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BioMed Research International
Volume 2013 (2013), Article ID 690415, 15 pages
http://dx.doi.org/10.1155/2013/690415
Research Article

Isolation of Small SSEA-4-Positive Putative Stem Cells from the Ovarian Surface Epithelium of Adult Human Ovaries by Two Different Methods

1Department of Obstetrics and Gynecology, University Medical Centre Ljubljana, Slajmerjeva 3, 1000 Ljubljana, Slovenia
2Institute for Anatomy and Cell Biology, University of Heidelberg, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany
3National Institute of Biology, Vecna Pot 111, 1000 Ljubljana, Slovenia
4BioSistemika, Tehnoloski Park 24, 1000 Ljubljana, Slovenia

Received 13 August 2012; Accepted 27 December 2012

Academic Editor: Leon Spicer

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. 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–e9, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. 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
  3. 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
  4. 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
  5. I. Virant-Klun, N. Zech, P. Rožman 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
  6. 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
  7. 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.
  8. S. Parte, D. Bhartiya, and V. Daithankar, “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
  9. 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
  10. K. Ivarsson, K. Sundfeldt, M. Brännström, and P. O. Janson, “Production of steroids by human ovarian surface epithelial cells in culture: possible role of progesterone as growth inhibitor,” Gynecologic Oncology, vol. 82, no. 1, pp. 116–121, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Bukovsky, “Ovarian stem cell niche and follicular renewal in mammals,” Anatomical Record, vol. 294, no. 8, pp. 1284–1306, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. R. Sottocornola and C. Lo Celso, “Dormancy in the stem cell niche,” Stem Cell Research and Therapy, vol. 3, no. 2, article 10, 2012. View at Publisher · View at Google Scholar
  13. O. Adewumi, L. Ahrlund-Richter, P. W. Andrews et al., et al., “Characterization of human embryonic stem cell lines by the International Stem Cell Initiative,” Nature Biotechnology, vol. 25, no. 7, pp. 803–816, 2007. View at Publisher · View at Google Scholar
  14. M. Richards, S. P. Tan, J. H. Tan, W. K. Chan, and A. Bongso, “The transcriptome profile of human embryonic stem cells as defined by SAGE,” Stem Cells, vol. 22, no. 1, pp. 51–64, 2004. View at Scopus
  15. M. Kucia, R. Reca, F. R. Campbell et al., “A population of very small embryonic-like (VSEL) CXCR4+ SSEA-1+Oct-4+ stem cells identified in adult bone marrow,” Leukemia, vol. 20, no. 5, pp. 857–869, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Kucia, E. Zuba-Surma, M. Wysoczynski et al., “Physiological and pathological consequences of identification of very small embryonic like (VSEL) stem cells in adult bone marrow,” Journal of Physiology and Pharmacology, vol. 57, no. 5, pp. 5–18, 2006. View at Scopus
  17. M. Kucia, M. Halasa, M. Wysoczynski et al., “Morphological and molecular characterization of novel population of CXCR4+ SSEA-4+ Oct-4+ very small embryonic-like cells purified from human cord blood - Preliminary report,” Leukemia, vol. 21, no. 2, pp. 297–303, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. C. McGuckin, M. Jurga, H. Ali, M. Strbad, and N. Forraz, “Culture of embryonic-like stem cells from human umbilical cord blood and onward differentiation to neural cells in vitro,” Nature Protocols, vol. 3, no. 6, pp. 1046–1055, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Halasa, M. Baskiewicz-Masiuk, E. Dabkowska, and B. Machalinski, “An efficient two-step method to purify very small embryonic-like (VSEL) stem cells from umbilical cord blood (UCB),” Folia Histochemica et Cytobiologica, vol. 46, no. 2, pp. 239–243, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Sauerzweig, T. Munsch, V. Leßmann, K. G. Reymann, and H. Braun, “A population of serumdeprivation-induced