Current perspectives on in vitro maturation and its effects on oocyte genetic and epigenetic profiles

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Abstract

In vitro maturation (IVM), the maturation in culture of immature oocytes, has been used in clinic for more than 20 years. Although IVM has the specific advantages of low cost and minor side effects over controlled ovarian stimulation, the prevalence of IVM is less than 1% of routine in vitro fertilization and embryo transfer techniques in many reproductive centers. In this review, we searched the MEDLINE database for all full texts and/or abstract articles published in English with content related to oocyte IVM mainly between 2000 and 2016. Many different aspects of the IVM method may influence oocyte potential, including priming, gonadotrophin, growth factors, and culture times. The culture conditions of IVM result in alterations in the oocyte or cumulus cell transcriptome that are not observed under in vivo culture conditions. Additionally, epigenetic modifications, such as DNA methylation or acetylation, are also different between in vitro and in vivo cultured oocytes. In sum, current IVM technique is still not popular and requires more systematic and intensive research to improve its effects and applications. This review will help point our problems, supply evidence or clues for future improving IVM technique, thus assist patients for fertility treatment or preservation as an additional option.

Keywords

in vitro maturation oocyte fertility genetics epigenetics 

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Notes

Acknowledgments

This wok was supported by the National Natural Science Foundation of China (81300456) and the Joint Research Fund for Overseas Natural Science of China (31429004).

References

  1. Anckaert, E., De Rycke, M., and Smitz, J. (2013). Culture of oocytes and risk of imprinting defects. Hum Reprod Update 19, 52–66.PubMedCrossRefGoogle Scholar
  2. Anderson, R.A., Bayne, R.A.L., Gardner, J., and De Sousa, P.A. (2010). Brain-derived neurotrophic factor is a regulator of human oocyte maturation and early embryo development. Fertil Steril 93, 1394–1406.PubMedCrossRefGoogle Scholar
  3. Appeltant, R., Beek, J., Vandenberghe, L., Maes, D., and Van Soom, A. (2015). Increasing the cAMP concentration during in vitro maturation of pig oocytes improves cumulus maturation and subsequent fertilization in vitro. Theriogenology 83, 344–352.PubMedCrossRefGoogle Scholar
  4. Bagg, M.A., Nottle, M.B., Grupen, C.G., and Armstrong, D.T. (2006). Effect of dibutyryl cAMP on the cAMP content, meiotic progression, and developmental potential of in vitro matured pre-pubertal and adult pig oocytes. Mol Reprod Dev 73, 1326–1332.PubMedCrossRefGoogle Scholar
  5. Baker, J., Liu, J.P., Robertson, E.J., and Efstratiadis, A. (1993). Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75, 73–82.PubMedCrossRefGoogle Scholar
  6. Bavister, B.D. (1995). Culture of preimplantation embryos: facts and artifacts. Hum Reprod Update 1, 91–148.PubMedCrossRefGoogle Scholar
  7. Beker, A.R.C.L., Colenbrander, B., and Bevers, M.M. (2002). Effect of 17β-estradiol on the in vitro maturation of bovine oocytes. Theriogenology 58, 1663–1673.PubMedCrossRefGoogle Scholar
  8. Beker-van Woudenberg, A.R., van Tol, H.T.A., Roelen, B.A.J., Colenbrander, B., and Bevers, M.M. (2004). Estradiol and its membraneimpermeable conjugate (estradiol-bovine serum albumin) during in vitro maturation of bovine oocytes: effects on nuclear and cytoplasmic maturation, cytoskeleton, and embryo quality. Biol Reprod 70, 1465–1474.PubMedCrossRefGoogle Scholar
  9. Ben-Ami, I., Komsky, A., Bern, O., Kasterstein, E., Komarovsky, D., and Ron-El, R. (2011). in vitro maturation of human germinal vesicle-stage oocytes: role of epidermal growth factor-like growth factors in the culture medium. Hum Reprod 26, 76–81.PubMedCrossRefGoogle Scholar
  10. Benkhalifa, M., Demirol, A., Ménézo, Y., Balashova, E., Abduljalil, A., Abbas, S., Giakoumakis, I., and Gurgan, T. (2009). Natural cycle IVF and oocyte in-vitro maturation in polycystic ovary syndrome: a collaborative prospective study. Reprod Biomed Online 18, 29–36.PubMedCrossRefGoogle Scholar
