About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 861460, 18 pages
http://dx.doi.org/10.1155/2013/861460
Research Article

Expression of Pluripotency and Oocyte-Related Genes in Single Putative Stem Cells from Human Adult Ovarian Surface Epithelium Cultured In Vitro in the Presence of Follicular Fluid

1Department of Obstetrics and Gynecology, University Medical Centre Ljubljana, Slajmerjeva 3, 1000 Ljubljana, Slovenia
2Institute for Anatomy and Cell Biology, Medical Faculty, University of Heidelberg, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany
3TATAA Biocenter AB, Odinsgatan 28, 41103 Göteborg, Sweden
4Institute of Biotechnology AS CR, Lb Building, 14220 Prague, Czech Republic

Received 30 October 2012; Accepted 24 December 2012

Academic Editor: Deepa Bhartiya

Copyright © 2013 Irma Virant-Klun et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. Hübner, G. Fuhrmann, L. K. Christenson et al., “Derivation of oocytes from mouse embryonic stem cells,” Science, vol. 300, no. 5623, pp. 1251–1256, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. A. T. Clark, M. S. Bodnar, M. Fox et al., “Spontaneous differentiation of germ cells from human embryonic stem cells in vitro,” Human Molecular Genetics, vol. 13, no. 7, pp. 727–739, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. O. Lacham-Kaplan, H. Chy, and A. Trounson, “Testicular cell conditioned medium supports differentiation of embryonic stem cells into ovarian structures containing oocytes,” Stem Cells, vol. 24, no. 2, pp. 266–273, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. I. Novak, D. A. Lightfoot, H. Wang, A. Eriksson, E. Mahdy, and C. Höög, “Mouse embryonic stem cells form follicle-like ovarian structures but do not progress through meiosis,” Stem Cells, vol. 24, no. 8, pp. 1931–1936, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. C. R. Nicholas, K. M. Haston, A. K. Grewall, T. A. Longacre, and R. A. Reijo Pera, “Transplantation directs oocyte maturation from embryonic stem cells and provides a therapeutic strategy for female infertility,” Human Molecular Genetics, vol. 18, no. 22, pp. 4376–4389, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Zou, Z. Yuan, Z. Yang et al., “Production of offspring from a germline stem cell line derived from neonatal ovaries,” Nature Cell Biology, vol. 11, no. 5, pp. 631–636, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. G. B. Zhou, Q. G. Meng, and N. Li, “In vitro derivation of germ cells from embryonic stem cells in mammals,” Molecular Reproduction and Development, vol. 77, no. 7, pp. 586–594, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. O. E. Psathaki, K. Hübner, D. Sabour, et al., “Ultrastructural characterization of mouse embryonic stem cell-derived oocytes and granulosa cells,” Stem Cells and Development, vol. 20, no. 12, pp. 2205–2215, 2011. View at Publisher · View at Google Scholar
  9. M. Richards, C. Y. Fong, and A. Bongso, “Comparative evaluation of different in vitro systems that stimulate germ cell differentiation in human embryonic stem cells,” Fertility and Sterility, vol. 93, no. 3, pp. 986–994, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. F. D. West, M. I. Roche-Rios, S. Abraham et al., “KIT ligand and bone morphogenetic protein signaling enhances human embryonic stem cell to germ-like cell differentiation,” Human Reproduction, vol. 25, no. 1, pp. 168–178, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. J. V. Medrano, C. Ramathal, H. N. Nguyen, C. Simon, and R. A. Reijo Pera, “Divergent RNA-binding proteins, DAZL and VASA, induce meiotic progression in human germ cells derived in vitro,” Stem Cells, vol. 30, no. 3, pp. 441–451, 2012. View at Publisher · View at Google Scholar
  12. X. Cheng, S. Chen, X. Yu, P. Zheng, and H. Wang, “BMP15 gene is activated during human amniotic fluid stem cell differentiation into oocyte-like cells,” DNA and Cell Biology, vol. 31, no. 7, pp. 1198–1204, 2012. View at Publisher · View at Google Scholar
