Detection, characterization, and spontaneous differentiation in vitro of very small embryonic-like putative stem cells in adult mammalian ovary

Stem Cells and Development

Volumn 20, Issue 8, 2011, Pages 1451-1464

  Parte, Seema ^a   Bhartiya, Deepa ^a   Telang, Jyoti ^a   Daithankar, Vinita ^a   Salvi, Vinita ^b   Zaveri, Kusum ^c   Hinduja, Indira ^c  

^a NATIONAL INSTITUTE FOR RESEARCH IN REPRODUCTIVE HEALTH   (India)

^b KEM HOSPITAL   (India)

^c Inkus IVF Centre   (India)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH DIFFERENTIATION FACTOR 9; OCTAMER TRANSCRIPTION FACTOR 4; OCTAMER TRANSCRIPTION FACTOR 4 A; STAGE SPECIFIC EMBRYO ANTIGEN 4; STAT3 PROTEIN; STEM CELL FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL SIZE; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOPLASM; EMBRYO CELL; EMBRYOID BODY; EMBRYONIC STEM CELL; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM; ERYTHROCYTE; EXPERIMENTAL MONKEY; EXPERIMENTAL RABBIT; FEMALE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN TISSUE; MENOPAUSE; NERVE CELL; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OVARIAN SURFACE EPITHELIUM; OVARY; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PUTATIVE STEM CELL; SHEEP; STEM CELL; RETRACTION NOTICE;

ADULT; ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; FEMALE; HAPLORHINI; HUMANS; MENOPAUSE; MIDDLE AGED; OCTAMER TRANSCRIPTION FACTOR-3; OOCYTES; OOGENESIS; OVARY; RABBITS; SHEEP; STAGE-SPECIFIC EMBRYONIC ANTIGENS;

MAMMALIA; ORYCTOLAGUS CUNICULUS; OVIS ARIES;

EID: 80051499572     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2010.0461     Document Type: Article

References (57)