  11. Borghol, N., Lornage, J., Blachère, T., Sophie Garret, A., and Lefèvre, A. (2006). Epigenetic status of the H19 locus in human oocytes following in vitro maturation. Genomics 87, 417–426.PubMedCrossRefGoogle Scholar
  12. Bormann, C.L., Ongeri, E.M., and Krisher, R.L. (2003). The effect of vitamins during maturation of caprine oocytes on subsequent developmental potential in vitro. Theriogenology 59, 1373–1380.PubMedCrossRefGoogle Scholar
  13. Cha, K.Y., Koo, J.J., Ko, J.J., Choi, D.H., Han, S.Y., and Yoon, T.K. (1991). 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 55, 109–113.PubMedCrossRefGoogle Scholar
  14. Chian, R.C., Uzelac, P.S., and Nargund, G. (2004). in-vitro maturation of immature oocytes for infertile women with PCOS. Reprod Biomed Online 8, 547–552.PubMedCrossRefGoogle Scholar
  15. Chian, R.C., Uzelac, P.S., and Nargund, G. (2013). in vitro maturation of human immature oocytes for fertility preservation. Fertil Steril 99, 1-173–1181.CrossRefGoogle Scholar
  16. Chian, R.C., and Cao, Y.X. (2014). in vitro maturation of immature human oocytes for clinical application. Methods Mol Biol 1154, 271–288.PubMedCrossRefGoogle Scholar
  17. Choavaratana, R., Thanaboonyawat, I., Laokirkkiat, P., Prechapanich, J., Suksompong, S., Mekemaharn, O., and Petyim, S. (2015). Outcomes of follicle-stimulating hormone priming and nonpriming in in vitro maturation of oocytes in infertile women with polycystic ovarian syndrome: a single-blinded randomized study. Gynecol Obstet Invest 79, 153–159.PubMedCrossRefGoogle Scholar
  18. Coticchio, G., Dal Canto, M., Fadini, R., Mignini, R.M., Guglielmo, M.C., Miglietta, S., Palmerini, M.G., Macchiarelli, G, and Nottola, S.A. (2016a). IVM in need of clear definitions. Hum Reprod 31, 1387–1389.PubMedCrossRefGoogle Scholar
  19. Coticchio, G., Dal Canto, M., Fadini, R., Mignini Renzini, M., Guglielmo, M.C., Miglietta, S., Palmerini, M.G., Macchiarelli, G., and Nottola, S. A. (2016b). Ultrastructure of human oocytes after in vitro maturation. Mol Hum Reprod 22, 110–118.PubMedCrossRefGoogle Scholar
  20. Coticchio, G., Dal-Canto, M., Guglielmo, M.C., Mignini-Renzini, M., and Fadini, R. (2012). Human oocyte maturation in vitro. Int J Dev Biol 56, 909–918.PubMedCrossRefGoogle Scholar
  21. Dahan, M.H., Tan, S.L., Chung, J., and Son, W.Y. (2016). Clinical definition paper on in vitro maturation of human oocytes. Hum Reprod 31, 1383–1386.PubMedCrossRefGoogle Scholar
  22. Das, M., Son, W.Y., Buckett, W., Tulandi, T., and Holzer, H. (2014). Invitro maturation versus IVF with GnRH antagonist for women with polycystic ovary syndrome: treatment outcome and rates of ovarian hyperstimulation syndrome. Reprod Biomed Online 29, 545–551.PubMedCrossRefGoogle Scholar
  23. De Sousa, P.A., Martins Da Silva, S.J., and Anderson, R.A. (2004). Neurotrophin signaling in oocyte survival and developmental competence: a paradigm for cellular toti-potency. Cloning Stem Cells 6, 375–385.PubMedCrossRefGoogle Scholar
  24. De Vos, M., Smitz, J., Thompson, J.G., and Gilchrist, R.B. (2016). The definition of IVM is clear-variations need defining. Hum Reprod 31, 2411–2415.PubMedCrossRefGoogle Scholar
  25. Del Collado, M., da Silveira, J.C., Oliveira, M.L.F., Alves, B.M.S.M., Simas, R.C., Godoy, A.T., Coelho, M.B., Marques, L.A., Carriero, M.M., Nogueira, M.F.G., et al. (2017). in vitro maturation impacts cumulusoocyte complex metabolism and stress in cattle. Reproduction 154, 8-81–893.Google Scholar
  26. Demeestere, I., Gervy, C., Centner, J., Devreker, F., Englert, Y., and Delbaere, A. (2004). Effect of insulin-like growth factor-I during preantral follicular culture on steroidogenesis, in vitro oocyte maturation, and embryo development in mice. Biol Reprod 70, 1664–1669.PubMedCrossRefGoogle Scholar
  27. Dolmans, M.M., Marinescu, C., Saussoy, P., Van Langendonckt, A., Amorim, C., and Donnez, J. (2010). Reimplantation of cryopreserved ovarian tissue from patients with acute lymphoblastic leukemia is potentially unsafe. Blood 116, 2908–2914.PubMedCrossRefGoogle Scholar
