Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
권호 표지
DOI QR코드

DOI QR Code

The potential role of granulosa cells in the maturation rate of immature human oocytes and embryo development: A co-culture study

  • Jahromi, Bahia Namavar (Infertility Research Center, Department of Obstetrics and Gynecology, Division of Reproductive Endocrinology and Infertility) ;
  • Mosallanezhad, Zahra (Student Research Committee, Department of Obstetrics and Gynecology, School of Medicine, Shiraz University of Medical Sciences) ;
  • Matloob, Najmeh (Infertility Research Center, Mother and Child Hospital) ;
  • Davari, Maryam (Infertility Research Center, Mother and Child Hospital) ;
  • Ghobadifar, Mohamed Amin (Zoonoses Research Center, Faculty of Medicine, Jahrom University of Medical Sciences)
  • Received : 2015.05.01
  • Accepted : 2015.08.25
  • Published : 2015.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: In order to increase the number of mature oocytes usable for intracytoplasmic sperm injection (ICSI), we aimed to investigate the effect of co-culturing granulosa cells (GCs) on human oocyte maturation in vitro, the fertilization rate, and embryo development. Methods: A total of 133 immature oocytes were retrieved and were randomly divided into two groups; oocytes that were cultured with GCs (group A) and oocytes that were cultured without GCs (group B). After in vitro maturation, only oocytes that displayed metaphase II (MII) underwent the ICSI procedure. The maturation and fertilization rates were analyzed, as well as the frequency of embryo development. Results: The mean age of the patients, their basal levels of follicle-stimulating hormone, and the number of oocytes recovered from the patients were all comparable between the two study groups. The number of oocytes that reached MII (mature oocytes) was 59 out of 70 (84.28%) in group A, compared to 41 out of 63 (65.07%) in group B (p=0.011). No significant difference between fertilization rates was found between the two study groups (p=0.702). The embryo development rate was higher in group A (33/59, 75%) than in group B (12/41, 42.85%; p=0.006). The proportion of highest-quality embryos and the blastocyst formation rate were significantly lower in group B than in group A (p=0.003 and p<0.001, respectively). Conclusion: The findings of the current study demonstrate that culturing immature human oocytes with GCs prior to ICSI improves the maturation rate and the likelihood of embryo development.