1. Jemal A, A Thomas, T Murray and M Thun. (2002). Cancer statistics, 2002. CA Cancer J Clin 52:23-47. (Pubitemid 34110469)
2. Auersperg N, AST Wong, KC Choi, SK Kang and PCK Leung. (2001). Ovarian surface epithelium: Biology, endocrinology and pathology. Endocr Rev 22:255-288. (Pubitemid 32458162)
3. Oktem O and K Oktay. (2009). Current knowledge in the renewal capability of germ cells in the adult ovary. Birth Defects Res 87:90-95.
4. TillyJL and EE Telfer. (2009). Purification of germline stem cells from adult mammalian ovaries: A step closer towards control of the female biological clock. Mol Hum Reprod 15:393-398.
5. Bukovsky A. (2010). How can female germline stem cells contribute to the physiological neo-oogenesis in mammals and why menopause occurs? Microsc Microanal 16:1-9.
6. Virant-Klun I and T Skutella. (2010). Stem cells in aged mammalian ovaries. Aging 2:3-6.
7. Felici M De. (2010). Germ stem cells in the mammalian adult ovary: Considerations by a fan of the primordial germ cells. Mol Hum Reprod 16:632-636.
8. Kirilly D and T Xie. (2007). The Drosophila ovary: An active stem cell community. Cell Res 17:15-25. (Pubitemid 46096420)
9. Pearl R and WF Schoppe. (1921). Studies on the physiology of reproduction in the domestic fowl. J Exp Zool 34:101-118.
10. Underwood JL, RS Hestand III and BZ Thompson. (1986). Gonad regeneration in grass carp following bilateral gonodectomy. Prog Fish Cult 48:54-56.
11. Draper BW, CM McCallum and CB Moens. (2007). Nanos1 is required to maintain oocyte production in adult zebrafish. Dev Biol 305:589-598. (Pubitemid 46705412)
12. Johnson J, J Canning, T Kaneko, JK Pru and JL Tilly. (2004). Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 428:145-150. (Pubitemid 38374304)
13. Niikura Y, T Niikura and JL Tilly. (2009). Aged mouse ovaries possess rare premeiotic germ cells that can generate oocytes following transplantation into a young host environment. Aging 1:971-978.
14. Johnson J, J Bagley, M Skaznik-Wikiel, H-J Lee, GB Adams, Y Niikura, KS Tschudy, JC Tilly, ML Cortes, R Forkert, T Spitzer, J Iacomini, DT Scadden and JL Tilly. (2005). Oocyte generation in adult mammalian ovaries by putative germ cells from bone marrow and peripheral blood. Cell 122:303-315. (Pubitemid 41032992)
15. Zou K, Z Yuan, Z Yang, H Luo, K Sun, L Zhou, J Xiang, L Shi, Q Yu, Y Zhang, R Hou and J Wu. (2009). Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol 5:631-636.
16. Szotek PP, HL Chang, K Brennand, A Fujino, R Pieretti-Vanmarcke, CL Celso, D Dombkowski, F Preffer, KS Cohen, J Teixeira and PK Donahoe. (2008). Normal ovarian surface epithelial label-retaining cells exhibit stem/progenitor cell characteristics. PNAS 105:12469-12473.
17. Pacchiarotti J, C Maki, T Ramos, J Marh, K Howerton, J Wong, J Pham, S Anorve, YC Chow and F Izadyar. (2010). Differentiation potential of germ line stem cells derived from the postnatal mouse ovary. Differentiation 79:159-170.
18. Gong SP, ST Lee, EJ Lee, DY Kim, G Lee, SG Chi, BK Ryu, CH Lee, KE Yum, HJ Lee, JY Han, JL Tilly and JM Lim. (2010). Embryonic stem cell-like cells established by culture of adult ovarian cells in mice. Fertil Steril 93:2594-2601.
19. Gong SP, JH Lee and JM Lim. (2010). Derivation of histocompatible stem cells from ovarian tissue. J Reprod Dev 56:481-494.
20. Bukovsky A, M Svetlikova and MR Caudle. (2005). Oogenesis in cultures derived from adult human ovaries. Reprod Biol Endocrinol 3:17-30.
21. Virant-Klun I, Z Nicolas, P Rozman, A Vogler, B Cvjeticanin, P Klemenc, E Malicev and H Meden-Vrtovec. (2008). Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation 76:843-856.
22. Virant-Klun I, P Rozman, B Cvjeticanin, E Vrtacnik-Bokal, S Novakovic, T Rülicke, P Dovc and H Meden-Vrtovec. (2009). Parthenogenetic embryo-like structures in the human ovarian surface epithelium cell culture in postmenopausal women with no naturally present follicles and oocytes. Stem Cells Dev 18:137-149.
