Adipose-derived stem cells: Isolation, characterization, and differentiation potential

Cell Transplantation

Volumn 22, Issue 4, 2013, Pages 701-709

  Huang, Shyh Jer ^a,b   Fu, Ru Huei ^a,b   Shyu, Woei Cherng ^a,b   Liu, Shih Ping ^b   Jong, Gwo Ping ^c   Chiu, Yung Wei ^d,e   Wu, Hsiao Su ^a   Tsou, Yung An ^a   Cheng, Chao Wen ^f   Lin, Shinn Zong ^a,b,g  

^a CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c TAICHUNG ARMED FORCES GENERAL HOSPITAL   (Taiwan)

^d CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^e TUNGS' TAICHUNG METROHARBOR HOSPITAL   (Taiwan)

^f TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^g CHINA MEDICAL UNIVERSITY BEIGANG HOSPITAL   (Taiwan)

Author keywords

Adipose derived stem cells (ADSCS); Bone marrow derived mesenchymal stem cells (BMSCS); CD marker; Stromal vascular fraction (SVF)

Indexed keywords

BIOLOGICAL MARKER;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE CELL; BROWN ADIPOSE TISSUE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CHONDROGENESIS; ENERGY CONSUMPTION; HUMAN; MUSCLE CELL; MUSCLE DEVELOPMENT; NONHUMAN; OSTEOBLAST; PODOCYTE; PRIORITY JOURNAL; REVIEW; STEM CELL; TISSUE ENGINEERING; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE; ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL SEPARATION; CELLS, CULTURED; HUMANS; STEM CELLS;

MAMMALIA;

EID: 84876497106     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X655127     Document Type: Review

References (94)

