Nonexpanded mesenchymal stem cells for regenerative medicine: Yield in stromal vascular fraction from adipose tissues

Tissue Engineering - Part C: Methods

Volumn 16, Issue 6, 2010, Pages 1515-1521

  Faustini, Massimo ^a   Bucco, Massimo ^b   Chlapanidas, Theodora ^b   Lucconi, Giulia ^b   Marazzi, Mario ^c   Tosca, Marta Cecilia ^c   Gaetani, Paolo ^d   Klinger, Marco ^d   Villani, Simona ^b   Ferretti, Virginia Valeria ^b   Vigo, Daniele ^a   Torre, Maria Luisa ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

^c OSPEDALE NIGUARDA CA GRANDA   (Italy)

^d HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; GENE THERAPY; GENETIC ENGINEERING; OSTEOBLASTS; RECOVERY; STEM CELLS; TISSUE; TISSUE ENGINEERING;

ADIPOCYTES; ADIPOSE TISSUE; BODY MASS INDEX; CANCER THERAPY; CARDIOMYOCYTES; CELL YIELDS; CHONDROCYTES; COLLAGENASE; DIGESTION TIME; HEPATOCYTES; LIVE CELL; MEAN AGES; MESENCHYMAL CELLS; MESENCHYMAL STEM CELL; MULTIVARIATE LINEAR MODEL; MYOCYTES; OPERATING CONDITION; PROCESSING PROCEDURES; REGENERATIVE MEDICINE; SURGICAL PROCEDURES; TISSUE PROCESSING;

ENDOTHELIAL CELLS;

ADIPOSE TISSUE; ADOLESCENT; ADULT; AGED; ARTICLE; BLOOD VESSEL; CELL CULTURE; CELL PROLIFERATION; CELL SEPARATION; CLINICAL TRIAL; CYTOLOGY; FEMALE; HUMAN; MALE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; METHODOLOGY; MIDDLE AGED; PHYSIOLOGY; PRODUCTIVITY; REGENERATIVE MEDICINE; STROMA CELL; VASCULARIZATION;

ADIPOSE TISSUE; ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; BLOOD VESSELS; CELL PROLIFERATION; CELL SEPARATION; CELLS, CULTURED; EFFICIENCY; FEMALE; HUMANS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MIDDLE AGED; REGENERATIVE MEDICINE; STROMAL CELLS; YOUNG ADULT;

EID: 78149362773     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2010.0214     Document Type: Article

References (56)