bone marrow stem cells (SD-BMSC) expresses marker typical for embryonic and neural stem cells,” Experimental Cell Research, vol. 315, no. 1, pp. 50–66, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Pang, Y. Zhang, X. Pan et al., “Embryonic-like stem cell derived from adult bone marrow: immature morphology, cell surface markers, ultramicrostructure and differentiation into multinucleated fibers in vitro,” Cellular and Molecular Biology, vol. 56, supplement, pp. OL1276–OL1285, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. H. Sovalat, M. Scrofani, A. Eidenschenk, S. Pasquet, V. Rimelen, and P. Hénon, “Identification and isolation from either adult human bone marrow or G-CSF-mobilized peripheral blood of CD34+/CD133+/CXCR4+/Lin-CD45-cells, featuring morphological, molecular, and phenotypic characteristics of very small embryonic-like (VSEL) stem cells,” Experimental Hematology, vol. 39, no. 4, pp. 495–505, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. S. A. Gharib, A. Khalyfa, M. J. Kucia et al., “Transcriptional landscape of bone marrow-derived very small embryonic-like stem cells during hypoxia,” Respiratory Research, vol. 12, article 63, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Bhartiya, A. Shaikh, P. Nagvenkar et al., “Very small embryonic-like stem cells with maximum regenerative potential get discarded during cord blood banking and bone marrow processing for autologous stem cell therapy,” Stem Cells and Development, vol. 21, no. 1, pp. 1–6, 2012. View at Publisher · View at Google Scholar
  25. S. Bao, H. G. Leitch, A. Gillich et al., “The germ cell determinant Blimp1 is not required for derivation of pluripotent stem cells,” Cell Stem Cell, vol. 11, no. 1, pp. 110–117, 2012. View at Publisher · View at Google Scholar
  26. Y. Ohinata, B. Payer, D. O'Carroll et al., “Blimp1 is a critical determinant of the germ cell lineage in mice,” Nature, vol. 436, no. 7048, pp. 207–213, 2005. View at Publisher · View at Google Scholar
  27. M. Coussens, Y. Yamazaki, S. Moisyadi, R. Suganuma, R. Yanagimachi, and R. Allsopp, “Regulation and effects of modulation of telomerase reverse transcriptase expression in primordial germ cells during development,” Biology of Reproduction, vol. 75, no. 5, pp. 785–791, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. W. Shen, B.-W. Park, D. Toms, and J. Li, “Midkine promotes proliferation of primordial germ cells by inhibiting the expression of the deleted in azoospermia-like gene,” Endocrinology, vol. 153, no. 7, pp. 3482–3492, 2012. View at Publisher · View at Google Scholar
  29. J. J. Vincent, Z. Li, X. Liu et al., “Single cell analysis facilitates staging of Blimp1-dependent primordial germ cells derived from mouse embryonic stem cells,” PLoS One, vol. 6, no. 12, Article ID e28960, 2011. View at Publisher · View at Google Scholar
  30. Y. Atlasi, S. J. Mowla, S. A. M. Ziaee, P. J. Gokhale, and P. W. Andrews, “OCT4 spliced variants are differentially expressed in human pluripotent and nonpluripotent cells,” Stem Cells, vol. 26, no. 12, pp. 3068–3074, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. R.-M. Törmälä, M. Jääskeläinen, J. Lakkakorpi, A. Liakka, J. S. Tapanainen, and T. E. Vaskivuo, “Zona pellucida components are present in human fetal ovary before follicle formation,” Molecular and Cellular Endocrinology, vol. 289, no. 1-2, pp. 10–15, 2008. View at Publisher · View at Google Scholar
  32. L. Yuan, J. G. Liu, M. R. Hoja, J. Wilbertz, K. Nordqvist, and C. Höög, “Female germ cell aneuploidy and embryo death in mice lacking the meiosis-specific protein SCP3,” Science, vol. 296, no. 5570, pp. 1115–1118, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Tanikawa, T. Harada, M. Mitsunari, Y. Onohara, T. Iwabe, and N. Terakawa, “Expression of c-kit messenger ribonucleic acid in human oocyte and presence of soluble c-kit in follicular fluid,” Journal of Clinical Endocrinology and Metabolism, vol. 83, no. 4, pp. 1239–1242, 1998. View at Publisher · View at Google Scholar · View at Scopus
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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