Multipotent mesenchymal stem cells of desquamated endometrium: Isolation, characterization, and application as a feeder layer for maintenance of human embryonic stem cells

Cell and Tissue Biology

Volumn 6, Issue 1, 2012, Pages 1-11

  Zemelko, V I ^a   Grinchuk, T M ^a   Domnina, A P ^a   Artzibasheva, I V ^a   Zenin, V V ^a   Kirsanov, A A ^c   Bichevaia, N K ^c   Korsak, V S ^c   Nikolsky, N N ^a,b  

^a INSTITUTE OF CYTOLOGY   (Russian Federation)

^b PETER THE GREAT ST PETERSBURG POLYTECHNIC UNIVERSITY   (Russian Federation)

^c International Center of Reproductive Medicine   (Russian Federation)

Author keywords

differentiation; feeder culture; human embryonic stem cells; human mesenchymal stem cells of endometrium; menstrual blood; multipotency

Indexed keywords

ANIMALIA;

EID: 84857387508     PISSN: 1990519X     EISSN: 19905203     Source Type: Journal    
DOI: 10.1134/S1990519X12010129     Document Type: Article

References (50)

1. Blondheim, N. R., Levy, Y. S., Ben-Zur, T., Burshtein, A., Cherlow, T., Kan, I., Barzilai, R., Bahat-Stromza, M., Barhum, Y., Bulvik, S., Melamed, E., and Offen, D., Human Mesenchymal Stem Cells Express Neural Genes, Suggesting a Neural Predisposition, Stem Cells Dev., 2006, vol. 15, pp. 141-164.
2. Borlongan, C. V., Kaneko, Y., Maki, M., Yu, S. J., Ali, M., Allickson, J. G., Sanberg, C. D., Kuzmin-Nichols, N., and Sanberg, P. R., Menstrual Blood Cells Display Stem Cell-Like Phenotypic Markers and Exert Neuroprotection Following Transplantation in Experimental Stroke, Stem Cells Dev., 2010, vol. 19, pp. 439-452.
3. Carpenter, M. K., Rosler, E. S., Gregory, J., Fisk, J. G., Brandenberger, R., Ares, X., Miura, T., Lucero, M., and Rao, M. S., Properties of Four Human Embryonic Stem Cells Lines Maintained in a Feeder-Free Culture System, Dev. Dynam., 2004, vol. 229, pp. 243-258.
4. Challen, G. A., and Little, M., A Side Order of Stem Cells: The SP Phenotype, Stem Cells, 2006, vol. 24, pp. 3-12.
5. Chen, L., He, D. M., and Zhang, Y., The Differentiation of Human Placenta-Derived Mesenchymal Stem Cells into Dopaminergic Cells in vitro, Cell. Mol. Biol. Lett., 2009, vol. 14, pp. 528-536.
6. Cho, N. H., Park, Y. K., Kim, Y. T., Yang, H., and Kim, S. K., Lifetime Expression of Stem Cell Markers in the Uterine Endometrium, Fertil. Steril., 2004, vol. 81, pp. 403-407.
7. Cui, C. H., Uyama, T., Miyado, K., Terai, M., Kyo, S., Kiyono, T., and Umezawa, A., Menstrual Blood-Derived Cells Confer Human Dystrophin Expression in the Murine Model of Duchenne Muscular Dystrophy via Cell Fusion and Myogenic Transdifferentiation, Mol. Biol. Cell, 2007, vol. 18, pp. 1586-1594.
8. De, Coppi, P., Bartsch, G., Jr., Siddiqui, M. M., Xu, T., Santos, C. C., Perin, L., Mostoslavsky, G., Serre, A. C., Snyder, E. Y., Yoo, J. J., Furth, M. E., Soker, S., and Atala, A., Isolation of Amniotic Stem Cell Lines with Potential for Therapy, Nat. Biotechnol., 2007, vol. 25, pp. 100-106.
9. Friedenstein, A. J., Petrakova, K. V., Kurolesova, A. I., and Frolova, G. P., Heterotopic of Bone Marrow. Analysis of Precursor Cells for Osteogenic and Hematopoietic Tissues, Transplantation, 1968, vol. 6, pp. 230-247.