1. Anghileri, E.; Marconi, S.; Pignatelli, A.; Cifelli, P.; Galie, M.; Sbarbati, A.; Krampera, M.; Belluzzi, O.; Bonetti, B. Neuronal differentiation potential of human adipose-derived mesenchymal stem cells. Stem Cells Dev. 17(5):909-916; 2008.
2. Awad, H. A.; Wickham, M. Q.; Leddy, H. A.; Gimble, J. M.; Guilak, F. Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials 25(16):3211-3222; 2004.
3. Bailey, A. M.; Kapur, S.; Katz, A. J. Characterization of adipose-derived stem cells: An update. Curr. Stem Cell Res. Ther. 5(2):95-102; 2010.
4. Banas, A.; Teratani, T.; Yamamoto, Y.; Tokuhara, M.; Takeshita, F.; Quinn, G.; Okochi, H.; Ochiya, T. Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. Hepatology 46(1):219-228; 2007.
5. Blanpain, C.; Lowry, W. E.; Geoghegan, A.; Polak, L.; Fuchs, E. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118(5):635-648; 2004.
6. Boland, G. M.; Perkins, G.; Hall, D. J.; Tuan, R. S. Wnt 3a promotes proliferation and suppresses osteogenic differentiation of adult human mesenchymal stem cells. J. Cell. Biochem. 93(6):1210-1230; 2004.
7. Cameron, T. L.; Belluoccio, D.; Farlie, P. G.; Brachvogel, B.; Bateman, J. F. Global comparative transcriptome analysis of cartilage formation in vivo. BMC Dev. Biol. 9:20; 2009.
8. Cho, S. W.; Kim, I.; Kim, S. H.; Rhie, J. W.; Choi, C. Y.; Kim, B. S. Enhancement of adipose tissue formation by implantation of adipogenic-differentiated preadipocytes. Biochem. Biophys. Res. Commun. 345(2):588-594; 2006.
9. Cornelius, P.; MacDougald, O. A.; Lane, M. D. Regulation of adipocyte development. Annu. Rev. Nutr. 14:99-129; 1994.
10. Cowan, C. M.; Shi, Y. Y.; Aalami, O. O.; Chou, Y. F.; Mari, C.; Thomas, R.; Quarto, N.; Contag, C. H.; Wu, B.; Longaker, M. T. Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat. Biotechnol. 22(5):560-567; 2004.
11. De Ugarte, D. A.; Alfonso, Z.; Zuk, P. A.; Elbarbary, A.; Zhu, M.; Ashjian, P.; Benhaim, P.; Hedrick, M. H.; Fraser, J. K. Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow. Immunol. Lett. 89(2-3):267-270; 2003.
12. De Ugarte, D. A.; Morizono, K.; Elbarbary, A.; Alfonso, Z.; Zuk, P. A.; Zhu, M.; Dragoo, J. L.; Ashjian, P.; Thomas, B.; Benhaim, P.; Chen, I.; Fraser, J.; Hedrick, M. H. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 174(3):101-109; 2003.
13. Dicker, A.; Le Blanc, K.; Astrom, G.; van Harmelen, V.; Gotherstrom, C.; Blomqvist, L.; Arner, P.; Ryden, M. Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Exp. Cell Res. 308(2):283-290; 2005.
14. Ding, D. C.; Shyu, W. C.; Lin, S. Z. Mesenchymal stem cells. Cell Transplant. 20(1):5-14; 2011.
15. Dominici, M.; Le Blanc, K.; Mueller, I.; Slaper-Cortenbach, I.; Marini, F.; Krause, D.; Deans, R.; Keating, A.; Prockop, D.; Horwitz, E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4):315-317; 2006.
16. Efimenko, A.; Starostina, E.; Kalinina, N.; Stolzing, A. Angiogenic properties of aged adipose derived mesenchymal stem cells after hypoxic conditioning. J. Transl. Med. 9:10; 2011.
17. Elabd, C.; Chiellini, C.; Massoudi, A.; Cochet, O.; Zaragosi, L. E.; Trojani, C.; Michiels, J. F.; Weiss, P.; Carle, G.; Rochet, N.; Dechesne, C. A.; Ailhaud, G.; Dani, C.; Amri, E. Z. Human adipose tissue-derived multipotent stem cells differentiate in vitro and in vivo into osteocyte-like cells. Biochem. Biophys. Res. Commun. 361(2):342-348; 2007.
