Skip to main content

Advertisement

Log in

Adult Human Adipose Tissue Contains Several Types of Multipotent Cells

  • Published:
Journal of Cardiovascular Translational Research Aims and scope Submit manuscript

Abstract

Multipotent mesenchymal stromal cells (MSCs) are a type of adult stem cells that can be easily isolated from various tissues and expanded in vitro. Many reports on their pluripotency and possible clinical applications have raised hopes and interest in MSCs. In an attempt to unify the terminology and the criteria to label a cell as MSC, in 2006 the International Society for Cellular Therapy (ISCT) proposed a standard set of rules to define the identity of these cells. However, MSCs are still extracted from different tissues, by diverse isolation protocols, are cultured and expanded in different media and conditions. All these variables may have profound effects on the selection of cell types and the composition of heterogeneous subpopulations, on the selective expansion of specific cell populations with totally different potentials and ergo, on the long-term fate of the cells upon in vitro culture. Therefore, specific molecular and cellular markers that identify MSCs subsets as well as standardization of expansion protocols for these cells are urgently needed. Here, we briefly discuss new useful markers and recent data supporting the rapidly emerging concept that many different types of progenitor cells are found in close association with blood vessels. This knowledge may promote the necessary technical improvements required to reduce variability and promote higher efficacy and safety when isolating and expanding these cells for therapeutic use. In the light of the discussed data, particularly the identification of new markers, and advances in the understanding of fundamental MSC biology, we also suggest a revision of the 2006 ISCT criteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Bailey, A. M., Kapur, S., & Katz, A. J. (2010). Characterization of adipose-derived stem cells: an update. Current Stem Cell Research & Therapy, 5(2), 95–102.

    Article  CAS  Google Scholar 

  2. Da Silva Meirelle, L., Caplan, A. I., & Nardi, N. B. (2008). In search of the in vivo identity of mesenchymal stem cells. Stem Cells, 26(9), 2287–2299.

    Article  Google Scholar 

  3. Colter, D. C., Sekiya, I., & Prockop, D. J. (2001). Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proceedings of the National Academy of Sciences of the United States of America, 98(14), 7841–7845.

    Article  PubMed  CAS  Google Scholar 

  4. Howson, K. M., Aplin, A. C., Gelati, M., Alessandri, G., Prati, E. A., & Nicosia, R. F. (2005). The postnatal rat aorta contains pericyte progenitor cells that form spheroidal colonies in suspension culture. American Journal of Physiology. Cell Physiology, 289, C1396–C1407.

    Article  PubMed  CAS  Google Scholar 

  5. De Francesco, F., Tirino, V., Desiderio, V., Ferraro, G., D’Andrea, F., Giuliano, M., et al. (2009). Human CD34+/CD90+ ASCs are capable of growing as spere clusters, producine high levels of VEGF and forming capillaries. PLoS ONE, 4(8), e6537.

    Article  PubMed  Google Scholar 

  6. Horwitz, E. M., Le Blanc, K., Dominici, M., Mueller, I., Slaper-Cortenbach, I., Marini, F. C., et al. (2005). Clarification of the nomenclature for MSC: the International Society for Cellular Therapy position statement. Cytotherapy, 7(5), 393–395.

    Article  PubMed  CAS  Google Scholar 

  7. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F. C., Krause, D. S., et al. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8(4), 315–317.

    CAS  Google Scholar 

  8. Ho, A. D., Wagner, W., & Franke, W. (2008). Heterogeneity of mesenchymal stromal cell preparations. Cytotherapy, 10(4), 320–330.

    Article  PubMed  CAS  Google Scholar 

  9. Kovacic, J. C., & Boehm, M. (2009). Resident vascular progenitor cells: an emerging role for non-terminally differentiated vessel-resident cells in vascular biology. Stem Cell Research, 2(1), 2–15.

    Article  PubMed  Google Scholar 

  10. Klein, D., Hohn, H.-P., Kleff, V., Tilki, D., & Ergün, S. (2010). Vascular wall-resident stem cells. Histology and Histopathology, 25(5), 681–689.

    PubMed  Google Scholar 

  11. Crisan, M., Chen, C.-W., Corselli, M., Andriolo, G., Lazzari, L., & Péault, B. (2009). Perivascular multipotent progenitor cells in human organs. Annals of the New York Academy of Sciences, 1176, 118–123.