1. Fantuzzi, G., and Mazzone, T. Preface. In: Fantuzzi, G., and Mazzone, T., eds. Adipose Tissue and Adipokines in Health and Disease. Totowa, NJ: Humana Press, Inc., xiiixv, 2007.
2. Choi, J.H., Gimble, J.M., Lee, K., Marra, K.G., Rubin, J.P., Yoo, J.J., Vunjak-Novakovic, G., and Kaplan, D.L. Adipose tissue engineering for soft tissue regeneration. Tissue Eng Part B Rev 2010 Mar 24 [Epub ahead of print].
3. Villani, S., Marazzi, M., Bucco, M., Faustini, M., Klinger, M., Gaetani, P., Crovato, F., Vigo, D., Caviggioli, F., and Torre, M.L. Statistical approach in alginate membrane formulation for cell encapsulation in a GMP-based cell factory. Acta Biomater 4, 943, 2008.
4. Gaetani, P., Torre, M.L., Klinger, M., Faustini, M., Crovato, F., Bucco, M., Marazzi, M., Chlapanidas, T., Levi, D., Vigo, D., and Rodriguez y Baena, R. Adipose derived stem cell therapy for intervertebral disc regeneration: an in vitro reconstructed tissue in alginate capsules. Tissue Eng Part A 14, 1415, 2008.
5. De Ugarte, D.A., Ashjian, P.H., Elbarbary, A., and Hedrick, M.H. Future of fat as raw material for tissue regeneration. Ann Plastic Surg 50, 215, 2003.
6. Mizuno, H. Adiposederived stem cells for tissue repair and regeneration: ten years of research and a literature review. J Nippon Med Sch 76, 56, 2009.
7. Gimble, J.M., Katz, A.J., and Bunnell, B.A. Adiposederived stem cells for regenerative medicine. Circ Res 100, 1249, 2007.
8. Helder, M.N., Knippenberg, M., Klein-Nulend, J., and Wuisman, P.I.J.M. Stem cells from adipose tissue allow challenging new concepts for regenerative medicine. Tissue Eng 13, 1799, 2007.
9. Romanov, Y.A., Darevskaya, A.N., Merzlikina, N.V., and Buravkova, L.B. Mesenchymal stem cells from human bone marrow and adipose tissue: isolation, characterization, and differentiation potentialities. Cell Technol Biol Med 3, 158, 2005.
10. Dicker, A., Le Blanc, K., Astrom, G., van Harmelen, V., Götherström, C., Blomqvist, L., Arner, P., and Rydèn, M. Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Exp Cell Res 308, 283, 2005.
11. Sanz-Ruiz, R., Fernández-Santos, E., Domínguez-Muñoa, M., Parma, R., Villa, A., Fernández, L., Sánchez, P.L., and Fernández-Avilés, F. Early translation of adiposederived cell therapy for cardiovascular disease. Cell Transplant 18, 245, 2009.
12. Safford, K.M., Safford, S.D., Gimble, J.M., Shetty, A.K., and Rice, H.E. Characterization of neuronal/glial differentiation of murine adiposederived adult stromal cells. Exp Neurol 187, 319, 2004.
13. Barnabé, G.F., Schwindt, T.T., Calcagnotto, M.E., Motta, F.L., Martinez, G., Jr., de Oliveira, A.C., Keim, L.M., D'Almeida, V., Mendez-Otero, R., and Mello, L.E. Chemicallyinduced RAT mesenchymal stem cells adopt molecular properties of neuronallike cells but do not have basic neuronal functional properties. PLoS One 4, e5222, 2009.
14. Le Blanc, K., and Ringdén, O. Mesenchymal stem cells: properties and role in clinical bone marrow transplantation. Curr Opin Immunol 18, 586, 2006.
15. Riordan, N.H., Ichim, T.E., Min, W.P., Wang, H., Solano, F., Lara, F., Alfaro, M., Rodriguez, J.P., Harman, R.J., Patel, A.N., Murphy, M.P., Lee, R.R., and Minev, B. Nonexpanded adipose stromal vascular fraction cell therapy for multiple sclerosis. J Transplant Med 7, 29, 2009.
16. Sensebé, L., and Bourin, P. Mesenchymal stem cells for therapeutic purposes. Transplantation 87, S49, 2009.
17. Tholpady, S.S., Ogle, R.C., and Katz, A.J. Adipose stem cells and solid organ transplantation. Curr Opin Organ Transplant 14, 51, 2009.
18. De Siena, R., Balducci, L., Blasi, A., Montanaro, M.G., Saldarelli, M., Saponaro, V., Martino, C., Logrieco, G., Soleti, A., Fiobellot, S., Madeddu, P., Rossi, G., Ribatti, D., Crovace, A., Cristini, S., Invernici, G., Parati, E.A., and Alessandri, G. Omentumderived stromal cells improve myocardial regeneration in pig postinfarcted heart through a potent paracrine mechanism. Exp Cell Res 2010 Feb 12 [Epub ahead of print].