18. Erickson, G. R.; Gimble, J. M.; Franklin, D. M.; Rice, H. E.; Awad, H.; Guilak, F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem. Biophys. Res. Commun. 290(2):763-769; 2002.
19. Eto, H.; Suga, H.; Inoue, K.; Aoi, N.; Kato, H.; Araki, J.; Doi, K.; Higashino, T.; Yoshimura, K. Adipose injury-associated factors mitigate hypoxia in ischemic tissues through activation of adipose-derived stem/progenitor/stromal cells and induction of angiogenesis. Am. J. Pathol. 178(5):2322-2332; 2011.
20. Festy, F.; Hoareau, L.; Bes-Houtmann, S.; Pequin, A. M.; Gonthier, M. P.; Munstun, A.; Hoarau, J. J.; Cesari, M.; Roche, R. Surface protein expression between human adipose tissue-derived stromal cells and mature adipocytes. Histochem. Cell Biol. 124(2):113-121; 2005.
21. Fraser, J. K.; Wulur, I.; Alfonso, Z.; Hedrick, M. H. Fat tissue: An underappreciated source of stem cells for biotechnology. Trends Biotechnol. 24(4):150-154; 2006.
22. Fruhbeck, G. Overview of adipose tissue and its role in obesity and metabolic disorders. Methods Mol. Biol. 456:1-22; 2008.
23. Gersbach, C. A.; Guldberg, R. E.; Garcia, A. J. In vitro and in vivo osteoblastic differentiation of BMP-2- and Runx2-engineered skeletal myoblasts. J. Cell. Biochem. 100(5):1324-1336; 2007.
24. Gimble, J. M.; Guilak, F. Differentiation potential of adipose derived adult stem (ADAS) cells. Curr. Top. Dev. Biol. 58:137-160; 2003.
25. Gimble, J. M.; Katz, A. J.; Bunnell, B. A. Adiposederived stem cells for regenerative medicine. Circ. Res. 100(9):1249-1260; 2007.
26. Giralt, M.; Martin, I.; Iglesias, R.; Vinas, O.; Villarroya, F.; Mampel, T. Ontogeny and perinatal modulation of gene expression in rat brown adipose tissue. Unaltered iodothyronine 5'-deiodinase activity is necessary for the response to environmental temperature at birth. Eur. J. Biochem. 193(1):297-302; 1990.
27. Gregoire, F. M.; Smas, C. M.; Sul, H. S. Understanding adipocyte differentiation. Physiol. Rev. 78(3):783-809; 1998.
28. Gronthos, S.; Franklin, D. M.; Leddy, H. A.; Robey, P. G.; Storms, R. W.; Gimble, J. M. Surface protein characterization of human adipose tissue-derived stromal cells. J. Cell. Physiol. 189(1):54-63; 2001.
29. Guilak, F.; Estes, B. T.; Diekman, B. O.; Moutos, F. T.; Gimble, J. M. 2010 Nicolas Andry Award: Multipotent adult stem cells from adipose tissue for musculoskeletal tissue engineering. Clin. Orthop. Relat. Res. 468(9):2530-2540; 2010.
30. Halvorsen, Y. D.; Franklin, D.; Bond, A. L.; Hitt, D. C.; Auchter, C.; Boskey, A. L.; Paschalis, E. P.; Wilkison, W. O.; Gimble, J. M. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng. 7(6):729-741; 2001.
31. Haniffa, M. A.; Wang, X. N.; Holtick, U.; Rae, M.; Isaacs, J. D.; Dickinson, A. M.; Hilkens, C. M.; Collin, M. P. Adult human fibroblasts are potent immunoregulatory cells and functionally equivalent to mesenchymal stem cells. J. Immunol. 179(3):1595-1604; 2007.
32. Hicok, K. C.; Du Laney, T. V.; Zhou, Y. S.; Halvorsen, Y. D.; Hitt, D. C.; Cooper, L. F.; Gimble, J. M. Human adipose-derived adult stem cells produce osteoid in vivo. Tissue Eng. 10(3-4):371-380; 2004.