  13. P. W. Dyce, L. Wen, and J. Li, “In vitro germline potential of stem cells derived from fetal porcine skin,” Nature Cell Biology, vol. 8, no. 4, pp. 384–390, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. P. W. Dyce, W. Shen, E. Huynh et al., “Analysis of oocyte-like cells differentiated from porcine fetal skin-derived stem cells,” Stem Cells and Development, vol. 20, no. 5, pp. 809–819, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Danner, J. Kajahn, C. Geismann, E. Klink, and C. Kruse, “Derivation of oocyte-like cells from a clonal pancreatic stem cell line,” Molecular Human Reproduction, vol. 13, no. 1, pp. 11–20, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. S. P. Gong, S. T. Lee, E. J. Lee et al., “Embryonic stem cell-like cells established by culture of adult ovarian cells in mice,” Fertility and Sterility, vol. 93, no. 8, pp. 2594–2601, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Pacchiarotti, C. Maki, T. Ramos et al., “Differentiation potential of germ line stem cells derived from the postnatal mouse ovary,” Differentiation, vol. 79, no. 3, pp. 159–170, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Bukovsky, M. Svetlikova, and M. R. Caudle, “Oogenesis in cultures derived from adult human ovaries,” Reproductive Biology and Endocrinology, vol. 3, p. 17, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. I. Virant-Klun, N. Zech, P. Rozman et al., “Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes,” Differentiation, vol. 76, no. 8, pp. 843–856, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. I. Virant-Klun, P. Rožman, B. Cvjeticanin et al., “Parthenogenetic embryo-like structures in the human ovarian surface epithelium cell culture in postmenopausal women with no naturally present follicles and oocytes,” Stem Cells and Development, vol. 18, no. 1, pp. 137–150, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. I. Virant-Klun, T. Skutella, M. Stimpfel, and J. Sinkovec, “Ovarian surface epithelium in patients with severe ovarian infertility: a potential source of cells expressing markers of pluripotent/multipotent stem cells,” Journal of Biomedicine and Biotechnology, vol. 2011, Article ID 381928, 2011. View at Publisher · View at Google Scholar
  22. S. Parte, D. Bhartiya, J. Telang, et al., “Detection, characterization, and spontaneous differentiation in vitro of very small embryonic-like putative stem cells in adult mammalian ovary,” Stem Cells and Development, vol. 20, no. 80, pp. 1451–1464, 2011. View at Publisher · View at Google Scholar
  23. Y. A. White, D. C. Woods, Y. Takai, O. Ishihara, H. Seki, and J. L. Tilly, “Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women,” Nature Medicine, vol. 18, no. 3, pp. 413–421, 2012. View at Publisher · View at Google Scholar
  24. D. Goswami and G. S. Conway, “Premature ovarian failure,” Hormone Research, vol. 68, no. 4, pp. 196–202, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Berthois, J. A. Katzenellenbogen, and B. S. Katzenellenbogen, “Phenol red in tissue culture media is a weak estrogen: implications concerning the study of estrogen-responsive cells in culture,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 8, pp. 2496–2500, 1986. View at Scopus
  26. M. Bengtsson, A. Ståhlberg, P. Rorsman, and M. Kubista, “Gene expression profiling in single cells from the pancreatic islets of Langerhans reveals lognormal distribution of mRNA levels,” Genome Research, vol. 15, no. 10, pp. 1388–1392, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Raj, C. S. Peskin, D. Tranchina, D. Y. Vargas, and S. Tyagi, “Stochastic mRNA synthesis in mammalian cells,” PLoS Biology, vol. 4, no. 10, p. e309, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Ståhlberg, D. Andersson, J. Aurelius et al., “Defining cell populations with single-cell gene expression profiling: correlations and identification of astrocyte subpopulations,” Nucleic Acids Research, vol. 39, no. 4, p. e24, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Bergkvist, V. Rusnakova, R. Sindelka et al., “Gene expression profiling-clusters of possibilities,” Methods, vol. 50, no. 4, pp. 323–335, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. I. J. Duijkers, W. N. Willemsen, H. M. Hollanders, C. J. Hamilton, C. M. Thomas, and H. M. Vemer, “Follicular fluid hormone concentrations after ovarian stimulation using gonadotropin preparations with different FSH/LH ratios. II. Comparison of hMG and recombinant FSH,” International Journal of Fertility and Women's Medicine, vol. 42, no. 6, pp. 431–435, 1997. View at Scopus
