun RZ, Lei L, Cheng L, Jin ZF, Zu SJ, Shan ZY, Wang ZD, Zhang JX, Liu ZH. Expression of GDF-9, BMP-15 and their receptors in mammalian ovary follicles. J Mol Histol. 2010;41(6):325–32.CrossRefPubMed
44.
go back to reference Sidis Y, Fujiwara T, Leykin L, Isaacson K, Toth T, Schneyer AL. Characterization of inhibin/activin subunit, activin receptor, and follistatin messenger ribonucleic acid in human and mouse oocytes: evidence for activin’s paracrine signaling from granulosa cells to oocytes. Biol Reprod. 1998;59(4):807–12.CrossRefPubMed Sidis Y, Fujiwara T, Leykin L, Isaacson K, Toth T, Schneyer AL. Characterization of inhibin/activin subunit, activin receptor, and follistatin messenger ribonucleic acid in human and mouse oocytes: evidence for activin’s paracrine signaling from granulosa cells to oocytes. Biol Reprod. 1998;59(4):807–12.CrossRefPubMed
45.
go back to reference Wei LN, Liang XY, Fang C, Zhang MF. Abnormal expression of growth differentiation factor 9 and bone morphogenetic protein 15 in stimulated oocytes during maturation from women with polycystic ovary syndrome. Fertil Steril. 2011;96(2):464–8.CrossRefPubMed Wei LN, Liang XY, Fang C, Zhang MF. Abnormal expression of growth differentiation factor 9 and bone morphogenetic protein 15 in stimulated oocytes during maturation from women with polycystic ovary syndrome. Fertil Steril. 2011;96(2):464–8.CrossRefPubMed
46.
go back to reference Hreinsson JG, Scott JE, Rasmussen C, Swahn ML, Hsueh AJW, Hovatta O. Growth differentiation factor-9 promotes the growth, development, and survival of human ovarian follicles in organ culture. J Clin Endocrinol Metab. 2002;87:316–21.CrossRefPubMed Hreinsson JG, Scott JE, Rasmussen C, Swahn ML, Hsueh AJW, Hovatta O. Growth differentiation factor-9 promotes the growth, development, and survival of human ovarian follicles in organ culture. J Clin Endocrinol Metab. 2002;87:316–21.CrossRefPubMed
47.
go back to reference Di Pasquale E, Beck-Peccoz P, Persani L. Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am J Hum Genet. 2004;75:106–11.CrossRefPubMedPubMedCentral Di Pasquale E, Beck-Peccoz P, Persani L. Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am J Hum Genet. 2004;75:106–11.CrossRefPubMedPubMedCentral
48.
go back to reference Di Pasquale E, Rossetti R, Marozzi A, Bodega B, Borgato S, Cavallo L, Einaudi S, Radetti G, Russo G, Sacco M, Wasniewska M, Cole T, Beck-Peccoz P, Nelson LM, Persani L. Identification of new variants of human BMP15 gene in a large cohort of women with premature ovarian failure. J Clin Endocrinol Metab. 2006;91(5):1976–9.CrossRefPubMed Di Pasquale E, Rossetti R, Marozzi A, Bodega B, Borgato S, Cavallo L, Einaudi S, Radetti G, Russo G, Sacco M, Wasniewska M, Cole T, Beck-Peccoz P, Nelson LM, Persani L. Identification of new variants of human BMP15 gene in a large cohort of women with premature ovarian failure. J Clin Endocrinol Metab. 2006;91(5):1976–9.CrossRefPubMed
50.
go back to reference Guéripel X, Brun V, Gougeon A. Oocyte bone morphogenetic protein 15, but not growth differentiation factor 9, is increased during gonadotropin-induced follicular development in the immature mouse and is associated with cumulus oophorus expansion. Biol Reprod. 2006;75(6):836–43.CrossRefPubMed Guéripel X, Brun V, Gougeon A. Oocyte bone morphogenetic protein 15, but not growth differentiation factor 9, is increased during gonadotropin-induced follicular development in the immature mouse and is associated with cumulus oophorus expansion. Biol Reprod. 2006;75(6):836–43.CrossRefPubMed
51.