19. Bernardo, M.E., Zaffaroni, N., Novara, F., Cometa, A.M., Avanzini, M.A., Moretta, A., Montagna, D., Maccario, R., Villa, R., Daidone, M.G., Zuffardi, O., and Locatelli, F. Human bone marrowderived mesenchymal stem cells do not undergo transformation after longterm in vitro culture and do not exhibit telomere maintenance mechanisms. Cancer Res 67, 9142, 2007.
20. Khakoo, A.Y., Pati, S., Anderson, S.A., Reid, W., Elshal, M.F., Rovira, I.I., Nguyen, A.T., Malide, D., Combs, C.A., Hall, G., Zhang, J., Raff, M., Rogers, T.B., Stetler-Stevenson, W., Frank, J.A., Reitz, M., and Finkel, T. Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma. J Exp Med 203, 1235, 2006.
21. Ren, H., Cao, Y., Zhao, Q., Li, J., Zhou, C., Liao, L., Jia, M., Zhao, Q., Cai, H., Han, Z.C., Yang, R., Chen, G., and Zhao, R.C. Proliferation and differentiation of bone marrow stromal cells under hypoxic conditions. Biochem Biophys Res Commun 347, 12, 2006.
22. Ren, C., Kumar, S., Chanda, D., Chen, J., Mountz, J.D., and Ponnazhagan, S. Therapeutic potential of mesenchymal stem cells producing interferona in a mouse melanoma lung metastasis model. Stem Cells 26, 2332, 2008.
23. Mizuno, H., and Hyakusoku, H. Mesengenic potential and future clinical perspective of human processed lipoaspirate cells. J Nippon Med Sch 70, 300, 2003.
24. Fraser, J.K., Wulur, I., Zeni, A., and Hedrick, M.H. Fat tissue an underappreciated source of stem cells for biotechnology. Trends Biotechnol 24, 150, 2006.
25. Gomillion, C.T., and Burg, K.J.L. Stem cells and adipose tissue engineering. Biomaterials 27, 6052, 2006.
26. Rydèn, M., Dicker, A., Götherström, C., Aström, G., Tammik, C., Arner, P., and Le Blanc, K. Functional characterization of human mesenchymal stem cellderived adipocytes. Biochem Biophys Res Commun 14, 391, 2003.
27. Rodriguez, A.M., Elabd, C., Delteil, F., Astier, J., Vernochet, C., Saint-Marc, P., Guesnet, J., Guezzenec, A., Amri, E.Z., Dani, C., and Ailhaud, G. Adipocyte differentiation of multipotent cells estabilished from human adipose tissue. Biochem Biophys Res Commun 315, 255, 2004.
28. Rodriguez, A.M., Elabd, C., Amri, E., Ailhaud, G., and Dani, C. The human adipose tissue is a source of multipotent stem cells. Biochimie 87, 125, 2005.
29. Nakagami, H., Morishita, R., Maeda, K., Kikuchi, Y., Ogihara, T., and Kaneda, Y. Adipose tissuederived stromal cells as a novel option for regenerative cell therapy. J Atheroscler Thromb 13, 77, 2006.
30. Strem, B.M., Hicok, K.C., Zhu, M., Wulur, I., Alfonso, Z., Schreiber, R.E., Fraser, J.K., and Hedrick, M.H. Multipotential differentiation of adipose tissuederived stem cells. Keio J Med 3, 132, 2005.
31. Musina, R.A., Bekchanova, E.S., Belyavskii, V., and Sukhikh, G.T. Differentiation potential of mesenchymal stem cells of different origin. Technol Biol Med 2, 147, 2006.
32. Guilak, F., Lott, K.E., Awad, H.A., Cao, Q., Hicok, K.C., Fermor, B., and Gimble, J.M. Clonal analysis of the differentiation potential of human adiposederived adult stem cells. J Cell Physiol 206, 229, 2006.
33. Mitchell, J.B., McIntosh, K., Zvonic, S., Garret, S., Ployd, Z.E., Loster, A., Di Halvorsen, Y., Storms, R.W., Goh, B., Kilroy, G., Wu, X., and Gimble, J.M. Immunophenotype of human adiposederived cells: temporal changes in stromalassociated markers. J Cell Physiol 208, 64, 2006.
34. Schäffler, A., and Bü chler, C. Concise review: adipose tissuederived stromal cellbasic and clinical implications for novel cellbased therapies. Stem Cells 25, 818, 2007.
35. García-Olmo, D., García-Arranz, M., García, L.G., Cuellar, E.S., Blanco, I.F., Prianes, L.A., Montes, J.A., Pinto, F.L., Marcos, D.H., and García-Sancho, L. Autologous stem cell transplantation for treatment of rectovaginal fistula in perianal Crohn's disease: a new cellbased therapy. Int J Colorectal Dis 18, 451, 2003.
36. Yañ ez, R., Lamana, M.L., García-Castro, J., Colmenero, I., Ramírez, M., and Bueren, J.A. Adipose tissuederived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graftversushost disease. Stem Cells 24, 2582, 2006.
