Abstract
Recently, the existence of a population of stem cells located in the adipose tissue has been observed. Adipose-derived stem cells are able to differentiate into multiple cell lineages including cardiac myocytes. Hence, adipose-derived cells are emerging as a new source of adult stem cells for cardiovascular repair. In this review, we discuss the basic principles of adipose-derived stem cells (types and characteristics, obtention processes, immunophenotypic characterization, and cell potency), the initial experimental studies, and the currently ongoing clinical trials.
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Villaron, E. M., Almeida, J., López-Holgado, N., Alcoceba, M., Sánchez-Abarca, L. I., Sanchez-Guijo, F. M., et al. (2004). Mesenchymal stem cells are present in peripheral blood and can engraft after allogeneic hematopoietic stem cell transplantation. Haematologica, 89, 1421–1427.
LĂłpez-Holgado, N., Arroyo, J. L., Pata, C., VillarĂłn, E., Sánchez Guijo, F., MartĂn, A., et al. (2004). Analysis of hematopoietic progenitor cells in patients with myelodysplastic syndromes according to their cytogenetic abnormalities. Leukemia Leukemia Research, 28, 1181–1187.
Zuk, P. A., Zhu, M., Mizuno, H., Huang, J., Futrell, J. W., Katz, A. J., et al. (2001). Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Engineering, 7, 211–228.
Zuk, P. A., Zhu, M., Ashjian, P., De Ugarte, D. A., Huang, J. I., Mizuno, H., et al. (2002). Human adipose tissue is a source of multipotent stem cells. Molecular Biology of the Cell, 13, 4279–4295.
Fickert, S., Fiedler, J., Brenner, R. E. (2004). Identification of subpopulations with characteristics of mesenchymal progenitor cells from human osteoarthritic cartilage using triple staining for cell surface markers. Arthritis Research & Therapy, 6, 422–432.
Sánchez, A., GarcĂa-Sancho, J. (2007). Cardiac repair by stem cells. Cell Death and Differentiation, 14, 1258–1261.
Kern, S., Eichler, H., Stoeve, J., Klüter, H., Bieback, K. (2006). Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells, 24, 1294–1301.
Izadpanah, R., Trygg, C., Patel, B., Kriedt, C., Dufour, J., Gimble, J. M., et al. (2006). Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. Journal of Cellular Biochemistry, 99, 1285–1297.
Yoshimura, H., Muneta, T., Nimura, A., Yokoyama, A., Koga, H., & Sekiya, I. (2007). Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell & Tissue Research, 327, 449–462.
Prunet-Marcassus, B., Cousin, B., Caton, D., André, M., Pénicaud, L., & Casteilla, L. (2006). From heterogeneity to plasticity in adipose tissues: site-specific differences. Experimental Cell Research, 312, 727–736.
Oedayrajsingh-Varma, M. J., van Ham, S. M., Knippenberg, M., Helder, M. N., Klein-Nulend, J., Schouten, T. E., et al. (2006). Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy, 8, 166–177.
Smith, P., Adams, W. P. Jr., Lipschitz, A. H., Chau, B., Sorokin, E., Rohrich, R. J., et al. (2006). Autologous human fat grafting: effect of harvesting and preparation techniques on adipocyte graft survival. Plastic and Reconstructive Surgery, 117, 1836–1844.
Dicker, A., Le Blanc, K., Aström, G., van Harmelen, V., Götherström, C., Blomqvist, L., et al. (2005). Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Experimental Cell Research, 308, 283–290.
Lee, R. H., Kim, B., Choi, I., Kim, H., Choi, H. S., Suh, K., et al. (2004). Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cellular Physiology and Biochemistry, 14, 311–324.
Xu, Y., Malladi, P., Wagner, D. R., Longaker, M. T. (2005). Adipose-derived mesenchymal cells as a potential cell source for skeletal regeneration. Current Opinion in Molecular Therapeutics, 7, 300–305.
Gimble, J. M., Katz, A. J., & Bunnell, B. A. (2007). Adipose-derived stem cells for regenerative medicine. Circulation Research, 11, 1249–1260.
Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., & Krause, D., et al. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8, 315–317.
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, 114–122.
