Reproductive BioMedicine Online
Volume 20, Issue 1 , Pages 11-25 , January 2010

Effect of insulin on oogenesis from mouse fetal germ cells in a serum-free 3D culture system

  • L.L. Sun

      Affiliations

    • Laboratory of Germ Cell Biology, College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China
    • These authors contributed equally to this work.
  • ,
  • Z.Y. Sun

      Affiliations

    • Department of Urology, Daping Hospital, Third Military Medical University, Chongqing 400042, China
    • These authors contributed equally to this work.
  • ,
  • P. Zhang

      Affiliations

    • Laboratory of Germ Cell Biology, College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China
  • ,
  • X.W. Zhai

      Affiliations

    • Laboratory of Germ Cell Biology, College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China
  • ,
  • J. Tang

      Affiliations

    • Laboratory of Molecular and Cell Genetics, Hefei National Laboratory for Physical Sciences at Microscale and School of Life Sciences, University of Science and Technology of China, Hefei, Anhui 230027, China
  • ,
  • Q.J. Pan

      Affiliations

    • Laboratory of Germ Cell Biology, College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China
  • ,
  • Q.H. Shi

      Affiliations

    • Laboratory of Molecular and Cell Genetics, Hefei National Laboratory for Physical Sciences at Microscale and School of Life Sciences, University of Science and Technology of China, Hefei, Anhui 230027, China
  • ,
  • W. Shen

      Affiliations

    • Laboratory of Germ Cell Biology, College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China
    • Corresponding Author InformationCorresponding author.

Received 25 February 2009 ,Revised 1 April 2009 ,Accepted 7 October 2009.