37. Cho, K.S., Park, H.K., Park, H.Y., Jung, J.S., Jeon, S.G., Kim, Y.K., and Roh, H.J. IFATS collection: immunomodulatory effects of adipose tissuederived stem cells in an allergic rhinitis mouse model. Stem Cells 27, 259, 2009.
38. Caplan, A.I. What's in a name? Tissue Eng Part A 2010 Apr 22 [Epub ahead of print].
39. Zhang, J., Niu, C., Ye, L., Huang, H., He, X., Tong, W.G., Ross, J., Haug, J., Johnson, T., Feng, J.Q., Harris, S., Wiedemann, L.M., Mishina, Y., and Li, L. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425, 836, 2003.
40. Rubio, D., Garcia-Castro, J., Martín, M.C., de la Fuente, R., Cigudosa, J.C., Lloyd, A.C., and Bernad, A. Spontaneous human adult stem cell transformation. Cancer Res 65, 3035, 2005.
41. Garcia-Olmo, D., Herreros, D., Pascual, M., Pascual, I., De-La-Quintana, P., Trebol, J., and Garcia-Arranz, M. Treatment of enterocutaneous fistula in Crohn's disease with adiposederived stem cells: a comparison of protocols with and without cell expansion. Int J Colorectal Dis 24, 27, 2009.
42. Schipper, B.M., Marra, K.G., Zhang, W., Donnenberg, A.D., and Rubin, J.P. Regional anatomic and age effects on cell function of human adiposederived stem cells. Ann Plast Surg 60, 538, 2008.
43. Aksu, A.E., Rubin, J.P., Dudas, J.R., and Marra, K.G. Role of gender and anatomicl region on induction of osteogenic differentiation of human adiposederived stem cells. Ann Plast Surg 60, 306, 2008.
44. Caplan, A.I. All MSCs are pericytes? Cell Stem Cell 3, 229, 2008.
45. da Silva Meirelles, L., Sand, T.T., Harman, R.J., Lennon, D.P., and Caplan, A.I. MSC frequency correlates with blood vessel density in equine adipose tissue. Tissue Eng Part A 15, 221, 2009.
46. da Silva Meirelles, L., Caplan, A.I., and Nardi, N.B. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 26, 2287, 2008.
47. Coleman, S.R. Longterm survival of fat transplants: controlled demonstrations. J Aesthetic Plast Surg 19, 421, 1995.
48. Zuk, P.A., Zhu, M., Mizuno, H., Huang, J., Futrell, J.W., Katz, A.J., Benhaim, P., Lorenz, H.P., and Hedrick, M.H. Multilineage cells from human adipose tissue: implications for cellbased therapies. Tissue Eng 7, 211, 2001.
49. Zuk, P.A., Zhu, M., Ashjan, P., De Ugarte, D.A., Huang, J.I., Mizuno, H., Alfonso, Z.C., Fraser, J.K., Benhiamin, P., and Hedrick, M.H. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13, 4279, 2002.
50. Bakker, A.H., Van Dielen, F.M., Greve, J.W., Adam, J.A., and Buurman, W.A. Preadipocyte number in omental and subcutaneous adipose tissue of obese individuals. Obes Res 12, 488, 2004.
51. von Heimburg, D., Hemmrich, K., Haydarlioglu, S., Staiger, H., and Pallua, N. Comparison of viable cell yield from excised versus aspirated adipose tissue. Cells Tissues Organs 178, 87, 2004.
52. Oedayrajsingh-Varma, M.J., van Ham, S.M., Knippenberg, M., Helder, M.N., Klein-Nulend, J., Schouten, T.E., Ritt, M.J.P.F., and van Milligen, F.J. Adipose tissuederived mesenchymal stem cell yield and growth characteristics are affected by the tissueharvesting procedure. Cytotherapy 8, 166, 2006.
53. van Harmelen, V., Röhring, K., and Hauner, H. Comparison of proliferation and differentiation capacity of human adipocyte precursor cells from the omental and subcuteneous adipose tissue depot of obese subjects. Metabolism 53, 632, 2004.
54. van Harmelen, V., Skurk, T., Röhrig, K., Lee, Y.M., Halbleib, M., Aprath-Husmann, I., and Hauner, H. Effect of BMI and age on adipose tissue cellularity and differentiation capacity in women. Int J Obes Relat Metab Disord 27, 889, 2003.
55. Aust, L., Devlin, B., Foster, S.J., Halvorsen, Y.D., Hicok, K., du Laney, T., Sen, A., Willingmyre, G.D., and Gimble, J.M. Yield of human adiposederived adult stem cells from liposuction aspirates. Cytotherapy 6, 7, 2004.
56. Hauner, H., and Entermann, G. Regional variation of adipose differentiation in culture stromalvascular cells from abdominal and femoral adipose tissue of obese women. Int J Obes 15, 121, 1991.