  28. Donnez, J., Martinez-Madrid, B., Jadoul, P., Van Langendonckt, A., Demylle, D., and Dolmans, M.M. (2006). Ovarian tissue cryopreservation and transplantation: a review. Hum Reprod Update 12, 519–535.PubMedCrossRefGoogle Scholar
  29. Downs, S.M. (1995). The influence of glucose, cumulus cells, and metabolic coupling on ATP levels and meiotic control in the isolated mouse oocyte. Dev Biol 167, 502–512.PubMedCrossRefGoogle Scholar
  30. Downs, S.M., Daniel, S.A.J., Bornslaeger, E.A., Hoppe, P.C., and Eppig, J. J. (1989). Maintenance of meiotic arrest in mouse oocytes by purines: modulation of cAMP levels and cAMP phosphodiesterase activity. Gamete Res 23, 323–334.PubMedCrossRefGoogle Scholar
  31. Edwards, L.J., Williams, D.A., and Gardner, D.K. (1998). Intracellular pH of the mouse preimplantation embryo: amino acids act as buffers of intracellular pH. Hum Reprod 13, 3441–3448.PubMedCrossRefGoogle Scholar
  32. Ezoe, K., Yabuuchi, A., Tani, T., Mori, C., Miki, T., Takayama, Y., Beyhan, Z., Kato, Y., Okuno, T., Kobayashi, T., et al. (2015). Developmental competence of vitrified-warmed bovine oocytes at the germinal-vesicle stage is improved by cyclic adenosine monophosphate modulators during in vitro maturation. PLoS ONE 10, e0126801.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Fahy, M.M., and Kane, M.T. (1992). Inositol stimulates DNA and protein synthesis, and expansion by rabbit blastocysts in vitro. Hum Reprod 7, 550–552.PubMedCrossRefGoogle Scholar
  34. Fan, H.Y., Li, M.Y., Tong, C., Chen, D.Y., Xia, G.L., Song, X.F., Schatten, H., and Sun, Q.Y. (2002). Inhibitory effects of cAMP and protein kinase C on meiotic maturation and MAP kinase phosphorylation in porcine oocytes. Mol Reprod Dev 63, 480–487.PubMedCrossRefGoogle Scholar
  35. Farsi, M.M., Kamali, N., and Pourghasem, M. (2013). Embryological aspects of oocyte in vitro maturation. Int J Mol Cell Med 2, 99–109.PubMedPubMedCentralGoogle Scholar
  36. Franciosi, F., Lodde, V., Goudet, G., Duchamp, G., Deleuze, S., Douet, C., Tessaro, I., and Luciano, A.M. (2012). Changes in histone H4 acetylation during in vivo versus in vitro maturation of equine oocytes. MHRBasic Sci Reprod Med 18, 243–252.CrossRefGoogle Scholar
  37. Gardner, D.K., Lane, M., Spitzer, A., and Batt, P.A. (1994). Enhanced rates of cleavage and development for sheep zygotes cultured to the blastocyst stage in vitro in the absence of serum and somatic cells: amino acids, vitamins, and culturing embryos in groups stimulate development. Biol Reprod 50, 390–400.PubMedCrossRefGoogle Scholar
  38. Ge, H.S., Huang, X.F., Zhang, W., Zhao, J.Z., Lin, J.J., and Zhou, W. (2008). Exposure to human chorionic gonadotropin during in vitro maturation does not improve the maturation rate and developmental potential of immature oocytes from patients with polycystic ovary syndrome. Fertil Steril 89, 98–103.PubMedCrossRefGoogle Scholar
  39. Gilchrist, R.B., Lane, M., and Thompson, J.G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update 14, 159–177.PubMedCrossRefGoogle Scholar
  40. Gilchrist, R.B., and Thompson, J.G. (2007). Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology 67, 6–15.PubMedCrossRefGoogle Scholar
  41. Gioia, L., Barboni, B., Turriani, M., Capacchietti, G., Pistilli, M.G., Berardinelli, P., and Mattioli, M. (2005). The capability of reprogramming the male chromatin after fertilization is dependent on the quality of oocyte maturation. Reproduction 130, 29–39.PubMedCrossRefGoogle Scholar
  42. Guler, A., Poulin, N., Mermillod, P., Terqui, M., and Cognié, Y. (2000). Effect of growth factors, EGF and IGF-I, and estradiol on in vitro maturation of sheep oocytes. Theriogenology 54, 209–218.PubMedCrossRefGoogle Scholar
  43. Hankinson, S.E., Willett, W.C., Colditz, G.A., Hunter, D.J., Michaud, D.S., Deroo, B., Rosner, B., Speizer, F.E., and Pollak, M. (1998). Circulating concentrations of insulin-like growth factor I and risk of breast cancer. Lancet 351, 1393–1396.PubMedCrossRefGoogle Scholar
