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Transporting cumulus complexes using novel meiotic arresting conditions permits maintenance of oocyte developmental competence

  • Gamete Biology
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Purpose

The aim of this study is to evaluate the effect of a novel bovine cumulus oocyte complex (COC) shipping media designed to arrest meiotic resumption during transport on meiotic arrest, as well as meiotic resumption, subsequent embryonic development, and embryo quality.

Methods

Bovine cumulus oocyte complexes were transported overnight from the collection facility to the laboratory. COCs were placed in control in vitro maturation (IVM) or in shipping arrest medium (SAM) containing multiple meiotic inhibitors, and then shipped to our laboratory. Upon arrival, meiotic status was assessed, control COCs were inseminated, and arrested COCs were matured and inseminated the next day. Embryonic development and quality were analyzed.

Results

When bovine COC arrived at the laboratory after overnight shipment (21 h) in SAM, the majority of oocytes remained at the GV stage (75.6 ± 2.9% GV). Arrested oocytes successfully resumed and completed meiosis during IVM after removal from SAM (96.8 ± 0.5% metaphase II compared to control 88.3 ± 5.0%). Moreover, the development of blastocysts per COC was not different from control (22.3 ± 2.4% for control and 18.7 ± 2.1% for SAM), nor was any difference detected in blastocyst quality as determined by cell number and allocation.

Conclusions

Our study demonstrates that a physiological system incorporating cyclic adenosine monophosphate and cyclic guanosine monophosphate modulators can be used to maintain meiotic arrest followed by successful nuclear maturation and pre-implantation embryo development equal to control IVM-derived embryos. Our results offer promising insights for the development of pre-IVM media that may improve oocyte developmental competence in vitro.

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References

  1. 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(5):665–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. ASRM. In vitro maturation: a committee opinion. Fertil Steril. 2013;99(3):663–6.

    Article  Google Scholar 

  3. Gremeau AS, Andreadis N, Fatum M, Craig J, Turner K, McVeigh E, et al. In vitro maturation or in vitro fertilization for women with polycystic ovaries? A case-control study of 194 treatment cycles. Fertil Steril. 2012;98(2):355–60.

    Article  PubMed  Google Scholar 

  4. Wrenzycki C, Stinshoff H. Maturation environment and impact on subsequent developmental competence of bovine oocytes. Reproduction in domestic animals = Zuchthygiene. 2013;48(Suppl 1):38–43.

    Article  PubMed  Google Scholar 

  5. Gilchrist RB, Thompson JG. Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology. 2007;67(1):6–15.

    Article  PubMed  Google Scholar 

  6. Eppig JJ, O’Brien MJ, Wigglesworth K, Nicholson A, Zhang W, King BA. Effect of in vitro maturation of mouse oocytes on the health and lifespan of adult offspring. Hum Reprod. 2009;24(4):922–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Gilchrist RB. Recent insights into oocyte-follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reprod Fertil Dev. 2011;23(1):23–31.

    Article  PubMed  Google Scholar 

  8. Edwards RG. Are minimal stimulation IVF and IVM set to replace routine IVF? Reprod BioMed Online. 2007;14(2):267–70.

    Article  CAS  PubMed  Google Scholar 

  9. Rose BI, Laky D, Miller B. The case for in vitro maturation lower cost and more patient friendly. J Reprod Med. 2014;59(11–12):571–8.

    PubMed  Google Scholar 

  10. Smitz JE, Thompson JG, Gilchrist RB. The promise of in vitro maturation in assisted reproduction and fertility preservation. Semin Reprod Med. 2011;29(1):24–37.

    Article  CAS  PubMed  Google Scholar 

  11. Walls M, Junk S, Ryan JP, Hart R. IVF versus ICSI for the fertilization of in-vitro matured human oocytes. Reprod BioMed Online. 2012;25(6):603–7.

    Article  CAS  PubMed  Google Scholar 

  12. Coticchio G, Dal Canto M, Mignini Renzini M, Guglielmo MC, Brambillasca F, Turchi D, et al. Oocyte maturation: gamete-somatic cells interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization. Hum Reprod Update. 2015;21(4):427–54.