go back to reference Persani L, Rossetti R, Di Pasquale E, Cacciatore C, Fabre S. The fundamental role of bone morphogenetic protein 15 in ovarian function and its involvement in female fertility disorders. Hum Reprod Update. 2014;20(6):869–83.CrossRefPubMed Persani L, Rossetti R, Di Pasquale E, Cacciatore C, Fabre S. The fundamental role of bone morphogenetic protein 15 in ovarian function and its involvement in female fertility disorders. Hum Reprod Update. 2014;20(6):869–83.CrossRefPubMed
52.
go back to reference Wells RG, Yankelev H, Lin HY, Lodish HF. Biosynthesis of the type I and type II TGF-beta receptors. Implications for complex formation. J Biol Chem. 1997;272(17):11444–51.CrossRefPubMed Wells RG, Yankelev H, Lin HY, Lodish HF. Biosynthesis of the type I and type II TGF-beta receptors. Implications for complex formation. J Biol Chem. 1997;272(17):11444–51.CrossRefPubMed
53.
go back to reference Mazerbourg S, Klein C, Roh J, Kaivo-Oja N, Mottershead DG, Korchynskyi O, Ritvos O, Hsueh AJ. Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5. Mol Endocrinol. 2004;18(3):653–65.CrossRefPubMed Mazerbourg S, Klein C, Roh J, Kaivo-Oja N, Mottershead DG, Korchynskyi O, Ritvos O, Hsueh AJ. Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5. Mol Endocrinol. 2004;18(3):653–65.CrossRefPubMed
54.
go back to reference Moore RK, Shimasaki S. Molecular biology and physiological role of the oocyte factor, BMP-15. Mol Cell Endocrinol. 2005;234(1–2):67–73.CrossRefPubMed Moore RK, Shimasaki S. Molecular biology and physiological role of the oocyte factor, BMP-15. Mol Cell Endocrinol. 2005;234(1–2):67–73.CrossRefPubMed
55.
go back to reference Feary ES, Juengel JL, Smith P, French MC, O’Connell AR, Lawrence SB, Galloway SM, Davis GH, McNatty KP. Patterns of expression of messenger RNAs encoding GDF9, BMP15, TGFBR1, BMPR1B, and BMPR2 during follicular development and characterization of ovarian follicular populations in ewes carrying the Woodlands FecX2W mutation. Biol Reprod. 2007;77(6):990–8.CrossRefPubMed Feary ES, Juengel JL, Smith P, French MC, O’Connell AR, Lawrence SB, Galloway SM, Davis GH, McNatty KP. Patterns of expression of messenger RNAs encoding GDF9, BMP15, TGFBR1, BMPR1B, and BMPR2 during follicular development and characterization of ovarian follicular populations in ewes carrying the Woodlands FecX2W mutation. Biol Reprod. 2007;77(6):990–8.CrossRefPubMed
56.
go back to reference Dixit H, Rao LK, Padmalatha VV, Kanakavalli M, Deenadayal M, Gupta N, Chakrabarty B, Singh L. Missense mutations in the BMP15 gene are associated with ovarian failure. Hum Genet. 2006;119:408–15.CrossRefPubMed Dixit H, Rao LK, Padmalatha VV, Kanakavalli M, Deenadayal M, Gupta N, Chakrabarty B, Singh L. Missense mutations in the BMP15 gene are associated with ovarian failure. Hum Genet. 2006;119:408–15.CrossRefPubMed
57.
go back to reference Laissue P, Christin-Maitre S, Touraine P, Kuttenn F, Ritvos O, Aittomaki K, Bourcigaux N, Jacquesson L, Bouchard P, Frydman R, Dewailly D, Reyss AC, Jeffery L, Bachelot A, Massin N, Fellous M, Veitia RA. Mutations and sequence variants in GDF9 and BMP15 in patients with premature ovarian failure. Eur J Endocrinol. 2006;154(5):739–44.CrossRefPubMed Laissue P, Christin-Maitre S, Touraine P, Kuttenn F, Ritvos O, Aittomaki K, Bourcigaux N, Jacquesson L, Bouchard P, Frydman R, Dewailly D, Reyss AC, Jeffery L, Bachelot A, Massin N, Fellous M, Veitia RA. Mutations and sequence variants in GDF9 and BMP15 in patients with premature ovarian failure. Eur J Endocrinol. 2006;154(5):739–44.CrossRefPubMed
58.