Keywords

References

  1. Chang EM, Song HS, Lee DR, Lee WS, Yoon TK. In vitro maturation of human oocytes: its role in infertility treatment and new possibilities. Clin Exp Reprod Med 2014;41:41-6. https://doi.org/10.5653/cerm.2014.41.2.41
  2. Pincus G, Enzmann EV. The comparative behavior of mammalian eggs in vivo and in vitro: I. the activation of ovarian eggs. J Exp Med 1935;62:665-75. https://doi.org/10.1084/jem.62.5.665
  3. Fukuda Y, Ichikawa M, Naito K, Toyoda Y. Birth of normal calves resulting from bovine oocytes matured, fertilized, and cultured with cumulus cells in vitro up to the blastocyst stage. Biol Reprod 1990;42:114-9. https://doi.org/10.1095/biolreprod42.1.114
  4. Cha KY, Koo JJ, Ko JJ, Choi DH, Han SY, Yoon TK. Pregnancy after in vitro fertilization of human follicular oocytes collected from nonstimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertil Steril 1991;55:109-13. https://doi.org/10.1016/S0015-0282(16)54068-0
  5. Trounson A, Wood C, Kausche A. In vitro maturation and the fertilization and developmental competence of oocytes recovered from untreated polycystic ovarian patients. Fertil Steril 1994;62: 353-62. https://doi.org/10.1016/S0015-0282(16)56891-5
  6. Guigon CJ, Cohen-Tannoudji M. Reconsidering the roles of female germ cells in ovarian development and folliculogenesis. Biol Aujourdhui 2011;205:223-33. https://doi.org/10.1051/jbio/2011022
  7. Sugiura K, Pendola FL, Eppig JJ. Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev Biol 2005;279:20-30. https://doi.org/10.1016/j.ydbio.2004.11.027
  8. Wigglesworth K, Lee KB, 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. Proc Natl Acad Sci U S A 2013;110:E3723-9. https://doi.org/10.1073/pnas.1314829110
  9. Su YQ, 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; 135:111-21.
  10. 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. https://doi.org/10.1095/biolreprod63.3.805
  11. Russell JB. Immature oocyte retrieval combined with in-vitro oocyte maturation. Hum Reprod 1998;13 Suppl 3:63-70. https://doi.org/10.1093/humrep/13.suppl_3.63
  12. Lainas TG, Sfontouris IA, Zorzovilis IZ, Petsas GK, Lainas GT, Alexopoulou E, et al. Flexible GnRH antagonist protocol versus GnRH agonist long protocol in patients with polycystic ovary syndrome treated for IVF: a prospective randomised controlled trial (RCT). Hum Reprod 2010;25:683-9. https://doi.org/10.1093/humrep/dep436
  13. Johnson JE, Higdon HL 3rd, Boone WR. Effect of human granulosa cell co-culture using standard culture media on the maturation and fertilization potential of immature human oocytes. Fertil Steril 2008;90:1674-9. https://doi.org/10.1016/j.fertnstert.2007.06.017
  14. Van Steirteghem AC, Liu J, Joris H, Nagy Z, Janssenswillen C, Tournaye H, et al. Higher success rate by intracytoplasmic sperm injection than by subzonal insemination: report of a second series of 300 consecutive treatment cycles. Hum Reprod 1993;8:1055-60. https://doi.org/10.1093/oxfordjournals.humrep.a138191
  15. Puissant F, Van Rysselberge M, Barlow P, Deweze J, Leroy F. Embryo scoring as a prognostic tool in IVF treatment. Hum Reprod 1987;2:705-8. https://doi.org/10.1093/oxfordjournals.humrep.a136618
  16. Reichman DE, Politch J, Ginsburg ES, Racowsky C. Extended in vitro maturation of immature oocytes from stimulated cycles: an analysis of fertilization potential, embryo development, and reproductive outcomes. J Assist Reprod Genet 2010;27:347-56. https://doi.org/10.1007/s10815-010-9416-5
  17. Mori T, Amano T, Shimizu H. Roles of gap junctional communication of cumulus cells in cytoplasmic maturation of porcine oocytes cultured in vitro. Biol Reprod 2000;62:913-9. https://doi.org/10.1095/biolreprod62.4.913
  18. Su YQ, Wu X, O'Brien MJ, Pendola FL, Denegre JN, Matzuk MM, et al. Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte-cumulus cell complex in mice: genetic evidence for an oocyte-granulosa cell regulatory loop. Dev Biol 2004;276:64-73. https://doi.org/10.1016/j.ydbio.2004.08.020
  19. Araujo VR, Gastal MO, Figueiredo JR, Gastal EL. In vitro culture of bovine preantral follicles: a review. Reprod Biol Endocrinol 2014; 12:78. https://doi.org/10.1186/1477-7827-12-78
  20. Goud PT, Goud AP, Qian C, Laverge H, Van der Elst J, De Sutter P, et al. In-vitro maturation of human germinal vesicle stage oocytes: role of cumulus cells and epidermal growth factor in the culture medium. Hum Reprod 1998;13:1638-44. https://doi.org/10.1093/humrep/13.6.1638
  21. Hwang JL, Lin YH, Tsai YL. In vitro maturation and fertilization of immature oocytes: a comparative study of fertilization techniques. J Assist Reprod Genet 2000;17:39-43. https://doi.org/10.1023/A:1009450014064
  22. Shu Y, Gebhardt J, Watt J, Lyon J, Dasig D, Behr B. Fertilization, embryo development, and clinical outcome of immature oocytes from stimulated intracytoplasmic sperm injection cycles. Fertil Steril 2007;87:1022-7. https://doi.org/10.1016/j.fertnstert.2006.08.110
  23. Strassburger D, Friedler S, Raziel A, Kasterstein E, Schachter M, Ron-El R. The outcome of ICSI of immature MI oocytes and rescued in vitro matured MII oocytes. Hum Reprod 2004;19:1587-90. https://doi.org/10.1093/humrep/deh236
  24. Choi BH, Bang JI, Jin JI, Kim SS, Jo HT, Deb GK, et al. Coculturing cumulus oocyte complexes with denuded oocytes alters zona pellucida ultrastructure in in vitro matured bovine oocytes. Theriogenology 2013;80:1117-23. https://doi.org/10.1016/j.theriogenology.2013.08.015
  25. Dey SR, Deb GK, Ha AN, Lee JI, Bang JI, Lee KL, et al. Coculturing denuded oocytes during the in vitro maturation of bovine cumulus oocyte complexes exerts a synergistic effect on embryo development. Theriogenology 2012;77:1064-77. https://doi.org/10.1016/j.theriogenology.2011.10.009
  26. Tao Y, Cao C, Zhang M, Fang F, Liu Y, Zhang Y, et al. Effects of cumulus cells on rabbit oocyte in vitro maturation. J Anim Physiol Anim Nutr (Berl) 2008;92:438-47. https://doi.org/10.1111/j.1439-0396.2007.00729.x
  27. Wongsrikeao P, Kaneshige Y, Ooki R, Taniguchi M, Agung B, Nii M, et al. Effect of the removal of cumulus cells on the nuclear maturation, fertilization and development of porcine oocytes. Reprod Domest Anim 2005;40:166-70. https://doi.org/10.1111/j.1439-0531.2005.00576.x
  28. Nyholt de Prada JK, Lee YS, Latham KE, Chaffin CL, VandeVoort CA. Role for cumulus cell-produced EGF-like ligands during primate oocyte maturation in vitro. Am J Physiol Endocrinol Metab 2009;296:E1049-58. https://doi.org/10.1152/ajpendo.90930.2008
  29. Downs SM, Mastropolo AM. Culture conditions affect meiotic regulation in cumulus cell-enclosed mouse oocytes. Mol Reprod Dev 1997;46:551-66. https://doi.org/10.1002/(SICI)1098-2795(199704)46:4<551::AID-MRD13>3.0.CO;2-Z
  30. Souza-Fabjan JM, Corbin E, Locatelli Y, Duffard N, Perreau C, Freitas VJ, et al. 306 effect of different in vitro maturation media on developmental potential of goat oocytes already found denuded at collection. Reprod Fertil Dev 2014;27:242.
  31. Cheng KW, Leung PC. The expression, regulation and signal transduction pathways of the mammalian gonadotropin-releasing hormone receptor. Can J Physiol Pharmacol 2000;78:1029-52. https://doi.org/10.1139/y00-096
  32. Salamone DF, Damiani P, Fissore RA, Robl JM, Duby RT. Biochemical and developmental evidence that ooplasmic maturation of prepubertal bovine oocytes is compromised. Biol Reprod 2001; 64:1761-8. https://doi.org/10.1095/biolreprod64.6.1761
  33. Cha KY, Chian RC. Maturation in vitro of immature human oocytes for clinical use. Hum Reprod Update 1998;4:103-20. https://doi.org/10.1093/humupd/4.2.103
  34. Ruddock NT, Wilson KJ, Cooney MA, Korfiatis NA, Tecirlioglu RT, French AJ. Analysis of imprinted messenger RNA expression during bovine preimplantation development. Biol Reprod 2004;70: 1131-5. https://doi.org/10.1095/biolreprod.103.022236
  35. Zhivkova R, Delimitreva S, Vatev I. Role of oocyte cytoplasmic factors in human IVF failure. Akush Ginekol (Sofiia) 2010;49:26-32.
  36. Rosenbusch BE, Schneider M. Separation of a pronucleus by premature cytokinesis: a mechanism for immediate diploidization of tripronuclear oocytes? Fertil Steril 2009;92:394.e5-8.
  37. Curnow EC, Ryan JP, Saunders DM, Hayes ES. In vitro developmental potential of macaque oocytes, derived from unstimulated ovaries, following maturation in the presence of glutathione ethyl ester. Hum Reprod 2010;25:2465-74. https://doi.org/10.1093/humrep/deq225
  38. Watson AJ. Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J Anim Sci 2007; 85(13 Suppl):E1-3. https://doi.org/10.2527/jas.2006-432
  39. Godard NM, Pukazhenthi BS, Wildt DE, Comizzoli P. Paracrine factors from cumulus-enclosed oocytes ensure the successful maturation and fertilization in vitro of denuded oocytes in the cat model. Fertil Steril 2009;91(5 Suppl):2051-60. https://doi.org/10.1016/j.fertnstert.2008.05.069
  40. Tanghe S, Van Soom A, Mehrzad J, Maes D, Duchateau L, de Kruif A. Cumulus contributions during bovine fertilization in vitro. Theriogenology 2003;60:135-49. https://doi.org/10.1016/S0093-691X(02)01360-2
  41. Zhang L, Jiang S, Wozniak PJ, Yang X, Godke RA. Cumulus cell function during bovine oocyte maturation, fertilization, and embryo development in vitro. Mol Reprod Dev 1995;40:338-44. https://doi.org/10.1002/mrd.1080400310