    Article  PubMed  CAS  Google Scholar 

  12. Crisan, M., Yap, S., Casteilla, L., Chen, C. W., Corselli, M., Park, T. S., et al. (2008). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell, 3(3), 301–313.

    Article  PubMed  CAS  Google Scholar 

  13. Chen, C.-W., Montelatici, E., Crisan, M., Corselli, M., Huard, J., Lazzari, L., et al. (2009). Perivascular multi-lineage progenitor cells in human organs: regenerative units, cytokine sources or both? Cytokine & Growth Factor Reviews, 20(5–6), 429–434.

    Article  CAS  Google Scholar 

  14. Zimmerlin, L., Donnenberg, V. S., Pfeifer, M. E., Meyer, E. M., Péault, B., Rubin, J. P., et al. (2010). Stromal vascular progenitors in adult human adipose tissue. Cytometry. Part A, 77(1), 22–30.

    Google Scholar 

  15. Pacilli, A., & Pasquinelli, G. (2009). Vascular wall progenitor cells. A review. Experimental Cell Research, 315(6), 901–914.

    Article  PubMed  CAS  Google Scholar 

  16. Diaz-Florez, L., Gutiérrez, R., Madrid, J. F., Varela, H., Valladares, F., Acosta, E., et al. (2009). Perycytes. Morphofunction, interactions, pathology in a quiescent and activated mesenchymal cell niche. Histology and Histopathology, 24(7), 909–969.

    Google Scholar 

  17. Andreeva, E. R., Pugach, I. M., Gordon, D., & Orekhov, A. N. (1998). Continuous subendothelial network formed by pericyte-like cells in human vascular bed. Tissue & Cell, 30(1), 127–135.

    Article  CAS  Google Scholar 

  18. Traktuev, D. O., Merfeld-Clauss, S., Li, J., Kolonin, M., Arap, W., Pasqualini, R., et al. (2008). A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circulation Research, 102(1), 77–85.

    Article  PubMed  CAS  Google Scholar 

  19. Morikawa, S., Mabuchi, Y., Kubota, Y., Nagai, Y., Niibe, K., Hiratsu, E., et al. (2009). Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. The Journal of Experimental Medicine, 206(11), 2483–2496.

    Article  PubMed  CAS  Google Scholar 

  20. Lin, G., Garcia, M., Ning, H., Banie, L., Guo, Y.-L., Lue, T. F., et al. (2008). Defining stem and progenitor cells within adipose tissue. Stem Cells and Development, 17(6), 1053–1063.

    Article  PubMed  CAS  Google Scholar 

  21. Suga, H., Matsumoto, D., Eto, H., Inoue, K., Aoi, N., Kato, H., et al. (2009). Functional implications of CD34 expression in human adipose-derived stem/progenitor cells. Stem Cells and Development, 18(8), 1201–1210.

    Article  PubMed  CAS  Google Scholar 

  22. Lin, C.-S., Xin, Z.-C., Deng, C.-H., Ning, H., Lin, G., & Lue, T. F. (2010). Defining adipose tissue-derived stem cells in tissue and culture. Histology and Histopathology, 25(6), 807–815.

    PubMed  Google Scholar 

  23. Gesta, S., Tseng, Y.-H., & Kahn, C. R. (2007). Developmental origin of fat: tracking obesity to its source. Cell, 131(10), 242–256.

    Article  PubMed  CAS  Google Scholar 

  24. Sengenès, C., Lolmède, K., Zakaroff-Girard, A., Busse, R., & Bouloumié, A. (2005). Preadipocytes in the human subcutaneous adipose tissue display distinct features from the adult mesenchymal and hematopoietic stem cells. Journal of Cellular Physiology, 205(1), 114–122.

    Article  PubMed  Google Scholar 

  25. Rodeheffer, M., Birsoy, K., & Friedman, J. M. (2008). Identification of white adipocyte progenitor cells in vivo. Cell, 135(10), 240–249.

    Article  PubMed  CAS  Google Scholar 

  26. Tang, W., Zeve, D., Suh, J. M., Bosnakovski, D., Kyba, M., Hammer, R. E., et al. (2008). White fat progenitors reside in the adipose vasculature. Science, 322, 583–586.

    Article  PubMed  CAS  Google Scholar 

  27. Zeve, D., Tang, W., & Graff, J. (2009). Fighting fat with fat: the expanding field of adipose stem cells. Cell Stem Cell, 5(11), 472–481.