23. Tilly JL, Y Niikura and BR Rueda. (2009).The current status of evidence for and against postnatal oogenesis in mammals: A case of ovarian optimism versus pessimism? Biol Reprod 80:2-12.
24. Bukovsky A, MR Caudle, M Svetlikova and NB Upadhyaya. (2004). Origin of germ cells and formation of new primary follicles in adult human ovaries. Reprod Biol Endocrinol 28: 2-20.
25. Bukovsky A, M Svetlikova and MR Caudle. (2005). Oogenesis in cultures derived from adult human ovaries. Reprod Biol Endocrinol 3:17-30.
26. Kumar N, I Hinduja, P Nagvenkar, L Pillai, K Zaveri, L Mukadam, J Telang, S Desai, V Mangoli, R Mangoli, S Padgaonkar, G Kaur, C Puri and D Bhartiya. (2009). Derivation and characterization of two genetically unique human embryonic stem cell lines on in-house-derived human feeders. Stem Cells Dev 18:67-77.
27. Crowley TE, EM Kaine, M Yoshida, A Nandi and DJ Wolgemuth. (2002). Reproductive cycle regulation of nuclear import, euchromatic localization, and association with components of pol II mediator of a mammalian doublebromodomain protein. Mol Endocrinol 16:1727-1737. (Pubitemid 34828084)
28. Jasencakova Z, A Meister, J Walter, BM Turner and I Schubert. (2000). Histone H4 acetylation of euchromatin and heterochromatin is cell cycle dependent and correlated with replication rather than with transcription. Am Soc Plant Physiol 12:2087-2100. (Pubitemid 32053397)
29. Shin DM, R Liu, I Klich, J Ratajczak, M Kucia and MZ Ratajczak. (2010). Molecular characterization of isolated from murine adult tissues very small embryonic/epiblast like stem cells (VSELs). Mol Cells 29:533-538.
30. Kucia M, R Reca, FR Campbell, E Zuba-Surma, M Majka, J Ratajczak, MZ Ratajczak. (2006). A population of very small embryonic-like (VSEL) CXCR4 ( + ) SSEA-1( + ) Oct-4 + stem cells identified in adult bone marrow. Leukemia 20:857-869.
31. Ratajczak MZ, EK Zuba-Surma, J Ratajczak, M Wysoczynski and M Kucia. (2008). Very small embryonic like (VSEL) stem cells-characterization, developmental origin and biological significance. Exp Hematol 36:742-751. (Pubitemid 351637617)
32. Bhartiya D, S Kasiviswanathan, SK Unni, P Pethe, JV Dhabalia, S Patwardhan and HB Tongaonkar. (2010). Newer insights into pre-meiotic development of germ cells in adult human testis using Oct-4 as a stem cell marker. J Histochem Cytochem 58:1093-1106.
33. Li L and H Clevers. (2010). Coexistence of quiescent and active adult stem cells in mammals. Science 327:542-545.
34. Sha K and LA Boyer. (2009) The chromatin signature of pluripotent cells. In: StemBook. Jaenisch R, L Peter, eds. Massachusetts Institute of Technology, Cambridge, www stembook.org
35. Nayernia K, JH Lee, N Drusenheimer, J Nolte, G Wulf, R Dressel, J Gromoll andWEngel. (2006). Derivation ofmale germ cells from bone marrow stem cells. Lab Investig 86:654-663. (Pubitemid 43901663)
36. Lengner CJ, FD Camargo, K Hochedlinger, GG Welstead, S Zaidi, S Gokhale, HR Scholer, A Tomilin and R Jaenisch. (2007). Oct4 expression is not required for mouse somatic stem cell self-renewal. Cell Stem Cell 1:403-415. (Pubitemid 47506536)
37. Lengner CJ, GG Welstead and R Jaenisch. (2008). The pluripotency regulator Oct4. A role in somatic stem cells? Cell Cycle 7:725-728. (Pubitemid 351520033)
38. Shin DM, EK Zuba-Surma, W Wu, J Ratajczak, M Wysoczynski, MZ Ratajczak and M Kucia. (2009). Novel epigeneitc mechanisms that control pluripotency and quiescence of adult bone marrow-derived Oct4 + very small embryonic like stem cells. Leukemia 23:2042-2051.
39. Adewumi O, B Aflatoonian, L Ahrlund-Richter, M Amit, PW Andrews, G Beighton, et al. (2007). The international stem cell initiative characterization of human embryonic stem cell lines by the international stem cell initiative. Nat Biotechnol 25:803-816. (Pubitemid 47052190)