10. Gang, E. J., Bosnakovski, D., Figueiredo, C. A., Visser, J. W., and Perlingeiro, R. C., SSEA-4 Identifies Mesenchymal Stem Cells from Bone Marrow, Blood, 2007, vol. 109, pp. 1743-1751.
11. Gargett, C. E., and Masuda, H., Adult Stem Cells in the Endometrium, Mol. Hum. Reprod., 2010, vol. 16, pp. 818-834.
12. Gargett, C. E., Identification and Characterization of Human Endometrial Stem/Progenitor Cells, Aust. Nz J. Obstet. Gynaecol., 2006, vol. 46, pp. 250-253.
13. Goodell, M. A., Brose, K., Paradis, G., Conner, A. S., and Mulligan, R. C., Isolation and Functional Properties of Murine Hematopoietic Stem Cells that Are Replicating in vivo, J. Exp. Med., 1996, vol. 183, pp. 1797-1806.
14. Han, X., Meng, X., Yin, Z., Rogers, A., Zhong, J., Rillema, P., Jackson, J. A., Ichim, T. E., Minev, B., Carrier, E., Patel, A. N., Murphy, M. P., Min, W. P., and Riordan, N. H., Inhibition of Intracranial Glioma Growth by Endometrial Regenerative Cells, Cell Cycle, 2009, vol. 8, pp. 606-610.
15. Harris, D. T., Badowski, M., Ahmad, N., and Gaballa, M. A., The Potential of Cord Blood Stem Cells for Use in Regenerative Medicine, Expert. Opin. Biol. Ther., 2007, vol. 7, pp. 1311-1322.
16. Hida, N., Nishiyama, N., Miyoshi, S., Kira, S., Segawa, K., Uyama, T., Mori, T., Miyado, K., and Ikegami, Y., Novel Cardiac Precursor-Like Cells from Human Menstrual Blood-Derived Mesenchymal Cells, Stem Cells, 2008, vol. 26, pp. 1695-1704.
17. Hoffman, L. M., and Carpenter, M. K., Human Embryonic Stem Cell Stability, Stem Cell Rev., 2005, vol. 1, pp. 139-144.
18. Husein, K. S., and Thiemermann, C., Mesenchymal Stromal Cells: Current Understanding and Clinical Status, Stem Cells, 2010, vol. 28, pp. 585-596.
19. Itskovitz-Eldor, J., Schuldiner, M., Karsenti, D., Eden, A., Yanuka, O., Amit, M., Soreq, H., and Benvenisty, N., Differentiation of Human Embryonic Stem Cells into Embryoid Bodies Comprising the Three Embryonic Germ Layers, Mol. Med., 2000, vol. 6, pp. 88-95.
20. Jori, F. P., Napolitano, M. A., Melone, M. A., Cipollaro, M., Cascino, A., Altucci, L., Peluso, G., Giordano, A., and Galderisi, U., Molecular Pathways Involved in Neural in vitro Differentiation of Marrow Stromal Stem Cells, J. Cell Biochem., 2005, vol. 94, pp. 645-655.
21. Kato, K., Yoshimoto, M., Kato, K., Adachi, S., Yamayoshi, A., Arima, T., Asanoma, K., Kyo, S., Nakahata, T., and Wake, N., Characterization of Side-Population Cells in Human Normal Endometrium, Hum. Reprod., 2007, vol. 22, pp. 1214-1223.
22. Kearns, M., and Lala, P. K., Bone Marrow Origin of Decidual Cell Precursors in the Pseudopregnant Mouse Uterus, J. Exp. Med., 1982, vol. 155, pp. 1537-1554.
23. Kozhukharova, I. V., Fridlyanskaya, I. I., Kovaleva, Z. V., Pugovkina, N. A., Alekseenko, L. L., Zenin, V. V., Ivantsov, K. M., Leont'eva, O. K., Grinchuk, T. M., and Nikol'sky, N. N., Novel Human Embryonic Stem Cell Lines C612 and C910, Tsitologiia, 2009, vol. 51, no. 7, pp. 551-558.