    Article  PubMed  CAS  Google Scholar 

  28. Rosen, E. D., & MacDougald, O. A. (2006). Adipocyte differentiation from the inside out. Nature Reviews. Molecular Cell Biology, 7, 885–896.

    Article  PubMed  CAS  Google Scholar 

  29. Billon, N., Monteiro, M. C., & Dani, C. (2008). Developmental origin of adipocytes: new insights into a pending question. Biology of the Cell, 100(10), 563–575.

    Article  PubMed  CAS  Google Scholar 

  30. Billon, N., Iannarelli, P., Monteiro, M. C., Glavieux-Pardanaud, C., Richardson, W. D., Kessaris, N., et al. (2007). The generation of adipocytes by the neural crest. Development, 134(12), 2283–2292.

    Article  PubMed  CAS  Google Scholar 

  31. Majka, S. M., Fox, K. E., Psilas, J. C., Helm, K. M., Childs, C. R., Acosta, A. S., et al. (2010). De novo generation of white adipocytes from the myeloid lineage via mesenchymal intermediates is age, adipose depot, and gender specific. Proceedings of the National Academy of Sciences of the United States of America, 107(33), 14781–14786.

    Article  PubMed  CAS  Google Scholar 

  32. Seale, P., Bjork, B., Yang, W., Kajimura, S., Kuang, S., Scime, A., et al. (2008). PRDM16 controls a brown fat/skeletal muscle switch. Nature, 454, 961–967.

    Article  PubMed  CAS  Google Scholar 

  33. Crisan, M., Casteilla, L., Lehr, L., Carmona, M., Paoloni-Giacobino, A., Yap, S., et al. (2008). A reservoir of brown adipocyte progenitors in human skeletal muscle. Stem Cell, 26, 2425–2433.

    Article  CAS  Google Scholar 

  34. Tchkonia, T., Lenburg, M., Thomou, T., Giorgadze, N., Frampton, G., Pirtskhalava, T., et al. (2007). Identification of depot-specific human fat cell progenitors through distinct expression profiles and developmental gene patterns. American Journal of Physiology. Endocrinology and Metabolism, 292(1), E298–E307.

    Article  PubMed  CAS  Google Scholar 

  35. Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., et al. (1997). Isolation of putative progenitor endothelial cells for angiogenesis. Science, 275, 964–967.

    Article  PubMed  CAS  Google Scholar 

  36. Alessandri, G., Girelli, M., Taccagni, G., Colombo, A., Nicosia, R., Caruso, A., et al. (2001). Human vasculogenesis ex vivo: embryonal aorta as a tool for isolation of progenitors. Laboratory Investigation, 81(6), 875–885.

    PubMed  CAS  Google Scholar 

  37. Ingram, D. A., Mead, L. E., Tanaka, H., Meade, V., Fenoglio, A., Mortell, K., et al. (2004). Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood, 104(9), 2752–2760.

    Article  PubMed  CAS  Google Scholar 

  38. Ingram, D. A., Mead, L. E., Moore, D. B., Woodard, W., Fenoglio, A., & Yoder, M. C. (2005). Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood, 105(7), 2783–2786.

    Article  PubMed  CAS  Google Scholar 

  39. Zengin, E., Chalajour, F., Gehling, U. M., Ito, W. D., Treede, H., Lauke, H., et al. (2006). Vascular wall resident progenitor cells: a source for postnatal vasculogenesis. Development, 133(8), 1543–1551.

    Article  PubMed  CAS  Google Scholar 

  40. Ergün, S., Tilki, D., Hohn, H.-P., Gehling, U., & Kilin, N. (2007). Potential implications of vascular wall resident endothelial progenitor cells. Thrombosis and Haemostasis, 98(5), 930–939.

    PubMed  Google Scholar 

  41. Cousin, B., André, M., Arnaud, E., Pénicaud, L., & Casteilla, L. (2003). Reconstitution of lethally irradiated mice by cells isolated from adipose tissue. Biochemical and Biophysical Research Communications, 301, 1016–1022.

    Article  PubMed  CAS  Google Scholar 

  42. Varma, M. J., Breuls, R. G., Schouten, T. E., Jurgens, W. J., Bontkes, H. J., Schuurhuis, G. J., et al. (2007). Phenotypical and functional characterization of freshly isolated adipose tissue-derived stem cells. Stem Cells and Development, 16(1), 91–104.