33. Huang, J. I.; Beanes, S. R.; Zhu, M.; Lorenz, H. P.; Hedrick, M. H.; Benhaim, P. Rat extramedullary adipose tissue as a source of osteochondrogenic progenitor cells. Plast. Reconstr. Surg. 109(3):1033-1041; 2002.
34. Huang, J. I.; Kazmi, N.; Durbhakula, M. M.; Hering, T. M.; Yoo, J. U.; Johnstone, B. Chondrogenic potential of progenitor cells derived from human bone marrow and adipose tissue: A patient-matched comparison. J. Orthop. Res. 23(6):1383-1389; 2005.
35. Huang, S. J.; Yang, W. S.; Lin, Y. W.; Wang, H. C.; Chen, C. C. Increase of insulin sensitivity and reversal of agedependent glucose intolerance with inhibition of ASIC3. Biochem. Biophys. Res. Commun. 371(4):729-734; 2008.
36. Jang, H. J.; Cho, K. S.; Park, H. Y.; Roh, H. J. Adipose tissuederived stem cells for cell therapy of airway allergic diseases in mouse. Acta Histochem. 113(5):501-507; 2011.
37. Katz, A. J.; Tholpady, A.; Tholpady, S. S.; Shang, H.; Ogle, R. C. Cell surface and transcriptional characterization of human adipose-derived adherent stromal (hADAS) cells. Stem Cells 23(3):412-423; 2005.
38. Kilroy, G. E.; Foster, S. J.; Wu, X.; Ruiz, J.; Sherwood, S.; Heifetz, A.; Ludlow, J. W.; Stricker, D. M.; Potiny, S.; Green, P.; Halvorsen, Y. D.; Cheatham, B.; Storms, R. W.; Gimble, J. M. Cytokine profile of human adipose-derived stem cells: Expression of angiogenic, hematopoietic, and pro-inflammatory factors. J. Cell. Physiol. 212(3):702- 709; 2007.
39. Kim, W. S.; Park, B. S.; Sung, J. H. The wound-healing and antioxidant effects of adipose-derived stem cells. Expert Opin. Biol. Ther. 9(7):879-887; 2009.
40. Kolf, C. M.; Cho, E.; Tuan, R. S. Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: Regulation of niche, self-renewal and differentiation. Arthritis Res. Ther. 9(1):204; 2007.
41. Lin, Y.; Luo, E.; Chen, X.; Liu, L.; Qiao, J.; Yan, Z.; Li, Z.; Tang, W.; Zheng, X.; Tian, W. Molecular and cellular characterization during chondrogenic differentiation of adipose tissue-derived stromal cells in vitro and cartilage formation in vivo. J. Cell. Mol. Med. 9(4):929-939; 2005.
42. Liu, S. P.; Fu, R. H.; Huang, Y. C.; Chen, S. Y.; Chien, Y. J.; Hsu, C. Y.; Tsai, C. H.; Shyu, W. C.; Lin, S. Z. Induced pluripotent stem (iPS) cell research overview. Cell Transplant. 20(1):15-19; 2011.
43. Liu, S. P.; Fu, R. H.; Yu, H. H.; Li, K. W.; Tsai, C. H.; Shyu, W. C.; Lin, S. Z. MicroRNAs regulation modulated self-renewal and lineage differentiation of stem cells. Cell Transplant. 18(9):1039-1045; 2009.
44. MacDougald, O. A.; Lane, M. D. Adipocyte differentiation. When precursors are also regulators. Curr. Biol. 5(6):618-621; 1995.
45. MacDougald, O. A.; Lane, M. D. Transcriptional regulation of gene expression during adipocyte differentiation. Annu. Rev. Biochem. 64:345-373; 1995.
46. Mandrup, S.; Lane, M. D. Regulating adipogenesis. J. Biol. Chem. 272(9):5367-5370; 1997.
47. Matsumoto, T.; Kano, K.; Kondo, D.; Fukuda, N.; Iribe, Y.; Tanaka, N.; Matsubara, Y.; Sakuma, T.; Satomi, A.; Otaki, M.; Ryu, J.; Mugishima, H. Mature adipocyte-derived dedifferentiated fat cells exhibit multilineage potential. J. Cell. Physiol. 215(1):210-222; 2008.
48. Mauney, J. R.; Nguyen, T.; Gillen, K.; Kirker-Head, C.; Gimble, J. M.; Kaplan, D. L. Engineering adipose-like tissue in vitro and in vivo utilizing human bone marrow and adipose-derived mesenchymal stem cells with silk fibroin 3D scaffolds. Biomaterials 28(35):5280-5290; 2007.