24. Lee, J. B., Lee, J. E., Park, J. H., Kim, S. J., Kim, M. K., Roh, S. I., and Yoon, H. S., Establishment and Maintenance of Human Embryonic Stem Cell Lines on Human Feeder Cells Derived from Uterine Endometrium under Serum-Free Condition, Biol. Reprod., 2005, vol. 72, pp. 42-49.
25. Lees, J. G., Lim, S. A., Croll, T., Williams, G., Lui, S., Cooper-White, J., McQuade, L. R., Mathiyalagan, B., and Tuch, B. E., Transplantation of 3D Scaffolds Seeded with Human Embryonic Stem Cells: Biological Features of Surrogate Tissue and Teratoma-Forming Potential, Regen. Med., 2007, vol. 2, pp. 289-300.
26. Ludwig, T. E., Levenstein, M. E., Jones, J. M., Berggren, W. T., Mitchen, E. R., Frane, J. L., Crandall, L. J., Daigh, C. A., Conard, K. R., Piekarczyk, M. S., Llanas, R. A., and Thomson, J. A., Derivation of Human Embryonic Stem Cells in Defined Conditions, Nat. Biotechnol., 2006, vol. 24, pp. 185-187.
27. Masuda, H., Matsuzaki, Y., Hiratsu, E., Ono, M., Nagashima, T., Kajitani, T., Arase, T., Oda, H., Uchida, H., Asada, H., Ito, M., Yoshimura, Y., Maruyama, T., and Okano, H., Stem Cell-Like Properties of the Endometrial Side Population: Implication in Endometrial Regeneration, PLoS One, 2010, vol. 5, p. e10387.
28. Meng, X., Ichim, T. E., Zhong, J., Rogers, A., Yin, Z., Jackson, J., Wang, H., Ge, W., Bogin, V., Chan, K. W., Thébaud, B., and Riordan, N. H., Endometrial Regenerative Cells: A Novel Stem Cell Population, J. Transl. Med., 2007, vol. 5, pp. 57-66.
29. Murphy, M. P., Wang, H., Patel, A. N., Kambhampati, S., Angle, N., Chan, K., Marleau, A. M., Pyszniak, A., Carrier, E., and Ichim, T. E., et al., Allogeneic Endometrial Regenerative Cells: An 'off the Shelf Solution' for Critical Limb Ischemia? J. Transl. Med., 2008, vol. 6, pp. 45-52.
30. Musina, R. A., Bekchanova, E. S., Belyavsky, A. V., and Sukhikh, G. T., Differentiation Potential of Mesenchymal Stem Cells of Different Origin, Klet. Tekhn. Biol. Med., 2006, vol. 1, pp. 39-43.
31. Musina, R. A., Belyavsky, A. V., Tarusova, O. V., Solovyeva, E. V., and Sukhikh, G. T., Endometrial Mesenchymal Stem Cells Obtained from Menstrual Blood, Klet. Tekhn. Biol. Med., 2008, vol. 2, pp. 110-114.
32. Padykula, H. A., Coles, L. G., Okulicz, W. C., Rapaport, S. I., McCracken, J. A., King, N. W., Jr., Longcope, C., and Kaiserman-Abramof, I. R., The Basalis of the Primate Endometrium: A Bifunctional Germinal Compartment, Biol. Reprod., 1989, vol. 40, pp. 681-690.
33. Padykula, H. A., Regeneration in the Primate Uterus: The Role of Stem Cells, Ann. N. Y. Acad. Sci., 1991, vol. 622, pp. 47-56.
34. Park, K. R., Inoue, T., Ueda, M., Hirano, T., Higuchi, T., Maeda, M., Konishi, I., Fujiwara, H., and Fujii, S., CD9 Is Expressed on Human Endometrial Epithelial Cells in Association with Integrins a6, a3 and B1, Mol. Human Reprod., 2000, vol. 6, pp. 252-257.
35. Parker, A. M., and Katz, A. J., Adipose-Derived Stem Cells for the Regeneration of Damaged Tissues, Expert. Opin. Bio. Ther., 2006, vol. 6, pp. 567-578.
36. Patel, A. N., Park, E., Kuzman, M., Benetti, F., Silva, F. J., and Allickson, J. G., Multipotent Menstrual Blood Stromal Stem Cells: Isolation, Characterization, and Differentiation, Cell Transplant., 2008, vol. 17, pp. 303-311.
37. Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S., and Marshak, D. R., Multilineage Potential of Adult Human Mesenchymal Stem Cells, Science, 1999, vol. 284, pp. 143-147.
38. Prianishnikov, V. A., On the Concept of Stem Cell and a Model of Functional Morphological Structure of the Endometrium, Contraception, 1978, vol. 18, pp. 213-223.
39. Schwab, K. E., and Gargett, C. E., Co-Expression of Two Peri-Vascular Cell Markers Isolates Mesenchymal Stem-Like Cells from Human Endometrium, Hum. Reprod., 2007, vol. 22, pp. 2903-2911.
40. Seli, E., Senturk, L., Bahtiyar, O. M., Kayisli, U. A., and Arici, A., Expression of Aminopeptidase N in Human Endometrium and Regulation of Its Activity by Estrogen, Fertil. Steril., 2001, vol. 75, pp. 1172-1176.
41. Smith, J. R., Pochampally, R., Perry, A., Shu-Ching, Hsu, and Prockop, D. J., Isolation of a Highly Clonogenic and Multipotential Subfraction of Adult Stem Cells from Bone Marrow Stroma, Stem Cells, 2004, vol. 22, pp. 823-837.
42. Swijnenburg, R. J., Tanaka, M., Vogel, H., Baker, J., Kofidis, T., Gunawan, F., Lebl, D. R., Caffarelli, A. D., De Bruin, J. L., Fedoseyeva, E. V., and Robbins, R., Embryonic Stem Cell Immunogenicity Increases upon Differentiation after Transplantation into Ischemic Myocardium, Circulation, 2005, vol. 112, pp. 166-172.
43. Taylor, H. S., Endometrial Cells Derived from Donor Stem Cells in Bone Marrow Transplant Recipients, J. Amer. Med. Assoc., 2004, vol. 292, pp. 81-85.
44. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S., and Jones, J. M., Embryonic Stem Cell Lines Derived from Human Blastocysts, Science, 1998, vol. 282, pp. 1145-1147.
45. Toyoda, M., Cui, C., and Umezawa, A., Myogenic Transdifferentiation of Menstrual Blood-Derived Cells, Acta Myol., 2007, vol. 26, pp. 176-178.
46. Trzaska, K. A., Kuzhikandathil, E. V., and Rameshwar, P., Specification of a Dopaminergic Phenotype from Adult Human Mesenchymal Stem Cells, Stem Cells, 2007, vol. 25, pp. 2797-2808.
47. Wolff, E. F., Gao, X. B., Yao, K. V., Andrews, Z. B., Du, H., Elsworth, J. D., and Taylor, H. S., Endometrial Stem Cell Transplantation Restores Dopamine Production in a Parkinson's Disease Model, J. Cell. Mol. Med., 2011, vol. 15, pp. 747-755.
48. Woodbury, D., Reynolds, A., and Black, I. B., Adult Bone Marrow Stromal Stem Cells Express Germline, Ectodermal, Endodermal and Mesodermal Genes Prior to Neurogenesis, J. Neurosci. Res., 2002, vol. 96, pp. 908-917.
49. Zhong, Z., Patel, A. N., Ichim, T. E., Riordan, N. H., Wang, H., Min, W. P., Woods, E. J., Reid, M., Mansilla, E., Marin, G. H., Drago, H., Murphy, M. P., and Minev, B., Feasibility Investigation of Allogeneic Endometrial Regenerative Cells, J. Transl. Med., 2009, vol. 7, pp. 15-21.
50. Zwart, I., Hill, A. J., Girdlestone, J., Manca, M. F., Navarrete, R., Navarrete, C., and Jen, L. S., Analysis of Neural Potential of Human Umbilical Cord Blood-Derived Multipotent Mesenchymal Stem Cells in Response to a Range of Neurogenic Stimuli, J. Neurosci. Res., 2008, vol. 86, pp. 1902-1915.