Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 964614, 10 pages
http://dx.doi.org/10.1155/2014/964614
Research Article

Female Aging Alters Expression of Human Cumulus Cells Genes that Are Essential for Oocyte Quality

1UFR de Médecine, Université Montpellier 1, 34295 Montpellier, France
2CHU Montpellier, Institut pour la Médecine Régénérative et Biothérapies, Hôpital Saint-Eloi, INSERM U1040, 34295 Montpellier, France
3ART-PGD Department, CHU Montpellier, Hôpital Arnaud de Villeneuve, 34295 Montpellier, France
4Institute of Molecular Genetics of Montpellier, 34293 Montpellier, France

Received 2 July 2014; Revised 15 July 2014; Accepted 17 July 2014; Published 3 September 2014

Academic Editor: Calvin Yu-Chian Chen

Copyright © 2014 Tamadir Al-Edani et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. J. Faddy, R. G. Gosden, A. Gougeon, S. J. Richardson, and J. F. Nelson, “Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause,” Human Reproduction, vol. 7, no. 10, pp. 1342–1346, 1992. View at Google Scholar · View at Scopus
  2. C. Alviggi, P. Humaidan, C. M. Howles, D. Tredway, and S. G. Hillier, “Biological versus chronological ovarian age: implications for assisted reproductive technology,” Reproductive Biology and Endocrinology, vol. 7, article 101, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. A. J. Wilcox, C. R. Weinberg, and D. D. Baird, “Post-ovulatory ageing of the human oocyte and embryo failure,” Human Reproduction, vol. 13, no. 2, pp. 394–397, 1998. View at Publisher · View at Google Scholar · View at Scopus
  4. R. P. S. Jansen, “Germline passage of mitochondria: quantitative considerations and possible embryological sequelae,” Human Reproduction, vol. 15, supplement 2, pp. 112–128, 2000. View at Google Scholar · View at Scopus
  5. T. A. L. Brevini Gandolfi and F. Gandolfi, “The maternal legacy to the embryo: cytoplasmic components and their effects on early development,” Theriogenology, vol. 55, no. 6, pp. 1255–1276, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Agarwal, S. Gupta, and R. K. Sharma, “Role of oxidative stress in female reproduction,” Reproductive Biology and Endocrinology, vol. 3, article 28, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. U. Eichenlaub-Ritter, M. Wieczorek, S. Lüke, and T. Seidel, “Age related changes in mitochondrial function and new approaches to study redox regulation in mammalian oocytes in response to age or maturation conditions,” Mitochondrion, vol. 11, no. 5, pp. 783–796, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. M. L. Grøndahl, C. Y. Andersen, J. Bogstad, F. C. Nielsen, H. Meinertz, and R. Borup, “Gene expression profiles of single human mature oocytes in relation to age,” Human Reproduction, vol. 25, no. 4, pp. 957–968, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Fragouli, D. Wells, and J. D. A. Delhanty, “Chromosome abnormalities in the human oocyte,” Cytogenetic and Genome Research, vol. 133, no. 2–4, pp. 107–118, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. R. B. Gilchrist, M. Lane, and J. G. Thompson, “Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality,” Human Reproduction Update, vol. 14, no. 2, pp. 159–177, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. D. F. Albertini, C. M. H. Combelles, E. Benecchi, and M. J. Carabatsos, “Cellular basis for paracrine regulation of ovarian follicle development,” Reproduction, vol. 121, no. 5, pp. 647–653, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. D. L. Russell and R. L. Robker, “Molecular mechanisms of ovulation: co-ordination through the cumulus complex,” Human Reproduction Update, vol. 13, no. 3, pp. 289–312, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Assou, D. Haouzi, J. de Vos, and S. Hamamah, “Human cumulus cells as biomarkers for embryo and pregnancy outcomes,” Molecular Human Reproduction, vol. 16, no. 8, Article ID gaq032, pp. 531–538, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Assou, D. Haouzi, K. Mahmoud et al., “A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study,” Molecular Human Reproduction, vol. 14, no. 12, pp. 711–719, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Hamel, I. Dufort, C. Robert et al., “Identification of differentially expressed markers in human follicular cells associated with competent oocytes,” Human Reproduction, vol. 23, no. 5, pp. 1118–1127, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Assou, I. Boumela, D. Haouzi et al., “Dynamic changes in gene expression during human early embryo development: from fundamental aspects to clinical applications,” Human Reproduction Update, vol. 17, no. 2, Article ID dmq036, pp. 272–290, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. S. McReynolds, M. Dzieciatkowska, B. R. McCallie et al., “Impact of maternal aging on the molecular signature of human cumulus cells,” Fertility and Sterility, vol. 98, no. 6, pp. 1574.e5–1580.e5, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. M.