Astori, G., Vignati, F., Bardelli, S., Tubio, M., Gola, M., Albertini, V., et al. (2007). “In vitro” and multicolor phenotypic characterization of cell subpopulations identified in fresh human adipose tissue stromal vascular fraction and in the derived mesenchymal stem cells. Journal of Translational Medicine, 5, 55.
Mitchell, J. B., McIntosh, K., Zvonic, S., Garrett, S., Floyd, Z. 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.
Liu, T. M., Martina, M., Hutmacher, D. W., Hui, J. H., Lee, E. H., Lim, B. (2007). Identification of common pathways mediating differentiation of bone marrow- and adipose tissue-derived human mesenchymal stem cells into three mesenchymal lineages. Stem Cells, 25, 750–760.
Duckers, H. J., Pinkernell, K., Milstein, A. M., & Hedrick, M. H. (2006). The Bedside Celution™ system for isolation of adipose derived regenerative cells. EIJ, 2, 395–398.
Schäffler, A., & Büchler, C. (2007). Concise review: adipose tissue-derived stromal cells—basic and clinical implications for novel cell-based therapies. Stem Cells, 25, 818–827.
McIntosh, K., Zvonic, S., Garrett, S., Mitchell, J. B., Floyd, Z. E., Hammill, L., et al. (2006). The immunogenicity of human adipose-derived cells: temporal changes in vitro. Stem Cells, 24, 1246–1253.
Mizuno, H., Zuk, P. A., Zhu, M., Lorenz, H. P., Benhaim, P., & Hedrick, M. H. (2002). Myogenic differentiation by human processed lipoaspirate cells. Plastic and Reconstructive Surgery, 109, 199–209.
Rangappa, S., Fen, C., Lee, E. H., Bongso, A., & Sim, E. K. (2003). Transformation of adult mesenchymal stem cells isolated from the fatty tissue into cardiomyocytes. Annals of Thoracic Surgery, 75, 775–779.
Planat-Bénard, V., Menard, C., André, M., Puceat, M., Perez, A., Garcia-Verdugo, J. M., et al. (2004). Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circulation Research, 94, 223–229.
Planat-Bénard, V., Silvestre, J. S., Cousin, B., André, M., Nibbelink, M., Tamarat, R., et al. (2004). Plasticity of human adipose lineage cells toward endothelial cells. Physiological and therapeutic perspectives. Circulation, 109, 656–663.
Miranville, A., Heeschen, C., Sengenès, C., Curat, C. A., Busse, R., & Bouloumié, A. (2004). Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation, 110, 349–355.
Nakagami, H., Morishita, R., Maeda, K., Kikuchi, Y., Ogihara, T., Kaneda, Y. (2006). Adipose tissue-derived stromal cells as a novel option for regenerative cell therapy. Journal of Atherosclerosis and Thrombosis, 13, 77–81.
Cao, Y., Sun, Z., Liao, L., Meng, Y., Han, Q., & Zhao, R. C. (2005). Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochemical and Biophysical Research Communications, 332, 370–379.
Rehman, J., Traktuev, D., Li, J., Merfeld-Clauss, S., Temm-Grove, C. J., Bovenkerk, J. E., et al. (2004). Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation, 109, 1292–1298.
Moon, M. H., Kim, S. Y., Kim, Y. J., Kim, S. J., Lee, J. B., Bae, Y. C., et al. (2006). Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Cellular Cellular Physiology and Biochemistry, 17, 279–290.
Nakagami, H., Maeda, K., Morishita, R., et al. (2005). Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arteriosclerosis, Thrombosis, and Vascular Biology, 25, 2542–2547.
Strem, B. M., Zhu, M., Alfonso, Z., Daniels, E. J., Schreiber, R., Beygui, R., et al. (2005). Expression of cardiomyocytic markers on adipose tissue-derived cells in a murine model of acute myocardial injury. Cytotherapy, 7, 282–291.
Strem, B. M., Jordan, M., Kim, J., Yang, J., Anderson, C. D., Daniels, E., et al. (2005). Adipose tissue-derived stem cells enhance cardiac function following surgically-induced myocardial infarction. Circulation, 112(suppl II), 274.
Yamada, Y., Wang, X. D., Yokoyama, S., Fukuda, N., & Takakura, N. (2006). Cardiac progenitor cells in brown adipose tissue repaired damaged myocardium. Biochemical and Biophysical Research Communications, 342, 662–670.
