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The effect of human cumulus cells on the maturation and developmental potential of immature oocytes in ICSI cycles

  • ASSISTED REPRODUCTION TECHNOLOGIES
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Abstract

Purpose

To investigate the effect of human cumulus cells on the maturation and developmental potential of immature oocytes in ICSI cycles.

Methods

Immature oocytes were randomly divided into two groups: the cumulus-denuded oocyte group (group A) and the cumulus-intact oocyte group (group B). Only oocytes that reached metaphase II (MII) stage after in vitro maturation were used in the ICSI procedure. In vivo mature sibling MII oocytes served as the control group. Maturation rate, fertilization rate, embryo quality and developmental potential were examined.

Results

There was no significant difference in maturation rate between group A (68.16%) and group B (70.49%; P > 0.05). The total fertilization rate among the three groups was comparable (P > 0.05), while the zygotes with two pronuclei in group A (74.59%) or group B (75.97%) were significantly lower than those in control group (84.29%; P < 0.05). The available embryo rate in group A (11.49%) was markedly lower than that in group B (27.66%; P < 0.05), and both of them were significantly lower than that in control group (62.38%; P < 0.05). The proportion of ≥6-cell embryos in group B (45.74%) was notably higher than in group A (26.44%; P < 0.05), and both were markedly lower than in control group (65.92%; P < 0.05). The proportion of embryos with <10% fragmentation in group A (13.79%) was significantly lower than in group B (29.79%; P < 0.05), and both were notably lower than in control group (42.98%; P < 0.05).

Conclusions

The presence of cumulus cells surrounding the immature oocytes during IVM before ICSI had no influence on nuclear maturation and fertilization, but leads to better subsequent embryonic development. This is perhaps mediated by an improvement in cytoplasmic maturation.

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References

  1. Balakier H, Sojecki A, Motamedi G, Librach C. Time-dependent capability of human oocytes for activation and pronuclear formation during metaphase II arrest. Hum Reprod. 2004;19:982–7 (Oxford, England).

    Article  PubMed  Google Scholar 

  2. Cha KY, Chian RC. Maturation in vitro of immature human oocytes for clinical use. Hum Reprod Update. 1998;4:103–20.

    Article  CAS  PubMed  Google Scholar 

  3. Cha KY, Chung HM, Lee DR, Kwon H, Chung MK, Park LS, Choi DH, Yoon TK. Obstetric outcome of patients with polycystic ovary syndrome treated by in vitro maturation and in vitro fertilization-embryo transfer. Fertil Steril. 2005;83:1461–5.

    Article  PubMed  Google Scholar 

  4. Chen SU, Chen HF, Lien YR, Ho HN, Chang HC, Yang YS. Schedule to inject in vitro matured oocytes may increase pregnancy after intracytoplasmic sperm injection. Arch Androl. 2000;44:197–205.

    Article  CAS  PubMed  Google Scholar 

  5. 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.

    Article  CAS  PubMed  Google Scholar 

  6. Combelles CM, Cekleniak NA, Racowsky C, Albertini DF. Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Hum Reprod. 2002;17:1006–16 (Oxford, England).

    Article  CAS  PubMed  Google Scholar 

  7. 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 (Oxford, England).

    Article  CAS  PubMed  Google Scholar 

  8. De Sousa PA, Caveney A, Westhusin ME, Watson AJ. Temporal patterns of embryonic gene expression and their dependence on oogenetic factors. Theriogenology. 1998;49:115–28.

    Article  PubMed  Google Scholar 

  9. De Vos A, Van de Velde H, Joris H, Van Steirteghem A. In-vitro matured metaphase-I oocytes have a lower fertilization rate but similar embryo quality as mature metaphase-II oocytes after intracytoplasmic sperm injection. Hum Reprod. 1999;14:1859–63 (Oxford, England).

    Article  PubMed  Google Scholar 

  10. Downs SM, Mastropolo AM. Culture conditions affect meiotic regulation in cumulus cell-enclosed mouse oocytes. Mol Reprod Dev. 1997;46:551–66.

    Article  CAS  PubMed  Google Scholar 

  11. 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;91:2051–60.