  44. Heinzmann, J., Hansmann, T., Herrmann, D., Wrenzycki, C., Zechner, U., Haaf, T., and Niemann, H. (2011). Epigenetic profile of developmentally important genes in bovine oocytes. Mol Reprod Dev 78, 188–201.PubMedCrossRefGoogle Scholar
  45. Heinzmann, J., Mattern, F., Aldag, P., Bernal-Ulloa, S.M., Schneider, T., Haaf, T., and Niemann, H. (2015). Extended in vitro maturation affects gene expression and DNA methylation in bovine oocytes. Mol Hum Reprod 21, 770–782.PubMedCrossRefGoogle Scholar
  46. Hillier, S.G., Smyth, C.D., Whitelaw, P.R., Miró, F., and Howles, C.M. (1995). Gonadotrophin control of follicular function. Horm Res 43, 216–223.PubMedCrossRefGoogle Scholar
  47. Hong, S.G., Jang, G., Oh, H.J., Koo, O.J., Park, J.E., Park, H.J., Kang, S.K., and Lee, B.C. (2009). The effects of brain-derived neurotrophic factor and metformin on in vitro developmental competence of bovine oocytes. Zygote 17, 187–193.PubMedCrossRefGoogle Scholar
  48. Hussein, T.S., Thompson, J.G., and Gilchrist, R.B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev Biol 296, 514–521.PubMedCrossRefGoogle Scholar
  49. Ibáñez, E., Sanfins, A., Combelles, C.M.H., Overström, E.W., and Albertini, D.F. (2005). Genetic strain variations in the metaphase-II phenotype of mouse oocytes matured in vivo or in vitro. Reproduction 130, 845–855.PubMedCrossRefGoogle Scholar
  50. Jones, G.M., Cram, D.S., Song, B., Magli, M.C., Gianaroli, L., Lacham-Kaplan, O., Findlay, J.K., Jenkin, G., and Trounson, A.O. (2008). Gene expression profiling of human oocytes following in vivo or in vitro maturation. Hum Reprod 23, 1138–1144.PubMedCrossRefGoogle Scholar
  51. Jurema, M.W., and Nogueira, D. (2006). in vitro maturation of human oocytes for assisted reproduction. Fertil Steril 86, 1277–1291.PubMedCrossRefGoogle Scholar
  52. Ka, H.H., Sawai, K., Wang, W.H., Im, K.S., and Niwa, K. (1997). Amino acids in maturation medium and presence of cumulus cells at fertilization promote male pronuclear formation in porcine oocytes matured and penetrated in vitro. Biol Reprod 57, 1478–1483.PubMedCrossRefGoogle Scholar
  53. Kafilzadeh, F., Karami Shabankareh, H., and Soltani, L. (2012). Effect of various concentrations of minimal essential medium vitamins (MEM vitamins) on development of sheep oocytes during in-vitro maturation. Iran J Reprod Med 10, 93–98.PubMedPubMedCentralGoogle Scholar
  54. Kawamura, K., Kawamura, N., Mulders, S.M., Sollewijn Gelpke, M.D., and Hsueh, A.J.W. (2005). Ovarian brain-derived neurotrophic factor (BDNF) promotes the development of oocytes into preimplantation embryos. Proc Natl Acad Sci USA 102, 9206–9211.PubMedPubMedCentralCrossRefGoogle Scholar
  55. Kim, M.K., Fibrianto, Y.H., Oh, H.J., Jang, G., Kim, H.J., Lee, K.S., Kang, S.K., Lee, B.C., and Hwang, W.S. (2005). Effects of estradiol-17β and progesterone supplementation on in vitro nuclear maturation of canine oocytes. Theriogenology 63, 1342–1353.PubMedCrossRefGoogle Scholar
  56. Kuhtz, J., Romero, S., De Vos, M., Smitz, J., Haaf, T., and Anckaert, E. (2014). Human in vitro oocyte maturation is not associated with increased imprinting error rates at LIT1, SNRPN, PEG3 and GTL2. Hum Reprod 29, 1995–2005.PubMedCrossRefGoogle Scholar
  57. Laforest, M.F., Pouliot, E., Guéguen, L., and Richard, F.J. (2005). Fundamental significance of specific phosphodiesterases in the control of spontaneous meiotic resumption in porcine oocytes. Mol Reprod Dev 70, 361–372.PubMedCrossRefGoogle Scholar
  58. Lane, M., and Gardner, D.K. (1998). Amino acids and vitamins prevent culture-induced metabolic perturbations and associated loss of viability of mouse blastocysts. Hum Reprod 13, 991–997.PubMedCrossRefGoogle Scholar
  59. Lee, E., Jeong, Y.I., Park, S.M., Lee, J.Y., Kim, J.H., Park, S.W., Hossein, M.S., Jeong, Y.W., Kim, S., Hyun, S.H., et al. (2007). Beneficial effects of brain-derived neurotropic factor on in vitro maturation of porcine oocytes. Reproduction 134, 405–414.PubMedCrossRefGoogle Scholar