References 

  1. Acevedo N, Ding J, Smith GD. Insulin signaling in mouse oocytes. Biol. Reprod. 2007;77:872–879
  2. Byskov AG, Hoyer PE. Embryology of mammalian gonads and ducts. In:  Knobil E,  Neill JD editor. Physiology of Reproduction. New York: Raven Press; 1994;p. 487–540
  3. Byskov AG, Xia G, Andersen CY. The cortex-medulla oocyte growth pattern is organized during fetal life: an in-vitro study of the mouse ovary. Mol. Hum. Reprod. 1997;3:795–800
  4. Chuma S, Nakatsuji N. Autonomous transition into meiosis of mouse fetal germ cells in vitro and its inhibition by gp130-mediated signaling. Dev. Biol. 2001;229:468–479
  5. de Felici M, McLaren A. In vitro culture mouse primordial germ cells. Exp. Cell Res. 1983;144:417–427
  6. de Matos DG, Furnus CC, Moses DF. Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol. Reprod. 1997;57:1420–1425
  7. Demeestere I, Centner J, Gervy C, et al. Impact of various endocrine and paracrine factors on in vitro culture of preantral follicles in rodents. Reprod. 2005;130:147–156
  8. Dong HS, Li L, Song ZH, et al. Premeiotic fetal murine germ cells cultured in vitro form typical oocyte-like cells but do not progress through meiosis. Theriogenol. 2009;72:219–231
  9. Eppig JJ, O’Brien MJ. Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod. 1996;54:197–207
  10. Eppig J, Hosoe M, O’Brien M, et al. Conditions that affect acquisition of developmental competence by mouse oocytes in vitro: FSH, insulin, glucose and ascorbic acid. Mol. Cell. Endocrinol. 2000;163:109–116
  11. Eppig J, O’Brien M, Pendola F, et al. Factors affecting the developmental competence of mouse oocytes grown in vitro: follicle stimulating hormone and insulin. Biol. Reprod. 1998;59:1445–1453
  12. Eppig JJ, Wigglesworth K, Pendola F, et al. Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biol. Reprod. 1997;56:976–984
  13. Fan HY, Tong C, Lian L, et al. Characterization of ribosomal s6 protein kinase p90rsk during meiotic maturation and fertilization in pig oocytes: mitogen-activated protein kinase-associated activation and localization. Biol. Reprod. 2003;68:968–977
  14. Farini D, Scaldaferri ML, Iona S, et al. Growth factors sustain primordial germ cell survival, proliferation and entering into meiosis in the absence of somatic cells. Dev. Biol. 2005;285:49–56
  15. Ge L, Sui HS, Lan GC, et al. Coculture with cumulus cells improves maturation of mouse oocytes denuded of the cumulus oophorus: observations of nuclear and cytoplasmic events. Fertil. Steril. 2008;90:2376–2388
  16. Hartshorne GM, Sargent IL, Barlow DH. Meiotic progression of mouse oocytes throughout follicle growth and ovulation in vitro. Hum. Reprod. 1994;9:352–359
  17. Kezele PR, Nilsson EE, Skinner MK. Insulin but not insulin-like growth factor-1 promotes the primordial to primary follicle transition. Mol. Cell. Endocrinol. 2002;192:37–43
  18. Klinger FG, de Felici M. In vitro development of growing oocytes from fetal mouse oocytes: stage-specific regulation by stem cell factor and granulosa cells. Dev. Biol. 2002;244:85–95
  19. Kim MK, Hossein MS, OH HJ, et al. Glutathione content of in vivo and in vitro matured canine oocytes collected from different reproductive stages. J. Veter. Med. Sci. 2007;69:627–632
  20. Latham K, Bautista F, Hirao Y, et al. Comparison of protein synthesis patterns in mouse cumulus cells and mural granulosa cells: effects of follicle-stimulating hormone and insulin on granulosa cell differentiation in vitro. Biol. Reprod. 1999;61:482–492
  21. Lee M, Kang S, Lee B, et al. The beneficial effects of insulin and metformin on in vitro developmental potential of porcine oocytes and embryos. Biol. Reprod. 2005;73:1264–1268
  22. Matzuk MM, Burns KH, Viveiros MM, et al. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Sci. 2002;296:2178–2180
  23. McLaren A, Southee D. Entry of mouse embryonic germ cells into meiosis. Dev. Biol. 1997;187:107–113
  24. Monget P, Bondy C. Importance of the IGF system in early folliculogenesis. Mol. Cell. Endocrinol. 2000;163:89–93
  25. Nayudu PL, Osborn SM. Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro. J. Reprod. Fertil. 1992;95:349–362
  26. Niwa K, Takano R, Obata Y, et al. Nuclei of oocytes derived from mouse parthenogenetic embryos are competent to support development to term. Biol. Reprod. 2004;71:1560–1567
  27. Obata Y, Kono T, Hatada I. Maturation of mouse fetal germ cells in vitro. Nat. 2002;418:497–498
  28. O’Brien MJ, Pendola JK, Eppig JJ. A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol. Reprod. 2003;68:1682–1686
  29. Pangas SA, Saudye H, Shea LD, et al. Novel approach for the three-dimensional culture of granulosa cell–oocyte complexes. Tissue Eng. 2003;9:1013–1021
  30. Pesce M, Farrace MG, Piacentini M, et al. Stem cell factor and leukemia inhibitory factor promote primordial germ cell survival by suppressing programmed cell death (apoptosis). Development. 1993;118:1089–1094
  31. Qing TT, Liu HS, Wei W, et al. Mature oocytes derived from purified mouse fetal germ cells. Hum. Reprod. 2008;23:54–61
  32. Rose UM, Hanssen RG, Kloosterboer HJ. Development and characterisation of an in vitro ovulation model using mouse ovarian follicles. Biol. Reprod. 1999;61:503–511
  33. Rucker EB, Dierisseau P, Wagner KU, et al. Bcl-x and Bax regulate mouse primordial germ cell survival and apoptosis during embryogenesis. Mol. Endocrinol. 2000;14:1038–1052
  34. SAS Institute, 1996. SAS User’s Guide: Statistics, Version 7.0. SAS Institute Inc., Cary, NC.
  35. Shen W, Li L, Bai ZD, et al. In vitro developmental of the fetal mouse germ cells into mature oocytes. Reprod. 2007;1:223–231
  36. Shen W, Li L, Zhang DH, et al. Mouse oocytes derived from fetal germ cells are competent to support the development of embryos by in vitro fertilization. Mol. Reprod. Dev. 2006;73:1312–1317
  37. Shen W, Zhang DH, Qing TT, et al. Living offspring produced by mouse oocytes derived from premeiotic fetal germ cells. Biol. Reprod. 2006;75:615–623
  38. Smitz JEJ, Cortvrindt RG. The earliest stages of folliculogenesis in vitro. Reprod. 2002;123:185–202
  39. Spears N, Boland NI, Murray AA, et al. Mouse oocytes derived from in vitro grown primary ovarian follicles are fertile. Hum. Reprod. 1994;9:527–532
  40. Su YQ, Denegre JM, Wigglesworth K, et al. Oocyte-dependent activation of mitogen-activated protein kinase (ERK1/2) in cumulus cells is required for the maturation of the mouse oocyte–cumulus cell complex. Dev. Biol. 2003;263:126–138
  41. Thomas FH, Walters KA, Telfer EE. How to make a good oocyte: an update on in-vitro models to study follicle regulation. Hum. Reprod. Update. 2003;9:541–555
  42. Wycherley G, Downey D, Kane MT, et al. A novel follicle culture system markedly increases follicle volume, cell number and oestradiol secretion. Reprod. 2004;127:669–677
  43. Xu M, West E, Shea LD, Woodruff TK. Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development. Biol. Reprod. 2006;75:916–923
  44. Yu N, Roy SK. Development of primordial and prenatal follicles from undifferentiated somatic cells and oocytes in the hamster prenatal ovary in vitro: effect of insulin. Biol. Reprod. 1999;61:1558–1567

 Lilan Sun undertook studies in animal science in China and graduated with a Bachelor’s degree in 2005. Subsequently, she undertook studies in animal reproduction and graduated with a Master’s degree in 2008. Since 2008, she has been working in the Department of Gynaecology, Infertility Centre at the Jinan Hospital as a laboratory technician. She is participating in research projects related to the culturing of germ cells in vitro.

PII: S1472-6483(09)00213-2

doi: 10.1016/j.rbmo.2009.11.001

Reproductive BioMedicine Online
Volume 20, Issue 1 , Pages 11-25 , January 2010