    Article  CAS  PubMed  Google Scholar 

  12. Goud PT, Goud AP, Qian C, Laverge H, Van der Elst J, De Sutter P, Dhont M. 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 (Oxford, England).

    Article  CAS  PubMed  Google Scholar 

  13. Grossmann M, Calafell JM, Brandy N, Vanrell JA, Rubio C, Pellicer A, Egozcue J, Vidal F, Santalo J. Origin of tripronucleate zygotes after intracytoplasmic sperm injection. Hum Reprod. 1997;12:2762–5 (Oxford, England).

    Article  CAS  PubMed  Google Scholar 

  14. Hassan HA. Cumulus cell contribution to cytoplasmic maturation and oocyte developmental competence in vitro. J Assist Reprod Genet. 2001;18:539–43.

    Article  CAS  PubMed  Google Scholar 

  15. Isachenko E, Rahimi G, Isachenko V, Nawroth F. In-vitro maturation of germinal-vesicle oocytes and cryopreservation in metaphase I/II: a possible additional option to preserve fertility during ovarian tissue cryopreservation. Reprod Biomed Online. 2004;8:553–7.

    Article  PubMed  Google Scholar 

  16. Johnson JE, Higdon 3rd HL, 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.

    Article  PubMed  Google Scholar 

  17. Kim BK, Lee SC, Kim KJ, Han CH, Kim JH. In vitro maturation, fertilization, and development of human germinal vesicle oocytes collected from stimulated cycles. Fertil Steril. 2000;74:1153–8.

    Article  CAS  PubMed  Google Scholar 

  18. Kito S, Bavister B. Maturation of hamster oocytes under chemically defined conditions and sperm penetration through the zona pellucida. Zygote. 1996;4:199–210 (Cambridge, England).

    Article  CAS  PubMed  Google Scholar 

  19. Marchal R, Vigneron C, Perreau C, Bali-Papp A, Mermillod P. Effect of follicular size on meiotic and developmental competence of porcine oocytes. Theriogenology. 2002;57:1523–32.

    Article  CAS  PubMed  Google Scholar 

  20. Metallinou C, Asimakopoulos B, Schroer A, Nikolettos N. Gonadotropin-releasing hormone in the ovary. Reprod Sci. 2007;14:737–49 (Thousand Oaks, Calif).

    Article  CAS  PubMed  Google Scholar 

  21. Mikkelsen AL. Strategies in human in-vitro maturation and their clinical outcome. Reprod Biomed Online. 2005;10:593–9.

    Article  PubMed  Google Scholar 

  22. 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.

    Article  CAS  PubMed  Google Scholar 

  23. Nagashima H, Grupen CG, Ashman RJ, Nottle MB. Developmental competence of in vivo and in vitro matured porcine oocytes after subzonal sperm injection. Mol Reprod Dev. 1996;45:359–63.

    Article  CAS  PubMed  Google Scholar 

  24. 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. 2009;296:E1049–58.

    Article  CAS  Google Scholar 

  25. Prins GS, Wagner C, Weidel L, Gianfortoni J, Marut EL, Scommegna A. Gonadotropins augment maturation and fertilization of human immature oocytes cultured in vitro. Fertil Steril. 1987;47:1035–7.

    CAS  PubMed  Google Scholar 

  26. 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 (Oxford, England).

    CAS  PubMed  Google Scholar 

  27. 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.

    Article  PubMed  Google Scholar 

  28. Rosenbusch BE, Schneider M. Separation of a pronucleus by premature cytokinesis: a mechanism for immediate diploidization of tripronuclear oocytes? Fertil Steril. 2009;92(394):e395–8.

    Google Scholar 

  29. Russell JB. Immature oocyte retrieval combined with in-vitro oocyte maturation. Human reproduction (Oxford, England). 1998;13 Suppl 3, 63–70; discussion 71–65.

  30. 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.

    Article  CAS  PubMed  Google Scholar 

  31. Sasseville M, Gagnon MC, Guillemette C, Sullivan R, Gilchrist RB, Richard FJ. Regulation of gap junctions in porcine cumulus-oocyte complexes: contributions of granulosa cell contact, gonadotropins, and lipid rafts. Mol Endocrinol. 2009;23:700–10 (Baltimore, Md).