  60. Lee, Y.S., Latham, K.E., and Vandevoort, C.A. (2008). Effects of in vitro maturation on gene expression in rhesus monkey oocytes. Physiol Genomics 35, 145–158.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Lequarre, A.S., Traverso, J.M., Marchandise, J., and Donnay, I. (2004). Poly(A) RNA is reduced by half during bovine oocyte maturation but increases when meiotic arrest is maintained with CDK inhibitors. Biol Reprod 71, 425–431.PubMedCrossRefGoogle Scholar
  62. Lindbloom, S.M., Farmerie, T.A., Clay, C.M., Seidel Jr., G.E., and Carnevale, E.M. (2008). Potential involvement of EGF-like growth factors and phosphodiesterases in initiation of equine oocyte maturation. Animal Reprod Sci 103, 187–192.CrossRefGoogle Scholar
  63. Makarevich, A.V., and Markkula, M. (2002). Apoptosis and cell proliferation potential of bovine embryos stimulated with insulin-like growth factor I during in vitro maturation and culture. Biol Reprod 66, 386–392.PubMedCrossRefGoogle Scholar
  64. Maman, E., Yung, Y., Kedem, A., Yerushalmi, G.M., Konopnicki, S., Cohen, B., Dor, J., and Hourvitz, A. (2012). High expression of luteinizing hormone receptors messenger RNA by human cumulus granulosa cells is in correlation with decreased fertilization. Fertil Steril 97, 592–598.PubMedCrossRefGoogle Scholar
  65. Martins da Silva, S.J., Gardner, J.O., Taylor, J.E., Springbett, A., De Sousa, P.A., and Anderson, R.A. (2005). Brain-derived neurotrophic factor promotes bovine oocyte cytoplasmic competence for embryo development. Reproduction 129, 423–434.PubMedCrossRefGoogle Scholar
  66. Matzuk, M.M., Burns, K.H., Viveiros, M.M., and Eppig, J.J. (2002). Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296, 2178–2180.PubMedCrossRefGoogle Scholar
  67. Mikkelsen, A.L. (2005). Strategies in human in-vitro maturation and their clinical outcome. Reprod Biomed Online 10, 593–599.PubMedCrossRefGoogle Scholar
  68. Mikkelsen, A.L., Høst, E., Blaabjerg, J., and Lindenberg, S. (2003). Time interval between FSH priming and aspiration of immature human oocytes for in-vitro maturation: a prospective randomized study. Reprod Biomed Online 6, 416–420.PubMedCrossRefGoogle Scholar
  69. Mikkelsen, A., and Lindenberg, S. (2001). Benefit of FSH priming of women with PCOS to the in vitro maturation procedure and the outcome: a randomized prospective study. Reproduction 122, 587–592.PubMedCrossRefGoogle Scholar
  70. Mottershead, D.G., Sugimura, S., Al-Musawi, S.L., Li, J.J., Richani, D., White, M.A., Martin, G.A., Trotta, A.P., Ritter, L.J., Shi, J., et al. (2015). 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 290, 24007–24020.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Nogueira, D., Sadeu, J.C., and Montagut, J. (2012). in vitro oocyte maturation: current status. Semin Reprod Med 30, 199–213.PubMedCrossRefGoogle Scholar
  72. Nyholt de Prada, J.K., Lee, Y.S., Latham, K.E., Chaffin, C.L., and VandeVoort, C.A. (2009). Role for cumulus cell-produced EGF-like ligands during primate oocyte maturation in vitro. Am J Physiol Endocrinol Metab 296, E1049–E1058.PubMedPubMedCentralCrossRefGoogle Scholar
  73. Ouandaogo, Z.G., Haouzi, D., Assou, S., Dechaud, H., Kadoch, I.J., De Vos, J., and Hamamah, S. (2011). Human cumulus cells molecular signature in relation to oocyte nuclear maturity stage. PLoS ONE 6, e27179.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Ouandaogo, Z.G., Frydman, N., Hesters, L., Assou, S., Haouzi, D., Dechaud, H., Frydman, R., and Hamamah, S. (2012). Differences in transcriptomic profiles of human cumulus cells isolated from oocytes at GV, MI and MII stages after in vivo and in vitro oocyte maturation. Hum Reprod 27, 2438–2447.PubMedCrossRefGoogle Scholar
  75. Piquette, G.N. (2006). The in vitro maturation (IVM) of human oocytes for in vitro fertilization (IVF): is it time yet to switch to IVM-IVF? Fertil Steril 85, 833–835, 841.PubMedCrossRefGoogle Scholar
  76. Pliushch, G., Schneider, E., Schneider, T., El Hajj, N., Rösner, S., Strowitzki, T., and Haaf, T. (2015). in vitro maturation of oocytes is not associated with altered deoxyribonucleic acid methylation patterns in children from in vitro fertilization or intracytoplasmic sperm injection. Fertil Steril 103, 720–727.e1.PubMedCrossRefGoogle Scholar