go back to reference Zhao SY, Qiao J, Chen YJ, Liu P, Li J, Yan J. Expression of growth differentiation factor-9 and bone morphogenetic protein-15 in oocytes and cumulus granulosa cells of patients with polycystic ovary syndrome. Fertil Steril. 2010;94(1):261–7.CrossRefPubMed Zhao SY, Qiao J, Chen YJ, Liu P, Li J, Yan J. Expression of growth differentiation factor-9 and bone morphogenetic protein-15 in oocytes and cumulus granulosa cells of patients with polycystic ovary syndrome. Fertil Steril. 2010;94(1):261–7.CrossRefPubMed
59.
go back to reference Xia Y, O’Shea T, Murison R, McFarlane JR. Concentrations of progesterone, follistatin, and follicle-stimulating hormone in peripheral plasma across the estrous cycle and pregnancy in merino ewes that are homozygous or noncarriers of the Booroola Gene1. Biol Reprod. 2003;69:1079–84.CrossRefPubMed Xia Y, O’Shea T, Murison R, McFarlane JR. Concentrations of progesterone, follistatin, and follicle-stimulating hormone in peripheral plasma across the estrous cycle and pregnancy in merino ewes that are homozygous or noncarriers of the Booroola Gene1. Biol Reprod. 2003;69:1079–84.CrossRefPubMed
60.
go back to reference Lambalk CB, De Koning CH, Braat DD. The endocrinology of dizygotic twinning in the human. Mol Cell Endocrinol. 1998;145(1–2):97–102.CrossRefPubMed Lambalk CB, De Koning CH, Braat DD. The endocrinology of dizygotic twinning in the human. Mol Cell Endocrinol. 1998;145(1–2):97–102.CrossRefPubMed
61.
go back to reference Inagaki K, Shimasaki S. Impaired production of BMP-15 and GDF-9 mature proteins derived from proproteins WITH mutations in the proregion. Mol Cell Endocrinol. 2010;328(1–2):1–7.CrossRefPubMedPubMedCentral Inagaki K, Shimasaki S. Impaired production of BMP-15 and GDF-9 mature proteins derived from proproteins WITH mutations in the proregion. Mol Cell Endocrinol. 2010;328(1–2):1–7.CrossRefPubMedPubMedCentral
62.
go back to reference Maheshwari A, Hamilton M, Bhattacharya S. Effect of female age on the diagnostic categories of infertility. Hum Reprod. 2008;23:538–42.CrossRefPubMed Maheshwari A, Hamilton M, Bhattacharya S. Effect of female age on the diagnostic categories of infertility. Hum Reprod. 2008;23:538–42.CrossRefPubMed
63.
go back to reference Li Y, Li RQ, Ou SB, Zhang NF, Ren L, Wei LN, Zhang QX, Yang DZ. Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reprod Biol Endocrinol. 2014;12:81.CrossRefPubMedPubMedCentral Li Y, Li RQ, Ou SB, Zhang NF, Ren L, Wei LN, Zhang QX, Yang DZ. Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reprod Biol Endocrinol. 2014;12:81.CrossRefPubMedPubMedCentral
Metadata
Title
Age-related expression of TGF beta family receptors in human cumulus oophorus cells
Authors
A. Ribeiro
C. Freitas
L. Matos
A. Gouveia
F. Gomes
J. L. Silva Carvalho
H. Almeida
Publication date
01-09-2017
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 9/2017
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-017-0930-6

Other articles of this Issue 9/2017

Journal of Assisted Reproduction and Genetics 9/2017 Go to the issue