49. Mehlhorn, A. T.; Niemeyer, P.; Kaiser, S.; Finkenzeller, G.; Stark, G. B.; Sudkamp, N. P.; Schmal, H. Differential expression pattern of extracellular matrix molecules during chondrogenesis of mesenchymal stem cells from bone marrow and adipose tissue. Tissue Eng. 12(10):2853-2862; 2006.
50. Metzele, R.; Alt, C.; Bai, X.; Yan, Y.; Zhang, Z.; Pan, Z.; Coleman, M.; Vykoukal, J.; Song, Y. H.; Alt, E. Human adipose tissue-derived stem cells exhibit proliferation potential and spontaneous rhythmic contraction after fusion with neonatal rat cardiomyocytes. FASEB J. 25(3):830-839; 2011.
51. Mimeault, M.; Hauke, R.; Batra, S. K. Stem cells: A revolution in therapeutics-Recent advances in stem cell biology and their therapeutic applications in regenerative medicine and cancer therapies. Clin. Pharmacol. Ther. 82(3):252-264; 2007.
52. Miranville, A.; Heeschen, C.; Sengenes, C.; Curat, C. A.; Busse, R.; Bouloumie, A. Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 110(3):349-355; 2004.
53. Mitchell, J. B.; McIntosh, K.; Zvonic, S.; Garrett, S.; Floyd, Z. E.; Kloster, A.; Di Halvorsen, Y.; Storms, R. W.; Goh, B.; Kilroy, G.; Wu, X.; Gimble, J. M. Immunophenotype of human adipose-derived cells: Temporal changes in stromalassociated and stem cell-associated markers. Stem Cells 24(2):376-385; 2006.
54. Park, I. H.; Zhao, R.; West, J. A.; Yabuuchi, A.; Huo, H.; Ince, T. A.; Lerou, P. H.; Lensch, M. W.; Daley, G. Q. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451(7175):141-146; 2008.
55. Peroni, D.; Scambi, I.; Pasini, A.; Lisi, V.; Bifari, F.; Krampera, M.; Rigotti, G.; Sbarbati, A.; Galie, M. Stem molecular signature of adipose-derived stromal cells. Exp. Cell Res. 314(3):603-615; 2008.
56. 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.; Marshak, D. R. Multilineage potential of adult human mesenchymal stem cells. Science 284(5411):143-147; 1999.
57. Planat-Benard, V.; Silvestre, J. S.; Cousin, B.; Andre, M.; Nibbelink, M.; Tamarat, R.; Clergue, M.; Manneville, C.; Saillan-Barreau, C.; Duriez, M.; Tedgui, A.; Levy, B.; Pénicaud, L.; Casteilla, L. Plasticity of human adipose lineage cells toward endothelial cells: Physiological and therapeutic perspectives. Circulation 109(5):656-663; 2004.
58. Prunet-Marcassus, B.; Cousin, B.; Caton, D.; Andre, M.; Penicaud, L.; Casteilla, L. From heterogeneity to plasticity in adipose tissues: Site-specific differences. Exp. Cell Res. 312(6):727-736; 2006.
59. Rodda, D. J.; Chew, J. L.; Lim, L. H.; Loh, Y. H.; Wang, B.; Ng, H. H.; Robson, P. Transcriptional regulation of nanog by OCT4 and SOX2. J. Biol. Chem. 280(26):24731-24737; 2005.
60. Rodeheffer, M. S.; Birsoy, K.; Friedman, J. M. Identification of white adipocyte progenitor cells in vivo. Cell 135(2):240-249; 2008.
61. Rodriguez, A. M.; Elabd, C.; Amri, E. Z.; Ailhaud, G.; Dani, C. The human adipose tissue is a source of multipotent stem cells. Biochimie 87(1):125-128; 2005.
62. Rosen, E. D.; Hsu, C. H.; Wang, X.; Sakai, S.; Freeman, M. W.; Gonzalez, F. J.; Spiegelman, B. M. C/EBPalpha induces adipogenesis through PPARgamma: A unified pathway. Genes Dev. 16(1):22-26; 2002.