    Article  PubMed  Google Scholar 

  13. Li R, Albertini DF. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol. 2013;14(3):141–52.

    Article  CAS  PubMed  Google Scholar 

  14. Albuz FK, Sasseville M, Lane M, Armstrong DT, Thompson JG, Gilchrist RB. Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum Reprod. 2010;25(12):2999–3011.

    Article  CAS  PubMed  Google Scholar 

  15. Downs SM, Schroeder AC, Eppig JJ. Developmental capacity of mouse oocytes following maintenance of meiotic arrest in vitro. Gamete research. 1986;15(4):305–16.

    Article  CAS  Google Scholar 

  16. Lonergan P, Khatir H, Carolan C, Mermillod P. Bovine blastocyst production in vitro after inhibition of oocyte meiotic resumption for 24 h. J Reprod Fertil. 1997;109(2):355–65.

    Article  CAS  PubMed  Google Scholar 

  17. Luciano AM, Pocar P, Milanesi E, Modina S, Rieger D, Lauria A, et al. Effect of different levels of intracellular cAMP on the in vitro maturation of cattle oocytes and their subsequent development following in vitro fertilization. Mol Reprod Dev. 1999;54(1):86–91.

    Article  CAS  PubMed  Google Scholar 

  18. Mermillod P, Tomanek M, Marchal R, Meijer L. High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 hours in culture by specific inhibition of MPF kinase activity. Mol Reprod Dev. 2000;55(1):89–95.

    Article  CAS  PubMed  Google Scholar 

  19. Nogueira D, Ron-El R, Friedler S, Schachter M, Raziel A, Cortvrindt R, et al. Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development. Biol Reprod. 2006;74(1):177–84.

    Article  CAS  PubMed  Google Scholar 

  20. Richani D, Wang X, Zeng HT, Smitz J, Thompson JG, Gilchrist RB. Pre-maturation with cAMP modulators in conjunction with EGF-like peptides during in vitro maturation enhances mouse oocyte developmental competence. Mol Reprod Dev. 2014;81(5):422–35.

    Article  CAS  PubMed  Google Scholar 

  21. Sirard MA, First NL. In vitro inhibition of oocyte nuclear maturation in the bovine. Biol Reprod. 1988;39(2):229–34.

    Article  CAS  PubMed  Google Scholar 

  22. Vanhoutte L, De Sutter P, Nogueira D, Gerris J, Dhont M, Van der Elst J. Nuclear and cytoplasmic maturation of in vitro matured human oocytes after temporary nuclear arrest by phosphodiesterase 3-inhibitor. Hum Reprod. 2007;22(5):1239–46.

    Article  CAS  PubMed  Google Scholar 

  23. Wu GM, Sun QY, Mao J, Lai L, McCauley TC, Park KW, et al. High developmental competence of pig oocytes after meiotic inhibition with a specific M-phase promoting factor kinase inhibitor, butyrolactone I. Biol Reprod. 2002;67(1):170–7.

    Article  CAS  PubMed  Google Scholar 

  24. Zeng HT, Richani D, Sutton-McDowall ML, Ren Z, Smitz JE, Stokes Y, et al. Prematuration with cyclic adenosine monophosphate modulators alters cumulus cell and oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocytes. Biol Reprod. 2014;91(2):47.

    Article  PubMed  Google Scholar 

  25. Guimaraes AL, Pereira SA, Leme LO, Dode MA. Evaluation of the simulated physiological oocyte maturation system for improving bovine in vitro embryo production. Theriogenology. 2015;83(1):52–7.

    Article  CAS  PubMed  Google Scholar 

  26. Gilchrist RB, Zeng HT, Wang X, Richani D, Smitz J, Thompson JG. “Re-evaluation and evolution of the simulated physiological oocyte maturation (SPOM) system.” Theriogenology. 2015;84(4):656–7.

  27. Li HJ, Sutton-McDowall ML, Wang X, Sugimura S, Thompson JG, Gilchrist RB. “Extending prematuration with cAMP modulators enhances the cumulus contribution to oocyte antioxidant defence and oocyte quality via gap junctions.” Hum Reprod. 2016;31(4):810-21.

  28. Campen KA, Clark ZL, Olds MA, McNatty KP, Pitman JL. The in-vitro effects of cAMP and cGMP modulators on inter-cellular dye transfer and gene expression levels in rat cumulus cell-oocyte complexes. Mol Cell Endocrinol. 2015;420:46–56.