Yamada, Y., Yokoyama, S., Fukuda, N., Kidoya, H., Huang, X. Y., Naitoh, H., et al. (2007). A novel approach for myocardial regeneration with educated blood cells cocultured with cells from brown adipose tissue. Biochemical and Biophysical Research Communications, 353, 182–188.
Yamada, Y., Yokoyama, S., Wang, X. D., Fukuda, N., & Takakura, N. (2007). Cardiac stem cells in brown adipose tissue express CD133 and induce bone marrow nonhematopoietic cells to differentiate into cardiomyocytes. Stem Cells, 25, 1326–1333.
Watanabe, C. T., Lee, S., Daniela, E., Naqvi, T. Z., Shah, P. K., Shah, A., et al. (2004). Intracoronary adipose tissue-derived stem cell therapy preserves left ventricular function in a porcine infarct model. American Journal of Cardiology, 94(suppl I), 188E.
Alt, E., Scharlau, M., Pinkernell, K., Amadi, C., Reddy, K., Mathias, N., et al. (2005). Uncultured, autologous adipose-derived stromal cells—a novel cell source for cardiac repair. American Journal of Cardiology, 96(suppl I), 71H.
Valina, C., Pinkernell, K., Song, Y. H., Bai, X., Sadat, S., Campeau, R. J., et al. (2007). Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion and remodeling after acute myocardial infarction. European Heart Journal, 28, 2667–2677.
Miyahara, Y., Nagaya, N., Kataoka, M., Yanagawa, B., Tanaka, K., Hao, H., et al. (2006). Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Natural Medicines, 12, 459–465.
Cardoso, C., Silva, G. V., Fernandes, M., Schreiber, R., Oliveira, E. M., Jiménez-Quevedo, P., et al. (2007). Catheter based delivery of adipose-derived stem cells in a large animal chronic ischemia model improves myocardial healing. European Heart Journal, 28(suppl I), 227.
Lendeckel, S., Jödicke, A., Christophis, P., Heidinger, K., Wolff, J., Fraser, J. K., et al. (2004). Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. Journal of Cranio-maxillo-facial Surgery, 32, 370–373.
GarcĂa-Olmo, D., GarcĂa-Arranz, M., GarcĂa, L. G., Cuellar, E. S., Blanco, I. F., Prianes, L. A., et al. (2003). Autologous stem cell transplantation for treatment of rectovaginal fistula in perianal Crohn’s disease: a new cell-based therapy. International Journal of Colorectal Disease, 18, 451–454.
GarcĂa-Olmo, D., GarcĂa-Arranz, M., Herreros, D., Pascual, I., Peiro, C., & RodrĂguez-Montes, J. A. (2005). A phase I clinical trial of the treatment of Crohn’s fistula by adipose mesenchymal stem cell transplantation. Diseases of the Colon & Rectum, 48, 1416–1423.
Yoshimura, K., Matsumoto, D., & Gonda, K. A clinical trial of soft-tissue augmentation by lipoinjection with adipose-derived stromal cells (ASCs). International Fat Applied Technology Society (IFATS); Third Annual Meeting, September 10–13, 2005, Charlottesville VA, p. 9.
Stosich, M. S., & Mao, J. J. (2007). Adipose tissue engineering from human adult stem cells: Clinical implications in plastic and reconstructive surgery. Plastic and Reconstructive Surgery, 119, 71–83.
Fraser, J. K., Schreiber, R., Strem, B., Zhu, M., Alfonso, Z., Wulur, I., et al. (2006). Plasticity of human adipose stem cells toward endothelial cells and cardiomyocytes. Nature Clinical Practice Cardiovascular Medicine, 3(suppl I), S33–S37.
Rubio, D., Garcia-Castro, J., Martin, M. C., de la Fuente, R., Cigudosa, J. C., Lloyd, A. C., et al. (2005). Spontaneous human adult stem cell transformation. Cancer Research, 65, 3035–3039.
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Sanz-Ruiz, R., Fernández Santos, M.E., DomĂnguez Muñoa, M. et al. Adipose Tissue-derived Stem Cells: The Friendly Side of a Classic Cardiovascular Foe. J. of Cardiovasc. Trans. Res. 1, 55–63 (2008). https://doi.org/10.1007/s12265-007-9006-9
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DOI: https://doi.org/10.1007/s12265-007-9006-9