    Article  PubMed  Google Scholar 

  43. Mangi, A. A., Noiseux, N., Kong, D., He, H., Rezvani, M., Ingwall, J. S., et al. (2003). Mesenchymal stem cells modified with Akt prevent remodelling and restore performance of infarcted hearts. Nature Medicine, 9, 1195–1201.

    Article  PubMed  CAS  Google Scholar 

  44. Da Silva Meirelles, L., Chagastelles, P. C., & Nardi, N. B. (2006). Mesenchymal stem cells reside in virtually all post-natal organs and tissues. Journal of Cell Science, 119(Pt11), 2204–2213.

    Article  PubMed  Google Scholar 

  45. Prunet-Marcassus, B., Cousin, B., Caton, D., André, M., Pénicaud, L., & Casteilla, L. (2006). From heterogeneity to plasticity in adipose tissue: site-specific differences. Experimental Cell Research, 312, 727–736.

    Article  PubMed  CAS  Google Scholar 

  46. Miñana, M.-D., Carbonell-Uberos, F., Mirabet, V., Marin, S., & Encabo, A. (2008). IFATS collection: identification of hemangioblasts in the adult human adipose tissue. Stem Cells, 26, 2696–2704.

    Article  PubMed  Google Scholar 

  47. Han, J., Koh, Y. J., Moon, H. R., Ryoo, H. G., Cho, C.-H., Kim, I., et al. (2010). Adipose tissue is an extramedullary reservoir for functional hematopoietic stem and progenitor cells. Blood, 115(5), 957–964.

    Article  PubMed  CAS  Google Scholar 

  48. Kuwana, M., Okazaki, Y., Kodama, H., Izumi, K., Yasuoka, H., Ogawa, Y., et al. (2003). Human circulating CD14+ monocytes as a source of progenitors that exhibit mesenchymal cell differentiation. Journal of Leukocyte Biology, 74, 833–845.

    Article  PubMed  CAS  Google Scholar 

  49. Zhao, Y., Glasne, D., & Huberman, E. (2003). A human peripheral blood monocyte-derived subset acts as pluripotent stem cells. Proceedings of the National Academy of Sciences of the United States of America, 100(5), 2426–2431.

    Article  PubMed  CAS  Google Scholar 

  50. Seta, N., & Kuwana, M. (2007). Human circulating monocytes as multipotential progenitors. The Keio Journal of Medicine, 56(2), 41–47.

    Article  PubMed  Google Scholar 

  51. Takashima, Y., Era, T., Nakao, K., Kondo, S., Kasuga, M., Smith, A. G., et al. (2007). Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell, 129, 1377–1388.

    Article  PubMed  CAS  Google Scholar 

  52. Vodyanik, M. A., Yu, J., Zhang, X., Tian, S., Stewart, R., Thomson, J. A., et al. (2010). A mesoderm-derived precursor for mesenchymal stem and endothelial cells. Cell Stem Cell, 7, 718–729.

    Article  PubMed  CAS  Google Scholar 

  53. Murfee, W. L., Skalak, T. C., & Peirce, S. M. (2005). Differential arterial/venous expression of NG2 proteoglycan in perivascular cells along microvessels: identifying a venule-specific phenotype. Microcirculation, 12(2), 151–160.

    Article  PubMed  CAS  Google Scholar 

  54. Murfee, W. L., Rehorn, M. R., Peirce, S. M., & Skalak, T. C. (2006). Perivascular cells along venules upregulate NG2 expression during microvasculature remodelling. Microcirculation, 13, 261–273.

    Article  PubMed  CAS  Google Scholar 

  55. Sobiesiak, M., Sivasubramaniyan, K., Herman, C., Tan, C., Örgel, M., Treml, S., et al. (2010). The Mesenchymal stem cell antigen MSCA-1 is identical to tissue non-specific alkaline phosphatase. Stem Cells and Development, 19(5), 669–677.

    Article  PubMed  CAS  Google Scholar 

  56. Sacchetti, B., Funari, A., Michienzi, S., Di Cesare, S., Piersanti, S., Saggio, I., et al. (2007). Self-renewing osteoprogenitors in bone morrow sinusoid can organize a hematopoietic microenvironment. Cell, 131(2), 324–336.

