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Journal of Biomedicine and Biotechnology
Volume 2011, Article ID 381928, 12 pages
http://dx.doi.org/10.1155/2011/381928
Research Article

Ovarian Surface Epithelium in Patients with Severe Ovarian Infertility: A Potential Source of Cells Expressing Markers of Pluripotent/Multipotent Stem Cells

1Department of Obstetrics and Gynecology, University Medical Centre Ljubljana, 1000 Ljubljana, Slovenia
2Institute for Anatomy and Cell Biology, Faculty of Medicine, University of Heidelberg, 69120 Heidelberg, Germany

Received 6 June 2011; Accepted 31 August 2011

Academic Editor: Matthew B. Wheeler

Copyright © 2011 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. N. Auersperg, C. H. Siemens, and S. E. Myrdal, “Human ovarian surface epithelium in primary culture,” In Vitro, vol. 20, no. 10, pp. 743–755, 1984. View at Google Scholar · View at Scopus
  2. C. H. Siemens and N. Auersperg, “Serial propagation of human ovarian surface epithelium in tissue culture,” Journal of Cellular Physiology, vol. 134, no. 3, pp. 347–356, 1988. View at Google Scholar · View at Scopus
  3. P. A. Kruk, S. L. Maines-Bandiera, and N. Auersperg, “A simplified method to culture human ovarian surface epithelium,” Laboratory Investigation, vol. 63, no. 1, pp. 132–136, 1990. View at Google Scholar · View at Scopus
  4. O. Gubbay, W. Guo, M. T. Rae et al., “Anti-inflammatory and proliferative responses in human and ovine ovarian surface epithelial cells,” Reproduction, vol. 128, no. 5, pp. 607–614, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. M. T. Rae, D. Niven, H. O. D. Critchley, C. R. Harlow, and S. G. Hillier, “Antiinflammatory steroid action in human ovarian surface epithelial cells,” Journal of Clinical Endocrinology and Metabolism, vol. 89, no. 9, pp. 4538–4544, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. F. Jiang, B. O. Saunders, E. Haller, S. Livingston, S. V. Nicosia, and W. Bai, “Conditionally immortal ovarian cell lines for investigating the influence of ovarian stroma on the estrogen sensitivity and tumorigenicity of ovarian surface epithelial cells,” In Vitro Cellular and Developmental Biology, vol. 39, no. 7, pp. 304–312, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. J. M. J. Piek, J. C. Dorsman, A. Shvarts et al., “Cultures of ovarian surface epithelium from women with and without a hereditary predisposition to develop female adnexal carcinoma,” Gynecologic Oncology, vol. 92, no. 3, pp. 819–826, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. D. G. Rosen, G. Yang, R. C. Bast, and J. Liu, “Use of ras-transformed human ovarian surface epithelial cells as a model for studying ovarian cancer,” Methods in Enzymology, vol. 407, pp. 660–676, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. T. G. Shepherd, B. L. Thériault, E. J. Campbell, and M. W. Nachtigal, “Primary culture of ovarian surface epithelial cells and ascites-derived ovarian cancer cells from patients,” Nature Protocols, vol. 1, no. 6, pp. 2643–2649, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. N. Ahmed, E. W. Thompson, and M. A. Quinn, “Epithelial-mesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: an exception to the norm,” Journal of Cellular Physiology, vol. 213, no. 3, pp. 581–588, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Okamoto, A. Okamoto, T. Nikaido et al., “Mesenchymal to epithelial transition in the human ovarian surface epithelium focusing on inclusion cysts,” Oncology Reports, vol. 21, no. 5, pp. 1209–1214, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Zhu, M. Nilsson, and K. Sundfeldt, “Phenotypic plasticity of the ovarian surface epithelium: TGF-β1 induction of Epithelial to Mesenchymal Transition (EMT) in vitro,” Endocrinology, vol. 151, no. 11, pp. 5497–5505, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. N. J. Bowen, L. D. Walker, L. V. Matyunina et al., “Gene expression profiling supports the hypothesis that human ovarian surface epithelia are multipotent and capable of serving as ovarian cancer initiating cells,” BMC Medical Genomics, vol. 2, article 71, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. J. A. Parrott, G. Kim, and M. K. Skinner, “Expression and action of kit ligand/stem cell factor in normal human and bovine ovarian surface epithelium and ovarian cancer,” Biology of Reproduction, vol. 62, no. 6, pp. 1600–1609, 2000. View at Google Scholar · View at Scopus
  15. P. M. Motta and S. Makabe, “Germ cells in the ovarian surface during fetal development in humans. A three-dimensional microanatomical study by scanning and transmission electron microscopy,” Journal of Submicroscopic Cytology, vol. 18, no. 2, pp. 271–290, 1986. View at Google Scholar · View at Scopus
  16. P. M. Motta and S. Makabe, “Development of the ovarian surface and associated germ cells in the human fetus. A correlated study by scanning and transmission electron microscopy,” Cell and Tissue Research, vol. 226, no. 3, pp. 493–510, 1982. View at Google Scholar · View at Scopus
  17. P. M. Motta and S. Makabe, “Elimination of germ cells during differentiation of the human ovary: an electron microscopic study,” European Journal of Obstetrics Gynecology and Reproductive Biology, vol. 22, no. 5-6, pp. 271–286, 1986. View at Google Scholar · View at Scopus
  18. W. Waldeyer, Ein Beitrag zur Anatomie und Entwicklungsgeschichte der Sexualorgane, Engelmann, Leipzig, Germany, 1870.
  19. H. M. Kingery, “Oogenesis in the white mouse,” Journal of Morphology, vol. 30, pp. 261–315, 1917. View at Google Scholar
  20. A. Allen, “Ovogenesis during sexual maturity,” American Journal of Anatomy, vol. 31, pp. 439–481, 1923. View at Google Scholar
  21. H. M. Evans and O. Swezy, “Ovogenesis and the normal follicular cycle in adult mammalia,” Memorial of the University of California, vol. 9, pp. 119–224, 1931. View at Google Scholar