  77. Qiao, J., and Li, R. (2014). Fertility preservation: challenges and opportunities. Lancet 384, 1246–1247.PubMedCrossRefGoogle Scholar
  78. Pfeifer, S., Fritz, M., Goldberg, J., Adamson, G.D., Mcclure, R.D., Lobo, R., Thomas, M.A., Widra, E., Licht, M., Collins, J., et al. (2013). in vitro maturation: a committee opinion. Fertil Steril 99, 663–666.CrossRefGoogle Scholar
  79. Reavey, J., Vincent, K., Child, T., and Granne, I.E. (2016). Human chorionic gonadotrophin priming for fertility treatment with in vitro maturation. Cochrane Database Syst Rev 11, D8720.Google Scholar
  80. Reinblatt, S.L., Son, W.Y., Shalom-Paz, E., and Holzer, H. (2011). Controversies in IVM. J Assist Reprod Genet 28, 525–530.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Richani, D., Ritter, L.J., Thompson, J.G., and Gilchrist, R.B. (2013). Mode of oocyte maturation affects EGF-like peptide function and oocyte competence. Mol Hum Reprod 19, 500–509.PubMedCrossRefGoogle Scholar
  82. Richani, D., Sutton-McDowall, M.L., Frank, L.A., Gilchrist, R.B., and Thompson, J.G. (2014). Effect of epidermal growth factor-like peptides on the metabolism of in vitro-matured mouse oocytes and cumulus cells. Biol Reprod 90, 1–10.CrossRefGoogle Scholar
  83. Richani, D., and Gilchrist, R.B. (2017). The epidermal growth factor network: role in oocyte growth, maturation and developmental competence. Hum Reprod Update 20, 1–14.Google Scholar
  84. Romero, S., Sanchez, F., Lolicato, F., Van Ranst, H., and Smitz, J. (2016). Immature oocytes from unprimed juvenile mice become a valuable source for embryo production when using C-type natriuretic peptide as essential component of culture medium. Biol Reprod 95, 64–64.PubMedCrossRefGoogle Scholar
  85. Rose-Hellekant, T.A., Libersky-Williamson, E.A., and Bavister, B.D. (1998). Energy substrates and amino acids provided during in vitro maturation of bovine oocytes alter acquisition of developmental competence. Zygote 6, 285–294.PubMedCrossRefGoogle Scholar
  86. Rosendahl, M., Andersen, M.T., Ralfkiær, E., Kjeldsen, L., Andersen, M. K., and Andersen, C.Y. (2010). Evidence of residual disease in cryopreserved ovarian cortex from female patients with leukemia. Fertil Steril 94, 2186–2190.PubMedCrossRefGoogle Scholar
  87. Safian, F., Khalili, M.A., Ashourzadeh, S., and Omidi, M. (2017). Analysis of meiotic spindle and zona pellucida birefringenceof IVM oocytes in PCOS patients. Turk J Med Sci 47, 368–373.PubMedCrossRefGoogle Scholar
  88. Sánchez, F., Lolicato, F., Romero, S., De Vos, M., Van Ranst, H., Verheyen, G., Anckaert, E., and Smitz, J.E.J. (2017). An improved IVM method for cumulus-oocyte complexes from small follicles in polycystic ovary syndrome patients enhances oocyte competence and embryo yield. Hum Reprod 32, 2056–2068.PubMedCrossRefGoogle Scholar
  89. Seifer, D.B., Feng, B., Shelden, R.M., Chen, S., and Dreyfus, C.F. (2002). Brain-derived neurotrophic factor: a novel human ovarian follicular protein. J Clin Endocrinol Metab 87, 655–659.PubMedCrossRefGoogle Scholar
  90. Seifer, D.B., Feng, B., and Shelden, R.M. (2006). Immunocytochemical evidence for the presence and location of the neurotrophin-Trk receptor family in adult human preovulatory ovarian follicles. Am J Obstet Gynecol 194, 1129–1134, 1134–1136.PubMedCrossRefGoogle Scholar
  91. Shavit, T., Ellenbogen, A., Michaeli, M., Kartchovsky, E., Ruzov, O., and Shalom-Paz, E. (2014). in-vitro maturation of oocytes vs. in-vitro fertilization with a gonadotropin-releasing hormone antagonist for women with polycystic ovarian syndrome: can superiority be defined? Eur J Obstet Gynecol Reprod Biol 179, 46–50.PubMedGoogle Scholar
  92. Shimada, M., Hernandez-Gonzalez, I., Gonzalez-Robanya, I., and Ri-chards, J.A.S. (2006). Induced Expression of pattern recognition receptors in cumulus oocyte complexes: novel evidence for innate immunelike functions during ovulation. Mol Endocrinol 20, 3228–3239.PubMedCrossRefGoogle Scholar