    Article  PubMed  Google Scholar 

  29. Zhang J, Wei Q, Cai J, Zhao X, Ma B. Effect of C-type natriuretic peptide on maturation and developmental competence of goat oocytes matured in vitro. PLoS One. 2015;10(7):e0132318.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Zhang M, Su YQ, Sugiura K, Wigglesworth K, Xia G, Eppig JJ. Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro. Endocrinology. 2011;152(11):4377–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Franciosi F, Coticchio G, Lodde V, Tessaro I, Modina SC, Fadini R, et al. Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biol Reprod. 2014;91(3):61.

    Article  PubMed  Google Scholar 

  32. Sugimura S, Ritter LJ, Sutton-McDowall ML, Mottershead DG, Thompson JG, Gilchrist RB. Amphiregulin co-operates with bone morphogenetic protein 15 to increase bovine oocyte developmental competence: effects on gap junction-mediated metabolite supply. Mol Hum Reprod. 2014;20(6):499–513.

    Article  CAS  PubMed  Google Scholar 

  33. Winterhager E, Kidder GM. Gap junction connexins in female reproductive organs: implications for women’s reproductive health. Hum Reprod Update. 2015;21(3):340–52.

    Article  PubMed  Google Scholar 

  34. Downs SM, Coleman DL, Ward-Bailey PF, Eppig JJ. Hypoxanthine is the principal inhibitor of murine oocyte maturation in a low molecular weight fraction of porcine follicular fluid. Proc Natl Acad Sci U S A. 1985;82(2):454–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Eppig JJ, Ward-Bailey PF, Coleman DL. Hypoxanthine and adenosine in murine ovarian follicular fluid: concentrations and activity in maintaining oocyte meiotic arrest. Biol Reprod. 1985;33(5):1041–9.

    Article  CAS  PubMed  Google Scholar 

  36. Laforest MF, Pouliot E, Gueguen L, Richard FJ. Fundamental significance of specific phosphodiesterases in the control of spontaneous meiotic resumption in porcine oocytes. Mol Reprod Dev. 2005;70(3):361–72.

    Article  CAS  PubMed  Google Scholar 

  37. Bakhtari A, Ross PJ. DPPA3 prevents cytosine hydroxymethylation of the maternal pronucleus and is required for normal development in bovine embryos. Epigenetics. 2014;9(9):1271–9.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Funahashi H, Cantley TC, Day BN. Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization. Biol Reprod. 1997;57(1):49–53.

    Article  CAS  PubMed  Google Scholar 

  39. Luciano AM, Modina S, Vassena R, Milanesi E, Lauria A, Gandolfi F. Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte-cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol Reprod. 2004;70(2):465–72.

    Article  CAS  PubMed  Google Scholar 

  40. Nogueira D, Albano C, Adriaenssens T, Cortvrindt R, Bourgain C, Devroey P, et al. Human oocytes reversibly arrested in prophase I by phosphodiesterase type 3 inhibitor in vitro. Biol Reprod. 2003a;69(3):1042–52.

    Article  CAS  PubMed  Google Scholar 

  41. Nogueira D, Cortvrindt R, De Matos DG, Vanhoutte L, Smitz J. Effect of phosphodiesterase type 3 inhibitor on developmental competence of immature mouse oocytes in vitro. Biol Reprod. 2003b;69(6):2045–52.

    Article  CAS  PubMed  Google Scholar 

  42. Shu YM, Zeng HT, Ren Z, Zhuang GL, Liang XY, Shen HW, et al. Effects of cilostamide and forskolin on the meiotic resumption and embryonic development of immature human oocytes. Hum Reprod. 2008;23(3):504–13.

    Article  CAS  PubMed  Google Scholar 

  43. Thomas RE, Armstrong DT, Gilchrist RB. Bovine cumulus cell-oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosophate levels. Biol Reprod. 2004a;70(3):548–56.

    Article  CAS  PubMed  Google Scholar 

  44. Thomas RE, Thompson JG, Armstrong DT, Gilchrist RB. Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biol Reprod. 2004b;71(4):1142–9.