40. Shin DM, R Liu, I Klich, W Wu, J Ratajczak, M Kucia and MZ Ratajczak. (2010). Molecular signature of adult bone marrow-purified very small embryonic-like stem cells supports their developmental epiblast/germ line origin. Leukemia 24:1450-1461.
41. Ratajczak MZ, M Kucia, D-M Shin, L Rui, J Drukala, W Marlicz, J Ratajczak and EK Zuba-Surma. (2008). A unique population of mobile very small embryonic/epiblast like (VSEL) stem cells resides in adult tissues: Physiological and pathological consequences. Cell Ther Transplant 1: 36-43.
42. Felici M De. (2010). Germ stem cells in the mammalian adult ovary: Considerations by a fan of the primordial germ cells. Mol Hum Reprod 16:632-636.
43. Zuba-Surma EK, Y Guo, H Taher, SK Sanganalmath, G Hunt, RJ Vincent, M Kucia, A Abdel-Latif, XL Tang, MZ Ratajczak, B Dawn and R Bolli. (2010). Transplantation of expanded bone marrow-derived very small embryonic-like stem cells (VSEL-SCs) improves left ventricular function and remodeling after myocardial infarction. J Cell Mol Med. [Epub ahead of print] DOI: 10.1111/j.1582-4934.2010.01126.x
44. Huang Y, M Kucia, LR Hussain, Y Wen, H Xu, J Yan, MZ Ratajczak and ST Ildstad. (2010). Bone marrow transplantation temporarily improves pancreatic function in streptozotocin-induced diabetes: Potential involvement of very small embryonic-like cells. Transplantation 89:677-685.
45. Wojakowski W, M Tendera, M Kucia, E Zuba-Surma, E Paczkowska, J Ciosek, M Halasa, M Krol, M Kazmierski, P Buszman, A Ochala, J Ratajczak, B Machalinski and M Ratajczak. (2009). Mobilization of bone marrow derived Oct-4 + SSEA-4 + very small embryonic like stem cells in patients with acute myocardial infarction. J Am Coll Cardiol 53:1-9.
46. Abdel-Latif A, EK Zuba-Surma, KM Ziada, M Kucia, DA Cohen, AM Kaplan, G Van Zant, S Selim, SS Smyth and MZ Ratajczak. (2010). Evidence of mobilization of pluripotent stem cells into peripheral blood of patients with myocardial ischemia. Exp Hematol 38:1131-1142.e1.
47. Losordo DW and R Kishore. (2009). A big promise from the very small identification of circulating embryonic stem-like pluripotent cells in patients with acute myocardial infarction. J Am Coll Cardiol 53:10
48. Golestaneh N, M Kokkinaki, D Pant, J Jiang, D DeStefano, C Fernandez-Bueno, JD Rone, BR Haddad, GI Gallicano and MM Dym. (2009). Pluripotent stem cells derived from adult human testes. Stem Cells Dev 18:1115-1126.
49. Kanatsu-Shinohara M, M Takehashi and T Shinohara. (2008). Brief history, pitfalls and prospects of mammalian spermatogonial stem cell research. Cold Spring Harbor Symp Quant Biol 73:17-23.
50. Sadri-Ardekani H, SC Mizrak, SKM van Daalen, et al. (2009). Propagation of human spermatogonial stem cells in vitro. J Am Med Assoc 302:2127-2134.
51. Kruk PA and N Auersperg. (1992). Human ovarian surface epithelial cells are capable of physically restructuring extracellular matrix. Am J Obstet Gynecol 167:1437-1443.
52. Dyck HG, TC Hamilton, AK Godwin, HT Lynch, S Maines-Bandiera and N Auersperg. (1996). Autonomy of the epithelial phenotype in human ovarian surface epithelium: Changes with neoplastic progression and with a family history of ovarian cancer. Int J Cancer 69:429-436. (Pubitemid 27050516)
53. Nelson LR and SE Bulun. (2001). Estrogen production and action. J Am Acad Dermatol 45:S116-S124. (Pubitemid 32783340)
54. Motta PM, SA Nottola, S Makabe and R Heyn. (2000). Mitochondrial morphology in human fetal and adult female germ cells. Hum Rep 15:129-147.
55. Carlsson JL, MR Bakst and MA Ottinger. (1996). Developmental stages of primary oocytes in turkeys. Poult Sci 75:1569-1578. (Pubitemid 126454347)
56. Ahmed N, EW Thompson and MA Quinn. (2007). Epithelialmesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: An exception to the norm. J Cell Physiol 213:581-588. (Pubitemid 350058249)
57. Massasa E, XS Costa and HS Taylor. (2010). Failure of the stem cell niche rather than loss of oocyte stem cells in the aging ovary. Aging 2:1-2.