  93. Smitz, J., and Cortvrindt, R. (1999). Oocyte in-vitro maturation and follicle culture: current clinical achievements and future directions. Hum Reprod 14, 145–161.PubMedCrossRefGoogle Scholar
  94. Söderström-Anttila, V., Mäkinen, S., Tuuri, T., and Suikkari, A.M. (2005). Favourable pregnancy results with insemination of in vitro matured oocytes from unstimulated patients. Hum Reprod 20, 1534–1540.PubMedCrossRefGoogle Scholar
  95. Somfai, T., Kikuchi, K., Onishi, A., Iwamoto, M., Fuchimoto, D., Bali Papp, Á., Sato, E., and Nagai, T. (2003). Meiotic arrest maintained by cAMP during the initiation of maturation enhances meiotic potential and developmental competence and reduces polyspermy of IVM/IVF porcine oocytes. Zygote 11, 199–206.PubMedCrossRefGoogle Scholar
  96. Son, W.Y., Chung, J.T., Herrero, B., Dean, N., Demirtas, E., Holzer, H., Elizur, S., Chian, R.C., and Tan, S.L. (2008). Selection of the optimal day for oocyte retrieval based on the diameter of the dominant follicle in hCG-primed in vitro maturation cycles. Hum Reprod 23, 2680–2685.PubMedCrossRefGoogle Scholar
  97. Su, J., Hu, G., Wang, Y., Liang, D., Gao, M., Sun, H., and Zhang, Y. (2014). Recombinant human growth differentiation factor-9 improves oocyte reprogramming competence and subsequent development of bovine cloned embryos. Cell Reprogram 16, 281–289.PubMedCrossRefGoogle Scholar
  98. Sudiman, J., Sutton-McDowall, M.L., Ritter, L.J., White, M.A., Mottershead, D.G., Thompson, J.G., and Gilchrist, R.B. (2014). Bone morphogenetic protein 15 in the pro-mature complex form enhances bovine oocyte developmental competence. PLoS ONE 9, e103563.PubMedPubMedCentralCrossRefGoogle Scholar
  99. Tesfaye, D., Ghanem, N., Carter, F., Fair, T., Sirard, M.A., Hoelker, M., Schellander, K., and Lonergan, P. (2009). Gene expression profile of cumulus cells derived from cumulus-oocyte complexes matured either in vivo or in vitro. Reprod Fertil Dev 21, 451–461.PubMedCrossRefGoogle Scholar
  100. Tkachenko, O.Y., Delimitreva, S., Isachenko, E., Valle, R.R., Michelmann, H.W., Berenson, A., and Nayudu, P.L. (2010). Epidermal growth factor effects on marmoset monkey (Callithrix jacchus) oocyte in vitro maturation, IVF and embryo development are altered by gonadotrophin concentration during oocyte maturation. Hum Reprod 25, 2047–2058.PubMedCrossRefGoogle Scholar
  101. Tkachenko, O.Y., Delimitreva, S., Heistermann, M., Scheerer-Bernhard, J. U., Wedi, E., and Nayudu, P.L. (2015). Critical estradiol dose optimization for oocyte in vitro maturation in the common marmoset. Theriogenology 83, 1254–1263.PubMedCrossRefGoogle Scholar
  102. Uhm, S.J., Gupta, M.K., Yang, J.H., Chung, H.J., Min, T.S., and Lee, H.T. (2010). Epidermal growth factor can be used in lieu of follicle-stimulating hormone for nuclear maturation of porcine oocytes in vitro. Theriogenology 73, 1024–1036.PubMedCrossRefGoogle Scholar
  103. Uppangala, S., Dhiman, S., Salian, S.R., Singh, V.J., Kalthur, G., and Adiga, S.K. (2015). in vitro matured oocytes are more susceptible than in vivo matured oocytes to mock ICSI induced functional and genetic changes. PLoS ONE 10, e0119735.PubMedPubMedCentralCrossRefGoogle Scholar
  104. Walls, M.L., Hart, R., Keelan, J.A., and Ryan, J.P. (2016). Structural and morphologic differences in human oocytes after in vitro maturation compared with standard in vitro fertilization. Fertil Steril 106, 1392–1398.e5.PubMedCrossRefGoogle Scholar
  105. Wang, Y., Kong, N., Li, N., Hao, X., Wei, K., Xiang, X., Xia, G., and Zhang, M. (2013). Epidermal growth factor receptor signaling-dependent calcium elevation in cumulus cells is required for NPR2 inhibition and meiotic resumption in mouse oocytes. Endocrinology 154, 3401–3409.PubMedCrossRefGoogle Scholar
  106. Wei, Z., Cao, Y., Cong, L., Zhou, P., Zhang, Z., and Li, J. (2008). RETRACTED: effect of metformin pretreatment on pregnancy outcome of in vitro matured oocytes retrieved from women with polycystic ovary syndrome. Fertil Steril 90, 1149–1154.PubMedCrossRefGoogle Scholar