63. Safford, K. M.; Hicok, K. C.; Safford, S. D.; Halvorsen, Y. D.; Wilkison, W. O.; Gimble, J. M.; Rice, H. E. Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem. Biophys. Res. Commun. 294(2):371-379; 2002.
64. Safford, K. M.; Safford, S. D.; Gimble, J. M.; Shetty, A. K.; Rice, H. E. Characterization of neuronal/glial differentiation of murine adipose-derived adult stromal cells. Exp. Neurol. 187(2):319-328; 2004.
65. Salgado, A. J.; Reis, R. L.; Sousa, N. J.; Gimble, J. M. Adipose tissue derived stem cells secretome: Soluble factors and their roles in regenerative medicine. Curr. Stem Cell Res. Ther. 5(2):103-110; 2010.
66. Seglen, P. O. Preparation of isolated rat liver cells. Methods Cell Biol. 13:29-83; 1976.
67. Seo, M. J.; Suh, S. Y.; Bae, Y. C.; Jung, J. S. Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem. Biophys. Res. Commun. 328(1):258-264; 2005.
68. Sgodda, M.; Aurich, H.; Kleist, S.; Aurich, I.; Konig, S.; Dollinger, M. M.; Fleig, W. E.; Christ, B. Hepatocyte differentiation of mesenchymal stem cells from rat peritoneal adipose tissue in vitro and in vivo. Exp. Cell Res. 313(13):2875-2886; 2007.
69. Song, Y. H.; Gehmert, S.; Sadat, S.; Pinkernell, K.; Bai, X.; Matthias, N.; Alt, E. VEGF is critical for spontaneous differentiation of stem cells into cardiomyocytes. Biochem. Biophys. Res. Commun. 354(4):999-1003; 2007.
70. Spiegelman, B. M.; Flier, J. S. Adipogenesis and obesity: Rounding out the big picture. Cell 87(3):377-389; 1996.
71. Strem, B. M.; Hicok, K. C.; Zhu, M.; Wulur, I.; Alfonso, Z.; Schreiber, R. E.; Fraser, J. K.; Hedrick, M. H. Multipotential differentiation of adipose tissue-derived stem cells. Keio J. Med. 54(3):132-141; 2005.
72. Sugii, S.; Kida, Y.; Kawamura, T.; Suzuki, J.; Vassena, R.; Yin, Y. Q.; Lutz, M. K.; Berggren, W. T.; Izpisua Belmonte, J. C.; Evans, R. M. Human and mouse adipose-derived cells support feeder-independent induction of pluripotent stem cells. Proc. Natl. Acad. Sci. USA 107(8):3558-3563; 2010.
73. Sun, N.; Panetta, N. J.; Gupta, D. M.; Wilson, K. D.; Lee, A.; Jia, F.; Hu, S.; Cherry, A. M.; Robbins, R. C.; Longaker, M. T.; Wu, J. C. Feeder-free derivation of induced pluripotent stem cells from adult human adipose stem cells. Proc. Natl. Acad. Sci. USA 106(37):15720-15725; 2009.
74. Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861-872; 2007.
75. Talens-Visconti, R.; Bonora, A.; Jover, R.; Mirabet, V.; Carbonell, F.; Castell, J. V.; Gomez-Lechon, M. J. Hepatogenic differentiation of human mesenchymal stem cells from adipose tissue in comparison with bone marrow mesenchymal stem cells. World J. Gastroenterol. 12(36):5834-5845; 2006.
76. Tapp, H.; Hanley, Jr., E. N.; Patt, J. C.; Gruber, H. E. Adipose-derived stem cells: Characterization and current application in orthopaedic tissue repair. Exp. Biol. Med. 234(1):1-9; 2009.
77. Tholpady, S. S.; Llull, R.; Ogle, R. C.; Rubin, J. P.; Futrell, J. W.; Katz, A. J. Adipose tissue: Stem cells and beyond. Clin. Plast. Surg. 33(1):55-62; 2006.
78. Timper, K.; Seboek, D.; Eberhardt, M.; Linscheid, P.; Christ- Crain, M.; Keller, U.; Muller, B.; Zulewski, H. Human adipose tissue-derived mesenchymal stem cells differentiate into insulin, somatostatin, and glucagon expressing cells. Biochem. Biophys. Res. Commun. 341(4):1135-1140; 2006.