Cited by

  1. Clinical outcome of cycles with oocyte degeneration after intracytoplasmic sperm injection vol.63, pp.2, 2017, https://doi.org/10.1080/19396368.2016.1272648
  2. Role of granulosa cell mitogen-activated protein kinase 3/1 in gonadotropin-mediated meiotic resumption from diplotene arrest of mammalian oocytes vol.36, pp.1, 2015, https://doi.org/10.1080/08977194.2018.1475372
  3. Oocyte in vitro maturation: A sytematic review vol.15, pp.2, 2015, https://doi.org/10.4274/tjod.23911
  4. Granulosa secreted factors improve the developmental competence of cumulus oocyte complexes from small antral follicles in sheep vol.15, pp.3, 2020, https://doi.org/10.1371/journal.pone.0229043
  5. MicroRNA-135a Regulates VEGFC Expression and Promotes Luteinized Granulosa Cell Apoptosis in Polycystic Ovary Syndrome vol.27, pp.7, 2020, https://doi.org/10.1007/s43032-020-00155-0
  6. Theca cell‐conditioned medium added to in vitro maturation enhances embryo developmental competence of buffalo (Bubalus bubalis) oocytes after parthenogenic activation vol.55, pp.11, 2015, https://doi.org/10.1111/rda.13799
  7. Potential mechanism of lead poisoning to the growth and development of ovarian follicle vol.457, pp.None, 2015, https://doi.org/10.1016/j.tox.2021.152810
  8. Vitamin E regulates bovine granulosa cell apoptosis via NRF2‐mediated defence mechanism by activating PI3K/AKT and ERK1/2 signalling pathways vol.56, pp.8, 2015, https://doi.org/10.1111/rda.13950