  31. A. Velazquez, A. Reyes, J. Chargoy, and A. Rosado, “Amino acid and protein concentrations of human follicular fluid,” Fertility and Sterility, vol. 28, no. 1, pp. 96–100, 1977. View at Scopus
  32. E. V. Bokal, K. F. Tacer, M. Vrbnjak et al., “Follicular sterol composition in gonadotrophin stimulated women with polycystic ovarian syndrome,” Molecular and Cellular Endocrinology, vol. 249, no. 1-2, pp. 92–98, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Smitz, H. M. Picton, P. Platteau et al., “Principal findings from a multicenter trial investigating the safety of follicular-fluid meiosis-activating sterol for in vitro maturation of human cumulus-enclosed oocytes,” Fertility and Sterility, vol. 87, no. 4, pp. 949–964, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. U. Ulug, E. Turan, S. B. Tosun, H. F. Erden, and M. Bahceci, “Comparison of preovulatory follicular concentrations of epidermal growth factor, insulin-like growth factor-I, and inhibins A and B in women undergoing assisted conception treatment with gonadotropin-releasing hormone (GnRH) agonists and GnRH antagonists,” Fertility and Sterility, vol. 87, no. 4, pp. 995–998, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. L. K. Doyle and F. X. Donadeu, “Regulation of the proliferative activity of ovarian surface epithelial cells by follicular fluid,” Animal Reproduction Science, vol. 114, no. 4, pp. 443–448, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Tesarik and C. Mendoza, “Nongenomic effects of 17β-estradiol on maturing human oocytes: relationship to oocyte developmental potential,” Journal of Clinical Endocrinology and Metabolism, vol. 80, no. 4, pp. 1438–1443, 1995. View at Scopus
  37. L. O. Costa, M. C. Mendes, R. A. Ferriani, M. D. Moura, R. M. Reis, and M. F. Silva de Sá, “Estradiol and testosterone concentrations in follicular fluid as criteria to discriminate between mature and immature oocytes,” Brazilian Journal of Medical and Biological Research, vol. 37, no. 11, pp. 1747–1755, 2004. View at Scopus
  38. K. Tsuji, M. Sowa, and R. Nakano, “Relationship among the status of the human oocyte, the 17β-estradiol concentration in the antral fluid and the follicular size,” Endocrinologia Japonica, vol. 30, no. 2, pp. 251–254, 1983. View at Scopus
  39. R. S. Carson, A. O. Trounson, and J. K. Findlay, “Successful fertilisation of human oocytes in vitro: concentration of estradiol-17β, progesterone and androstenedione in the antral fluid of donor follicles,” Journal of Clinical Endocrinology and Metabolism, vol. 55, no. 4, pp. 798–800, 1982. View at Scopus
  40. J. S. Kim, B. S. Song, S. R. Lee et al., “Supplementation with estradiol-17β improves porcine oocyte maturation and subsequent embryo development,” Fertility and Sterility, vol. 95, no. 8, pp. 2582–2584, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. B. Siriaroonrat, P. Comizzoli, N. Songsasen, S. L. Monfort, D. E. Wildt, and B. S. Pukazhenthi, “Oocyte quality and estradiol supplementation affect in vitro maturation success in the white-tailed deer (Odocoileus virginianus),” Theriogenology, vol. 73, no. 1, pp. 112–119, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. P. Zheng, W. Si, B. D. Bavister, J. Yang, C. Ding, and W. Ji, “17β-Estradiol and progesterone improve in-vitro cytoplasmic maturation of oocytes from unstimulated prepubertal and adult rhesus monkeys,” Human Reproduction, vol. 18, no. 10, pp. 2137–2144, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Garcia-Cruz, M. A. Brieño, I. Roig et al., “Dynamics of cohesin proteins REC8, STAG3, SMC1β and SMC3 are consistent with a role in sister chromatid cohesion during meiosis in human oocytes,” Human Reproduction, vol. 25, no. 9, pp. 2316–2327, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. W. Chen, W. Jia, K. Wang, et al., “Retinoic acid regulates germ cell differentiation in mouse embryonic stem cells through a Smad-dependent pathway,” Biochemical and Biophysical Research Communications, vol. 418, no. 3, pp. 571–577, 2012. View at Publisher · View at Google Scholar