    Article  CAS  PubMed  Google Scholar 

  45. Vanhoutte L, Nogueira D, De Sutter P. Prematuration of human denuded oocytes in a three-dimensional co-culture system: effects on meiosis progression and developmental competence. Hum Reprod. 2009a;24(3):658–69.

    Article  CAS  PubMed  Google Scholar 

  46. Vanhoutte L, Nogueira D, Dumortier F, De Sutter P. Assessment of a new in vitro maturation system for mouse and human cumulus-enclosed oocytes: three-dimensional prematuration culture in the presence of a phosphodiesterase 3-inhibitor. Hum Reprod. 2009b;24(8):1946–59.

    Article  CAS  PubMed  Google Scholar 

  47. Zeng HT, Ren Z, Guzman L, Wang X, Sutton-McDowall ML, Ritter LJ, et al. Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence. Hum Reprod. 2013;28(6):1536–45.

    Article  CAS  PubMed  Google Scholar 

  48. Kawamura K, Cheng Y, Kawamura N, Takae S, Okada A, Kawagoe Y, et al. Pre-ovulatory LH/hCG surge decreases C-type natriuretic peptide secretion by ovarian granulosa cells to promote meiotic resumption of pre-ovulatory oocytes. Hum Reprod. 2011;26(11):3094–101.

    Article  CAS  PubMed  Google Scholar 

  49. Kiyosu C, Tsuji T, Yamada K, Kajita S, Kunieda T. NPPC/NPR2 signaling is essential for oocyte meiotic arrest and cumulus oophorus formation during follicular development in the mouse ovary. Reproduction. 2012;144(2):187–93.

    Article  CAS  PubMed  Google Scholar 

  50. Robinson JW, Zhang M, Shuhaibar LC, Norris RP, Geerts A, Wunder F, et al. Luteinizing hormone reduces the activity of the NPR2 guanylyl cyclase in mouse ovarian follicles, contributing to the cyclic GMP decrease that promotes resumption of meiosis in oocytes. Dev Biol. 2012;366(2):308–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Santiquet N, Papillon-Dion E, Djender N, Guillemette C, Richard FJ. New elements in the C-type natriuretic peptide signaling pathway inhibiting swine in vitro oocyte meiotic resumption. Biol Reprod. 2014;91(1):16.

    Article  PubMed  Google Scholar 

  52. Zhang M, Su YQ, Sugiura K, Xia G, Eppig JJ. Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science. 2010;330(6002):366–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Cho WK, Stern S, Biggers JD. Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J Exp Zool. 1974;187(3):383–6.

    Article  CAS  PubMed  Google Scholar 

  54. Dekel N, Beers WH. Rat oocyte maturation in vitro: relief of cyclic AMP inhibition by gonadotropins. Proc Natl Acad Sci U S A. 1978;75(9):4369–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Schultz RM, Montgomery RR, Belanoff JR. Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev Biol. 1983;97(2):264–73.

    Article  CAS  PubMed  Google Scholar 

  56. Labrecque R, Lodde V, Dieci C, Tessaro I, Luciano AM, Sirard MA. Chromatin remodelling and histone m RNA accumulation in bovine germinal vesicle oocytes. Mol Reprod Dev. 2015;82(6):450–62.

    Article  CAS  PubMed  Google Scholar 

  57. Lodde V, Franciosi F, Tessaro I, Modina SC, Luciano AM. Role of gap junction-mediated communications in regulating large-scale chromatin configuration remodeling and embryonic developmental competence acquisition in fully grown bovine oocyte. J Assist Reprod Genet. 2013;30(9):1219–26.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Koyama K, Kang SS, Huang W, Yanagawa Y, Takahashi Y, Nagano M. Aging-related changes in in vitro-matured bovine oocytes: oxidative stress, mitochondrial activity and ATP content after nuclear maturation. J Reprod Dev. 2014;60(2):136–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Nicolas W. Santiquet.

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Santiquet, N.W., Herrick, J.R., Giraldo, A. et al. Transporting cumulus complexes using novel meiotic arresting conditions permits maintenance of oocyte developmental competence. J Assist Reprod Genet 34, 1079–1086 (2017). https://doi.org/10.1007/s10815-017-0958-7

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  • DOI: https://doi.org/10.1007/s10815-017-0958-7

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