-S. Lee, C.-H. Liu, T.-H. Lee et al., “Association of creatin kinase B and peroxiredoxin 2 expression with age and embryo quality in cumulus cells,” Journal of Assisted Reproduction and Genetics, vol. 27, no. 11, pp. 629–639, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Pacella, D. L. Zander-Fox, D. T. Armstrong, and M. Lane, “Women with reduced ovarian reserve or advanced maternal age have an altered follicular environment,” Fertility and Sterility, vol. 98, no. 4, pp. 986.e2–994.e2, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Assou, D. Haouzi, H. Dechaud, A. Gala, A. Ferrieres, and S. Hamamah, “Comparative gene expression profiling in human cumulus cells according to ovarian gonadotropin treatments,” BioMed Research International, vol. 2013, Article ID 354582, 13 pages, 2013. View at Publisher · View at Google Scholar
  21. S. Assou, T. Al-Edani, D. Haouzi et al., “MicroRNAs: new candidates for the regulation of the human cumulus-oocyte complex,” Human Reproduction, vol. 28, no. 11, pp. 3038–3049, 2013. View at Google Scholar
  22. C. C. Sprenger, S. R. Plymate, and M. J. Reed, “Aging-related alterations in the extracellular matrix modulate the microenvironment and influence tumor progression,” International Journal of Cancer, vol. 127, no. 12, pp. 2739–2748, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Martin, R. H. Jenkins, R. Bennagi et al., “Post-transcriptional regulation of transforming growth factor beta-1 by microRNA-744,” PLoS ONE, vol. 6, no. 10, Article ID e25044, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Goto, N. Suganuma, K. Takata et al., “Morphological analyses of interleukin-8 effects on rat ovarian follicles at ovulation and luteinization in vivo,” Cytokine, vol. 20, no. 4, pp. 168–173, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Vujisić, S. Ž. Lepej, I. Emedi, R. Bauman, A. Remenar, and M. K. Tiljak, “Ovarian follicular concentration of IL-12, IL-15, IL-18 and p40 subunit of IL-12 and IL-23,” Human Reproduction, vol. 21, no. 10, pp. 2650–2655, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Kõks, A. Velthut, A. Sarapik et al., “The differential transcriptome and ontology profiles of floating and cumulus granulosa cells in stimulated human antral follicles,” Molecular Human Reproduction, vol. 16, no. 4, Article ID gap103, pp. 229–240, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. H. Louhio, O. Hovatta, J. Sjöberg, and T. Tuuri, “The effects of insulin, and insulin-like growth factors I and II on human ovarian follicles in long-term culture,” Molecular Human Reproduction, vol. 6, no. 8, pp. 694–698, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Zhao, M. A. Taverne, G. C. van der Weijden, M. M. Bevers, and R. van den Hurk, “Insulin-like growth factor-I (IGF-I) stimulates the development of cultured rat pre-antral follicles,” Molecular Reproduction and Development, vol. 58, no. 3, pp. 287–296, 2001. View at Publisher · View at Google Scholar
  29. J. Kwintkiewicz and L. C. Giudice, “The interplay of insulin-like growth factors, gonadotropins, and endocrine disruptors in ovarian follicular development and function,” Seminars in Reproductive Medicine, vol. 27, no. 1, pp. 43–51, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. P. L. Lorenzo, M. J. Illera, J. C. Illera, and M. Illera, “Enhancement of cumulus expansion and nuclear maturation during bovine oocyte maturation in vitro by the addition of epidermal growth factor and insulin-like growth factor I,” Journal of Reproduction and Fertility, vol. 101, no. 3, pp. 697–701, 1994. View at Publisher · View at Google Scholar · View at Scopus