    Article  PubMed  CAS  Google Scholar 

  57. Quirici, N., Scavullo, C., de Girolamo, L., Lopa, S., Arrigoni, E., Deliliers, G. L., et al. (2010). Anti-L-NGFR and -CD34 monoclonal antibodies identify multipotent mesenchymal stem cells in human adipose tissue. Stem Cells and Development, 19(6), 915–925.

    Article  PubMed  CAS  Google Scholar 

  58. Krause, D. S., Fackler, M. J., Civin, C. I., & May, W. S. (1996). CD34: structure, biology, and clinical utility. Blood, 87(1), 1–13.

    PubMed  CAS  Google Scholar 

  59. Gangenahalli, G. U., Singh, V. K., Verma, Y. K., Gupta, P., Sharma, R. K., Chandra, R., et al. (2006). Hematopoietic stem cell antigen CD34: role in adhesion or homing. Stem Cells and Development, 15(3), 305–313.

    Article  PubMed  CAS  Google Scholar 

  60. Nielsen, J. S., & McNagny, K. M. (2008). Novel functions of the CD34 family. Journal of Cell Science, 121(22), 3683–3692.

    Article  PubMed  CAS  Google Scholar 

  61. Ieronimakis, N., Balasundaram, G., Rainey, S., Srirangam, K., Yablonka-Reuveni, Z., & Reyes, M. (2010). Absence of CD34 on murine skeletal muscle satellite cells marks a reversible state of activation during acute injury. PLoS ONE, 5(6), e10920.

    Article  PubMed  Google Scholar 

  62. Russell, K. C., Phinney, D. G., Lacey, M. R., Barrilleaux, B. L., Meyertholen, K. E., & O’Connor, K. C. (2010). In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment. Stem Cells, 28(4), 788–798.

    Article  PubMed  CAS  Google Scholar 

  63. Cerletti, M., Molloy, M. J., Tomaczak, K. K., Yoon, S., Ramoni, M. F., Kho, A. T., et al. (2006). Melanoma cell adhesion molecule is a novel marker for human fetal myogenic cells and affects myoblast fusion. Journal of Cell Science, 119(15), 3117–3127.

    Article  PubMed  CAS  Google Scholar 

  64. Elshal, M. F., Khan, S. S., Takahashi, Y., Solomon, M. A., & McCay, J. P., Jr. (2005). CD146 (Mel-CAM), an adhesion marker of endothelial cells, ia a novel marker of lymphocyte subset activation in normal peripheral blood. Blood, 106(8), 2923–2929.

    Article  PubMed  CAS  Google Scholar 

  65. Shih, I. M. (1999). The role of CD146 (Mel-CAM) in biology and pathology. The Journal of Pathology, 189(1), 4–11.

    Article  PubMed  CAS  Google Scholar 

  66. Ouhtit, A., Gaur, R. L., Abd Elmageed, Z. Y., Fernando, A., Thouta, R., Trappey, A. K., et al. (2009). Towards understanding the mode of action of the multifaceted cell adhesion receptor CD146. Biochemical and Biophysical Acta, 1795(2), 130–136.

    CAS  Google Scholar 

  67. Chen, W., Cao, G., & Zhang, S. L. (2010). Is CD146 pivotal in neoplasm invasion and bastocyst embedding? Med Hypotheses (in press).

  68. Bühring, H.-J., Battula, V. L., Treml, S., Schewe, B., Kanz, L., & Vogel, W. (2007). Novel markers for the prospective isolation of human MSC. Annals of the New York Academy of Sciences, 1106, 262–271.

    Article  PubMed  Google Scholar 

  69. Battula, V. L., Treml, S., Bareiss, P. M., Gieseke, F., Roelofs, H., de Zwart, P., et al. (2009). Isolation of functionally distinct mesenchymal stem cell subsets using antibodies against CD56, CD271, and mesenchymal stem cell antigen-1. Haematologica, 94(2), 173–184.

    Article  PubMed  CAS  Google Scholar 

  70. Bühring, H.-J., Treml, S., Cerabona, F., de Zwart, P., Kanz, L., & Sobiesiak, M. (2009). Phenotypic characterization of distinct human bone marrow-derived MSC subsets. Annals of the New York Academy of Sciences, 1176, 124–134.