  107. Wei, Q., Zhou, C., Yuan, M., Miao, Y., Zhao, X., and Ma, B. (2015). Effect of C-type natriuretic peptide on maturation and developmental competence of immature mouse oocytes in vitro. Reprod Fertil Dev 29, 319–324.Google Scholar
  108. Wynn, P., Picton, H.M., Krapez, J.A., Rutherford, A.J., Balen, A.H., and Gosden, R.G. (1998). Pretreatment with follicle stimulating hormone promotes the numbers of human oocytes reaching metaphase II by invitro maturation. Hum Reprod 13, 3132–3138.PubMedCrossRefGoogle Scholar
  109. Xia, P., Tekpetey, F.R., and Armstrong, D.T. (1994). Effect of IGF-I on pig oocyte maturation, fertilization, and early embryonic development in vitro, and on granulosa and cumulus cell biosynthetic activity. Mol Reprod Dev 38, 373–379.PubMedCrossRefGoogle Scholar
  110. Yang, Z.Y., and Chian, R.C. (2017). Development of in vitro maturation techniques for clinical applications. Fertil Steril 108, 577–584.PubMedCrossRefGoogle Scholar
  111. Yeo, C.X., Gilchrist, R.B., Thompson, J.G., and Lane, M. (2008). Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum Reprod 23, 67–73.PubMedCrossRefGoogle Scholar
  112. Yerushalmi, G.M., Maman, E., Yung, Y., Kedem, A., and Hourvitz, A. (2011). Molecular characterization of the human ovulatory cascadelesson from the IVF/IVM model. J Assist Reprod Genet 28, 509–515.PubMedPubMedCentralCrossRefGoogle Scholar
  113. Yu, Y., Yan, J., Li, M., Yan, L., Zhao, Y., Lian, Y., Li, R., Liu, P., and Qiao, J. (2012). Effects of combined epidermal growth factor, brain-derived neurotrophic factor and insulin-like growth factor-1 on human oocyte maturation and early fertilized and cloned embryo development. Hum Reprod 27, 2146–2159.PubMedCrossRefGoogle Scholar
  114. Zeng, H.T., Richani, D., Sutton-McDowall, M.L., Ren, Z., Smitz, J.E.J., Stokes, Y., Gilchrist, R.B., and Thompson, J.G. (2014). Prematuration with cyclic adenosine monophosphate modulators alters cumulus cell and oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocytes. Biol Reprod 91, 47.PubMedCrossRefGoogle Scholar
  115. Zhang, J., Wei, Q., Cai, J., Zhao, X., and Ma, B. (2015). Effect of C-type natriuretic peptide on maturation and developmental competence of goat oocytes matured in vitro. PLoS ONE 10, e132318.Google Scholar
  116. Zhang, T., Zhang, C., Fan, X., Li, R., and Zhang, J. (2016). Effect of C-type natriuretic peptide pretreatment on in vitro bovine oocyte maturation. in vitro Cell Dev Biol Animal 53, 199–206.CrossRefGoogle Scholar
  117. Zheng, P. (2007). Effects of in vitro maturation of monkey oocytes on their developmental capacity. Animal Reprod Sci 98, 56–71.CrossRefGoogle Scholar
  118. Zheng, X., Wang, L., Zhen, X., Lian, Y., Liu, P., and Qiao, J. (2012a). Effect of hCG priming on embryonic development of immature oocytes collected from unstimulated women with polycystic ovarian syndrome. Reprod Biol Endocrinol 10, 40.PubMedPubMedCentralCrossRefGoogle Scholar
  119. Zheng, X., Wang, L., Zhen, X., Liu, P., and Qiao, J. (2012b). Pregnancy outcomes in women with polycystic ovary syndrome after in vitro oocyte maturation. Reprod Contracept 32, 749–753.Google Scholar
  120. Zuelke, K.A., and Bracketf, B.G. (1990). Luteinizing hormone-enhanced in vitro maturation of bovine oocytes with and without protein supplementation. Biol Reprod 43, 784–787.PubMedCrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Cuiling Lu
    • 1
    • 2
    • 3
  • Yaoyao Zhang
    • 1
    • 2
    • 3
  • Xiaoying Zheng
    • 1
    • 2
    • 3
  • Xueling Song
    • 1
    • 2
    • 3
  • Ruiyang
    • 1
    • 2
    • 3
  • Jieyan
    • 1
    • 2
    • 3
  • Huailiang Feng
    • 4
  • Jie Qiao
    • 1
    • 2
    • 3
  1. 1.Reproductive Medical Center, Department of Obstetrics and GynecologyPeking University Third HospitalBeijingChina
  2. 2.Key Laboratory of Assisted ReproductionMinistry of EducationBeijingChina
  3. 3.Beijing Key Laboratory of Reproductive Endocrinology and Assisted ReproductionBeijingChina
  4. 4.Department of Obstetrics and GynecologyNew York Hospital Queens-affiliated Weill Medical College of Cornell UniversityNew YorkUSA

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