  22. A. Bukovsky, M. Svetlikova, and M. R. Caudle, “Oogenesis in cultures derived from adult human ovaries,” Reproductive Biology and Endocrinology, vol. 3, article 17, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. 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
  24. I. Virant-Klun, P. Rozman, 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. 7, p. 1109, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Virant-Klun and T. Skutella, “Stem cells in aged mammalian ovaries,” Aging, vol. 2, no. 1, pp. 3–6, 2010. View at Google Scholar · View at Scopus
  26. 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. 8, pp. 1451–1464, 2011. View at Publisher · View at Google Scholar
  27. D. Goswami and G. S. Conway, “Premature ovarian failure,” Human Reproduction Update, vol. 11, no. 4, pp. 391–410, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. J. P. Liu and H. Li, “Telomerase in the ovary,” Reproduction, vol. 140, no. 2, pp. 215–222, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Spanel-Borowski, “Footmarks of innate immunity in the ovary and cytokeratin-positive cells as potential dendritic cells,” Advances in Anatomy Embryology and Cell Biology, vol. 209, pp. 1–126, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Löffler, L. C. Horn, W. Weber, and K. Spanel-Borowski, “The transient disappearance of cytokeratin in human fetal and adult ovaries,” Anatomy and Embryology, vol. 201, no. 3, pp. 207–215, 2000. View at Google Scholar · View at Scopus
  31. H. Serke, C. Vilser, M. Nowicki et al., “Granulosa cell subtypes respond by autophagy or cell death to oxLDL-dependent activation of the oxidized lipoprotein receptor 1 and toll-like 4 receptor,” Autophagy, vol. 5, no. 7, pp. 991–1003, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. H. H. Ortega, N. R. Salvetti, L. A. Müller et al., “Characterization of cytoskeletal proteins in follicular structures of cows with cystic ovarian disease,” Journal of Comparative Pathology, vol. 136, no. 4, pp. 222–230, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Z. Ratajczak, E. K. Zuba-Surma, M. Wysoczynski, J. Ratajczak, and M. Kucia, “Very small embryonic-like stem cells: characterization, developmental origin, and biological significance,” Experimental Hematology, vol. 36, no. 6, pp. 742–751, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Z. Ratajczak, E. K. Zuba-Surma, D. M. Shin, J. Ratajczak, and M. Kucia, “Very small embryonic-like (VSEL) stem cells in adult organs and their potential role in rejuvenation of tissues and longevity,” Experimental Gerontology, vol. 43, no. 11, pp. 1009–1017, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Z. Ratajczak, M. Kucia, J. Ratajczak, and E. K. Zuba-Surma, “A multi-instrumental approach to identify and purify very small embryonic like stem cells (VSELs) from adult tissues,” Micron, vol. 40, no. 3, pp. 386–393, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. W. Wojakowski, M. Tendera, M. Kucia et al., “Cardiomyocyte differentiation of bone marrow-derived Oct-4 +CXCR4+SSEA-1+ very small embryonic-like stem cells,” International Journal of Oncology, vol. 37, no. 2, pp. 237–247, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. D. M. Shin, R. Liu, I. Klich et al., “Molecular signature of adult bone marrow-purified very small embryonic-like stem cells supports their developmental epiblast/germ line origin,” Leukemia, vol. 24, no. 8, pp. 1450–1461, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. V. M. Y. Ding, P. J. Boersema, L. Y. Foong et al., “Tyrosine phosphorylation profiling in FGF-2 stimulated human embryonic stem cells,” PLoS ONE, vol. 6, no. 3, article e17538, 2011. View at Publisher · View at Google Scholar
  39. L. R. Nelson and S. E. Bulun, “Estrogen production and action,” Journal of the American Academy of Dermatology, vol. 45, no. 3, supplement, pp. S116–S124, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. 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
  41. I. J. M. Duijkers, W. N. P. Willemsen, H. M. G. Hollanders, C. J. C. M. Hamilton, C. M. G. 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 Google Scholar · View at Scopus
  42. 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 Google Scholar · View at Scopus
  43. 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
  44. 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
  45. K. Ko, P. Reinhardt, N. Tapia et al., “Brief report: evaluating the potential of putative pluripotent cells derived from human testis,” Stem Cells, vol. 29, no. 8, pp. 1304–1309, 2011. View at Publisher · View at Google Scholar
  46. N. Tapia, M. J. Araúzo-Bravo, K. Ko, and H. R. Schöler, “Concise review: challenging the pluripotency of human testis-derived ESC-like cells,” Stem Cells, vol. 29, no. 8, pp. 1165–1169, 2011. View at Publisher · View at Google Scholar
  47. U. Riekstina, I. Cakstina, V. Parfejevs et al., “Embryonic stem cell marker expression pattern in human mesenchymal stem cells derived from bone marrow, adipose tissue, heart and dermis,” Stem Cell Reviews and Reports, vol. 5, no. 4, pp. 378–386, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Kuroda, M. Kitada, S. Wakao et al., “Unique multipotent cells in adult human mesenchymal cell populations,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 19, pp. 8639–8643, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. O. Trubiani, S. F. Zalzal, R. Paganelli et al., “Expression profile of the embryonic markers nanog, OCT-4, SSEA-1, SSEA-4, and Frizzled-9 receptor in human periodontal ligament mesenchymal stem cells,” Journal of Cellular Physiology, vol. 225, no. 1, pp. 123–131, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. 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
  51. 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
  52. 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