    Article  CAS  PubMed  Google Scholar 

  32. 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.

    Article  PubMed  Google Scholar 

  33. Smitz J, Cortvrindt R. Oocyte in-vitro maturation and follicle culture: current clinical achievements and future directions. Hum Reprod. 1999;14 Suppl 1:145–61 (Oxford, England).

    PubMed  Google Scholar 

  34. 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 (Oxford, England).

    Article  CAS  PubMed  Google Scholar 

  35. Strassburger D, Goldstein A, Friedler S, Raziel A, Kasterstein E, Mashevich M, Schachter M, Ron-El R, Reish O. The cytogenetic constitution of embryos derived from immature (metaphase I) oocytes obtained after ovarian hyperstimulation. Fertil Steril. 2010;94:971–8.

    Article  PubMed  Google Scholar 

  36. 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.

    Article  PubMed  Google Scholar 

  37. Tao Y, Cao C, Zhang M, Fang F, Liu Y, Zhang Y, Ding J, Zhang X. Effects of cumulus cells on rabbit oocyte in vitro maturation. J Anim Physiol Anim Nutr. 2008;92:438–47.

    Article  CAS  Google Scholar 

  38. Van de Velde H, De Vos A, Joris H, Nagy ZP, Van Steirteghem AC. Effect of timing of oocyte denudation and micro-injection on survival, fertilization and embryo quality after intracytoplasmic sperm injection. Hum Reprod. 1998;13:3160–4 (Oxford, England).

    Article  PubMed  Google Scholar 

  39. Van Steirteghem AC, Liu J, Joris H, Nagy Z, Janssenswillen C, Tournaye H, Derde MP, Van Assche E, Devroey P. 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 (Oxford, England).

    PubMed  Google Scholar 

  40. Vanderhyden BC, Armstrong DT. Role of cumulus cells and serum on the in vitro maturation, fertilization, and subsequent development of rat oocytes. Biol Reprod. 1989;40:720–8.

    Article  CAS  PubMed  Google Scholar 

  41. Vanhoutte L, De Sutter P, Van der Elst J, Dhont M. Clinical benefit of metaphase I oocytes. Reprod Biol Endocrinol. 2005;3:71.

    Article  PubMed  Google Scholar 

  42. Watson AJ. Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J Anim Sci. 2007;85:E1–3.

    Article  CAS  PubMed  Google Scholar 

  43. Wongsrikeao P, Kaneshige Y, Ooki R, Taniguchi M, Agung B, Nii M, Otoi T. Effect of the removal of cumulus cells on the nuclear maturation, fertilization and development of porcine oocytes. Reprod Domest Anim=Zuchthygiene. 2005;40:166–70.

    Article  CAS  Google Scholar 

  44. 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.

    Article  CAS  PubMed  Google Scholar 

  45. Zhivkova R, Delimitreva S, Vatev I. Role of oocyte cytoplasmic factors in human IVF failure. Akush Ginekol. 2010;49:26–32.

    CAS  Google Scholar 

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Acknowledgements

This work was supported by grants from the Natural Science Foundation of Shanghai Science and Technology Commission (No.11ZR1422700), the Science Foundation of Shanghai Municipal Health Bureau (No.2010266), the Science and Technology Foundation of Shanghai Jiao Tong University (No.YZ1041), the Science and Technology Commission of Shanghai Municipality (10DZ2270600), Shanghai Leading Academic Discipline Project (S30201) and Shanghai Basic Research Project (09DJ1400400).

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Correspondence to Yun Feng or Chen Xu.

Additional information

Capsule Cytoplasmic but not nuclear maturation is improved when IVM and ICSI are carried out with cumulus cells attached to human oocytes.

Aijun Zhang and Bufang Xu contributed equally to this work.

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Zhang, A., Xu, B., Sun, Y. et al. The effect of human cumulus cells on the maturation and developmental potential of immature oocytes in ICSI cycles. J Assist Reprod Genet 29, 313–319 (2012). https://doi.org/10.1007/s10815-012-9712-3

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  • DOI: https://doi.org/10.1007/s10815-012-9712-3

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