79. Tran, T. T.; Kahn, C. R. Transplantation of adipose tissue and stem cells: Role in metabolism and disease. Nat. Rev. Endocrinol. 6(4):195-213; 2010.
80. Varma, M. J.; Breuls, R. G.; Schouten, T. E.; Jurgens, W. J.; Bontkes, H. J.; Schuurhuis, G. J.; van Ham, S. M.; van Milligen, F. J. Phenotypical and functional characterization of freshly isolated adipose tissue-derived stem cells. Stem Cells Dev. 16(1):91-104; 2007.
81. Wagner, W.; Wein, F.; Seckinger, A.; Frankhauser, M.; Wirkner, U.; Krause, U.; Blake, J.; Schwager, C.; Eckstein, V.; Ansorge, W.; Ho, A. D. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp. Hematol. 33(11):1402-1416; 2005.
82. Williams, S. K.; Wang, T. F.; Castrillo, R.; Jarrell, B. E. Liposuction-derived human fat used for vascular graft sodding contains endothelial cells and not mesothelial cells as the major cell type. J. Vasc. Surg. 19(5):916-923; 1994.
83. Wilson, A.; Butler, P. E.; Seifalian, A. M. Adipose-derived stem cells for clinical applications: A review. Cell Prolif. 44(1):86-98; 2011.
84. Yamamoto, N.; Akamatsu, H.; Hasegawa, S.; Yamada, T.; Nakata, S.; Ohkuma, M.; Miyachi, E.; Marunouchi, T.; Matsunaga, K. Isolation of multipotent stem cells from mouse adipose tissue. J. Dermatol. Sci. 48(1):43-52; 2007.
85. Yanez, R.; Lamana, M. L.; Garcia-Castro, J.; Colmenero, I.; Ramirez, M.; Bueren, J. A. Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 24(11):2582-2591; 2006.
86. Yoshimura, K.; Shigeura, T.; Matsumoto, D.; Sato, T.; Takaki, Y.; Aiba-Kojima, E.; Sato, K.; Inoue, K.; Nagase, T.; Koshima, I.; Gonda, K. Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates. J. Cell. Physiol. 208(1):64-76; 2006.
87. Young, C.; Jarrell, B. E.; Hoying, J. B.; Williams, S. K. A porcine model for adipose tissue-derived endothelial cell transplantation. Cell Transplant. 1(4):293-298; 1992.
88. Yu, J.; Vodyanik, M. A.; Smuga-Otto, K.; Antosiewicz- Bourget, J.; Frane, J. L.; Tian, S.; Nie, J.; Jonsdottir, G. A.; Ruotti, V.; Stewart, R.; Slukvin, I. I.; Thomson, J. A. Induced pluripotent stem cell lines derived from human somatic cells. Science 318(5858):1917-1920; 2007.
89. Zachar, V.; Rasmussen, J. G.; Fink, T. Isolation and growth of adipose tissue-derived stem cells. Methods Mol. Biol. 698:37-49; 2011.
90. Zheng, B.; Cao, B.; Li, G.; Huard, J. Mouse adipose-derived stem cells undergo multilineage differentiation in vitro but primarily osteogenic and chondrogenic differentiation in vivo. Tissue Eng. 12(7):1891-1901; 2006.
91. Zhu, Y.; Liu, T.; Song, K.; Fan, X.; Ma, X.; Cui, Z. Adiposederived stem cell: A better stem cell than BMSC. Cell Biochem. Funct. 26(6):664-675; 2008.
92. Zimmerlin, L.; Donnenberg, V. S.; Pfeifer, M. E.; Meyer, E. M.; Peault, B.; Rubin, J. P.; Donnenberg, A. D. Stromal vascular progenitors in adult human adipose tissue. Cytometry A 77(1):22-30; 2010.
93. Zuk, P. A.; Zhu, M.; Ashjian, P.; De Ugarte, D. A.; Huang, J. I.; Mizuno, H.; Alfonso, Z. C.; Fraser, J. K.; Benhaim, P.; Hedrick, M. H. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 13(12):4279-4295; 2002.
94. Zuk, P. A.; Zhu, M.; Mizuno, H.; Huang, J.; Futrell, J. W.; Katz, A. J.; Benhaim, P.; Lorenz, H. P.; Hedrick, M. H. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng. 7(2):211-228; 2001.