  31. S. M. Firth and R. C. Baxter, “Cellular actions of the insulin-like growth factor binding proteins,” Endocrine Reviews, vol. 23, no. 6, pp. 824–854, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. S.-H. Oh, W.-Y. Kim, O.-H. Lee et al., “Insulin-like growth factor binding protein-3 suppresses vascular endothelial growth factor expression and tumor angiogenesis in head and neck squamous cell carcinoma,” Cancer Science, vol. 103, no. 7, pp. 1259–1266, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. M. J. Moreno, M. Ball, M. Rukhlova et al., “IGFBP-4 anti-angiogenic and anti-tumorigenic effects are associated with anti-cathepsin B activity,” Neoplasia, vol. 15, no. 5, pp. 554–567, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Zhang, L. Lu, Y. Li et al., “IGF binding protein-6 expression in vascular endothelial cells is induced by hypoxia and plays a negative role in tumor angiogenesis,” International Journal of Cancer, vol. 130, no. 9, pp. 2003–2012, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. H. M. Fraser, “Regulation of the ovarian follicular vasculature,” Reproductive Biology and Endocrinology, vol. 4, article 18, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. C. W. Pugh and P. J. Ratcliffe, “Regulation of angiogenesis by hypoxia: role of the HIF system,” Nature Medicine, vol. 9, no. 6, pp. 677–684, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Neeman, R. Abramovitch, Y. S. Schiffenbauer, and C. Tempel, “Regulation of angiogenesis by hypoxic stress: from solid tumours to the ovarian follicle,” International Journal of Experimental Pathology, vol. 78, no. 2, pp. 57–70, 1997. View at Google Scholar · View at Scopus
  38. P. González-Muniesa, C. de Oliveira, F. P. de Heredia, M. P. Thompson, and P. Trayhurn, “Fatty acids and hypoxia stimulate the expression and secretion of the adipokine ANGPTL4 (angiopoietin-like protein 4/ fasting-induced adipose factor) by human adipocytes,” Journal of Nutrigenetics and Nutrigenomics, vol. 4, no. 3, pp. 146–153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. S.-H. Kim, Y.-Y. Park, S.-W. Kim, J.-S. Lee, D. Wang, and R. N. DuBois, “ANGPTL4 induction by prostaglandin E 2 under hypoxic conditions promotes colorectal cancer progression,” Cancer Research, vol. 71, no. 22, pp. 7010–7020, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. C. I. Friedman, D. R. Danforth, C. Herbosa-Encarnacion, L. Arbogast, B. M. Alak, and D. B. Seifer, “Follicular fluid vascular endothelial growth factor concentrations are elevated in women of advanced reproductive age undergoing ovulation induction,” Fertility and Sterility, vol. 68, no. 4, pp. 607–612, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Y. Fujii and M. Nakayama, “The measurements of RAGE, VEGF, and AGEs in the plasma and follicular fluid of reproductive women: the influence of aging,” Fertility and Sterility, vol. 94, no. 2, pp. 694–700, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. J. van Blerkom, M. Antczak, and R. Schrader, “The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics,” Human Reproduction, vol. 12, no. 5, pp. 1047–1055, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. E. Fragouli, V. Bianchi, P. Patrizio et al., “Transcriptomic profiling of human oocytes: association of meiotic aneuploidy and altered oocyte gene expression,” Molecular Human Reproduction, vol. 16, no. 8, pp. 570–582, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. Q. Li, D.-Q. Miao, P. Zhou et al., “Glucose metabolism in mouse cumulus cells prevents oocyte aging by maintaining both energy supply and the intracellular redox potential,” Biology of Reproduction, vol. 84, no. 6, pp. 1111–1118, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. D. Brisard, A. Desmarchais, J. L. Touze et al., “Alteration of energy metabolism gene expression in cumulus cells affects oocyte maturation via MOS-mitogen-activated protein kinase pathway in dairy cows with an unfavorable “Fertil-” haplotype of one female fertility quantitative trait locus,” Theriogenology, vol. 81, no. 4, pp. 599–612, 2014. View at Publisher · View at Google Scholar