    Article  PubMed  Google Scholar 

  71. Zheng, B., Cao, B., Crisan, M., Sun, B., Li, G., Logar, A., et al. (2007). Prospective identification of myogenic endothelial cells in human skeletal muscle. Nature Biotechnology, 25(9), 1025–1034.

    Article  PubMed  CAS  Google Scholar 

  72. Turnovcova, K., Ruzickova, K., Vanecek, V., Sykova, E., & Jendelova, P. (2009). Properties and growth of human bone marrow mesenchymal stromal cells cultivated in different media. Cytotherapy, 11(7), 874–885.

    Article  PubMed  CAS  Google Scholar 

  73. Lindroos, B., Boucher, S., Chase, L., Kuokkanen, H., Huhtala, H., Haataja, R., et al. (2009). Serum-free, xeno-free culture media maintain the proliferation rate and multipotentiality of adipose stem cells in vitro. Cytotherapy, 11(7), 958–72.

    Article  PubMed  CAS  Google Scholar 

  74. Mitchell, J. B., McIntosh, K., Zvonic, S., Garret, S., Floyd, E., Kloster, A., et al. (2006). Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells, 24, 376–385.

    Article  PubMed  Google Scholar 

  75. Delorme, B., Ringe, J., Gallay, N., Le Vern, Y., Kerboeuf, D., Jorgensen, C., et al. (2008). Specific plasma membrane protein phenotype of culture-amplified and native human bone marrow mesenchymal stem cells. Blood, 111(5), 2631–2635.

    Article  PubMed  CAS  Google Scholar 

  76. Martinez, C., Hofman, T. J., Marino, R., Dominici, M., & Horwitz, E. M. (2007). Human bone marrow mesenchymal stromal cells express the neural ganglioside GD2: a novel surface marker for the identification of MSCs. Blood, 109(10), 4245–4248.

    Article  PubMed  CAS  Google Scholar 

  77. Wagner, W., Wein, F., Seckinger, A., Frankhauser, M., Wirkner, U., Krause, U., et al. (2005). Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbelical cord blood. Experimental Hematology, 33, 1402–1416.

    Article  PubMed  CAS  Google Scholar 

  78. Kern, S., Eichler, H., Stoeve, J., Klüter, H., & Bieback, K. (2006). Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blod, or adipose tissue. Stem Cells, 24(5), 1294–1301.

    Article  PubMed  CAS  Google Scholar 

  79. Estes, B. T., Wu, A. W., & Guilak, F. (2006). Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenic protein 6. Arthritis and Rheumatism, 54(4), 1222–1232.

    Article  PubMed  CAS  Google Scholar 

  80. Wagers, A. J., & Weissman, I. L. (2004). Plasticity of adult stem cells. Cell, 116(5), 639–648.

    Article  PubMed  CAS  Google Scholar 

  81. Ankrum, J., & Karp, J. M. (2010). Mesenchymal stem cell therapy: two steps forward, one step back. Trends in Molecular Medicine, 16(5), 203–209.

    Article  PubMed  Google Scholar 

  82. Haasters, F., Prall, W. C., Anz, D., Bourquin, C., Pautke, C., Endres, S., et al. (2009). Morphological and immunocytochemical characteristics indicate the yield of early progenitors and represent a quality control for human mesenchymal stem cell culturing. Journal of Anatomy, 214, 759–767.

    Article  PubMed  Google Scholar 

  83. Ozerdem, U., Grako, K. A., Dahlin-Huppe, K., Monosov, E., & Stallcup, W. B. (2001). NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Developmental Dynamics, 222(2), 218–227.

    Article  PubMed  CAS  Google Scholar 

  84. Bardin, B., George, F., Mutin, M., Brisson, C., Horschowski, N., Francès, V., et al. (1996). S-Endo 1, a pan-endothelial monoclonal antibody recognizing a novel human endothelial antigen. Tissue Antigens, 48(5), 531–539.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Lorenzo Tallone for the drawings of Fig. 3 and Dr. Michael Braun (Beckman Coulter GmbH, Germany) and Luciano Gilardoni (Cardiocentro Ticino) for their help with the graphic artwork.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tiziano Tallone.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tallone, T., Realini, C., Böhmler, A. et al. Adult Human Adipose Tissue Contains Several Types of Multipotent Cells. J. of Cardiovasc. Trans. Res. 4, 200–210 (2011). https://doi.org/10.1007/s12265-011-9257-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12265-011-9257-3

Keywords

Navigation