  46. P. G. Knight and C. Glister, “Local roles of TGF-β superfamily members in the control of ovarian follicle development,” Animal Reproduction Science, vol. 78, no. 3-4, pp. 165–183, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. Z. Merhi, E. Buyuk, D. S. Berger et al., “Leptin suppresses anti-Mullerian hormone gene expression through the JAK2/STAT3 pathway in luteinized granulosa cells of women undergoing IVF,” Human Reproduction, vol. 28, no. 6, pp. 1661–1669, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. A. L. L. Durlinger, M. J. G. Gruijters, P. Kramer et al., “Anti-Müllerian hormone inhibits initiation of primordial follicle growth in the mouse ovary,” Endocrinology, vol. 143, no. 3, pp. 1076–1084, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. P. Lehmann, M. P. Velez, J. Saumet et al., “Anti-mullerian hormone (AMH): a reliable biomarker of oocyte quality in IVF,” Journal of Assisted Reproduction and Genetics, vol. 31, no. 4, pp. 493–498, 2014. View at Publisher · View at Google Scholar
  50. D. P. Bartel, “MicroRNAs: target recognition and regulatory functions,” Cell, vol. 136, no. 2, pp. 215–233, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. E. Huntzinger and E. Izaurralde, “Gene silencing by microRNAs: contributions of translational repression and mRNA decay,” Nature Reviews Genetics, vol. 12, no. 2, pp. 99–110, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. D. Xu and H. Tahara, “The role of exosomes and microRNAs in senescence and aging,” Advanced Drug Delivery Reviews, vol. 65, no. 3, pp. 368–375, 2013. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Diez-Fraile, T. Lammens, K. Tilleman et al., “Age-associated differential microRNA levels in human follicular fluid reveal pathways potentially determining fertility and success of in vitro fertilization,” Human Fertility, vol. 17, no. 2, pp. 90–98, 2014. View at Publisher · View at Google Scholar
  54. X. Yang, Y. Zhou, S. Peng et al., “Differentially expressed plasma microRNAs in premature ovarian failure patients and the potential regulatory function of mir-23a in granulosa cell apoptosis,” Reproduction, vol. 144, no. 2, pp. 235–244, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. J. C. da Silveira, D. N. R. Veeramachaneni, Q. A. Winger, E. M. Carnevale, and G. J. Bouma, “Cell-secreted vesicles in equine ovarian follicular fluid contain mirnas and proteins: a possible new form of cell communication within the ovarian follicle,” Biology of Reproduction, vol. 86, no. 3, article 71, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Z. Carletti, S. D. Fiedler, and L. K. Christenson, “MicroRNA 21 blocks apoptosis in mouse periovulatory granulosa cells,” Biology of Reproduction, vol. 83, no. 2, pp. 286–295, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. F. X. Donadeu, S. N. Schauer, and S. D. Sontakke, “Involvement of miRNAs in ovarian follicular and luteal development,” Journal of Endocrinology, vol. 215, no. 3, pp. 323–334, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. Y. C. Chan, J. Banerjee, S. Y. Choi, and C. K. Sen, “miR-210: the master hypoxamir,” Microcirculation, vol. 19, no. 3, pp. 215–223, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. L. Zeng, X. He, Y. Wang et al., “MicroRNA-210 overexpression induces angiogenesis and neurogenesis in the normal adult mouse brain,” Gene Therapy, vol. 21, no. 1, pp. 37–43, 2014. View at Google Scholar
  60. J. Y. Li, T. Y. Yong, M. Z. Michael, and J. M. Gleadle, “MicroRNAs: are they the missing link between hypoxia and pre-eclampsia?” Hypertens Pregnancy, vol. 33, no. 1, pp. 102–114, 2014. View at Google Scholar
  61. T. Bertero, S. Grosso, K. Robbe-Sermesant et al., ““Seed-milarity” confers to hsa-miR-210 and hsa-miR-147b similar functional activity,” PLoS ONE, vol. 7, no. 9, Article ID e44919, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. J. F. Mouillet, R. B. Donker, T. Mishima, T. Cronqvist, T. Chu, and Y. Sadovsky, “The unique expression and function of miR-424 in human placental trophoblasts,” Biology of Reproduction, vol. 89, no. 2, p. 25, 2013. View at Publisher · View at Google Scholar
  63. T. Ren, Y. Qing, N. Dai et al., “Apurinic/apyrimidinic endonuclease 1 induced upregulation of fibroblast growth factor 2 and its receptor 3 induces angiogenesis in human osteosarcoma cells,” Cancer Science, vol. 105, no. 2, pp. 186–194, 2014. View at Publisher · View at Google Scholar
  64. J. Kim, Y. Kang, Y. Kojima et al., “An endothelial apelin-FGF link mediated by miR-424 and miR-503 is disrupted in pulmonary arterial hypertension,” Nature Medicine, vol. 19, no. 1, pp. 74–82, 2013. View at Publisher · View at Google Scholar · View at Scopus