Concise review: Adipose-derived stem cells as a novel tool for future regenerative medicine

Stem Cells

Volumn 30, Issue 5, 2012, Pages 804-810

  Mizuno, Hiroshi ^a   Tobita, Morikuni ^b   Uysal, A Cagri ^c  

^a JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b Japan Self Defense Forces Hospital Yokosuka   (Japan)

^c BASKENT UNIVERSITY   (Turkey)

Author keywords

Adipose derived stem cells; Clinical trials; Differentiation; Growth factors; Proliferation; Regenerative medicine

Indexed keywords

ADIPONECTIN; ANGIOTENSIN; BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; CATHEPSIN D; CD146 ANTIGEN; CD31 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; CELL THERAPY AGENT; CYTOKERATIN 18; ENDOGLIN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; INTERLEUKIN 11; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; PENTRAXIN; PREGNANCY ASSOCIATED ALPHA2 GLYCOPROTEIN; RETINOL BINDING PROTEIN; SCATTER FACTOR; SOMATOMEDIN C; STROMAL CELL DERIVED FACTOR 1; THY 1 ANTIGEN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UVOMORULIN; VASCULOTROPIN;

ABSENCE OF SIDE EFFECTS; ACUTE GRAFT VERSUS HOST DISEASE; ADIPOSE DERIVED STEM CELL; ALLERGIC RHINITIS; ANGIOGENESIS; APOPTOSIS; ARTHRITIS; BRAIN HEMORRHAGE; BRAIN ISCHEMIA; BROWN ADIPOSE TISSUE; CELL DIFFERENTIATION; CELL GROWTH; CELL ISOLATION; CELL LINEAGE; CELL PROLIFERATION; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; COLONY FORMING UNIT F; DIGESTIVE SYSTEM FISTULA; GRAFT VERSUS HOST REACTION; HUMAN; KERATINOCYTE; NONHUMAN; PROTEIN EXPRESSION; REGENERATIVE MEDICINE; REVIEW; SPINAL CORD INJURY; STEM CELL TRANSPLANTATION; SUBCUTANEOUS FAT; TH1 CELL; TH2 CELL; TISSUE REGENERATION; WOUND HEALING;

ADIPOSE TISSUE; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; REGENERATIVE MEDICINE; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84860523401     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1076     Document Type: Review

References (106)

1. Lenoir N. Europe confronts the embryonic stem cell research challenge. Science 2000;287:1425-1427. (Pubitemid 30127125)
2. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-676. (Pubitemid 44233629)
3. Ben-David U, Benvenisty N. The tumorigenicity of human embryonic and induced pluripotent stem cells. Nat Rev Cancer 2011;11: 268-277.
4. Song L, Young NJ, Webb NE et al. Origin and characterization of multipotential mesenchymal stem cells derived from adult human trabecular bone. Stem Cells Dev 2005;14:712-721. (Pubitemid 43201905)
5. Choi YS, Noh SE, Lim SM et al. Multipotency and growth characteristic of periosteum-derived progenitor cells for chondrogenic, osteogenic, and adipogenic differentiation. Biotechnol Lett 2008;30: 593-601.
6. De Bari C, Dell'Accio F, Tylzanowski P et al. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 2001;44:1928-1942. (Pubitemid 32758241)
7. Dodson MV, Hausman GJ, Guan L et al. Skeletal muscle stem cells from animals I. Basic cell biology. Int J Biol Sci 2010;6: 465-474.
8. Belicchi M, Pisati F, Lopa R et al. Human skin-derived stem cells migrate throughout forebrain and differentiate into astrocytes after injection into adult mouse brain. J Neurosci Res 2004;77:475-486. (Pubitemid 39006999)
9. Feng J, Mantesso A, Sharpe PT. Perivascular cells as mesenchymal stem cells. Expert Opin Biol Ther 2010;10:1441-1451.
10. Shi M, Ishikawa M, Kamei N et al. Acceleration of skeletal muscle regeneration in a rat skeletal muscle injury model by local injection of human peripheral blood-derived cd133-positive cells. Stem Cells 2009;27:949-960.
11. Miura M, Gronthos S, Zhao M et al. Shed: Stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA 2003;100: 5807-5812. (Pubitemid 36576889)
12. Seo BM, Miura M, Gronthos S et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004; 364:149-155. (Pubitemid 38891686)
13. Baksh D, Yao R, Tuan RS. Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem Cells 2007;25: 1384-1392. (Pubitemid 47106005)
14. Musina RA, Bekchanova ES, Sukhikh GT. Comparison of mesenchymal stem cells obtained from different human tissues. Bull Exp Biol Med 2005;139:504-509. (Pubitemid 41131253)
15. Zuk PA, Zhu M, Mizuno H et al. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng 2001;7: 211-228. (Pubitemid 32295155)
16. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res 2007;100:1249-1260. (Pubitemid 46742916)
17. Tobita M, Orbay H, Mizuno H. Adipose-derived stem cells: Current findings and future perspectives. Discov Med 2011;11:160-170.
18. Yoshimura K, Suga H, Eto H. Adipose-derived stem/progenitor cells: Roles in adipose tissue remodeling and potential use for soft tissue augmentation. Regen Med 2009;4:265-273.
19. Weisberg SP, McCann D, Desai M et al. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003;112: 1796-1808. (Pubitemid 38063703)
20. Xu H, Barnes GT, Yang Q et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003;112:1821-1830. (Pubitemid 38063705)
21. Schipper BM, Marra KG, Zhang W et al. Regional anatomic and age effects on cell function of human adipose-derived stem cells. Ann Plast Surg 2008;60:538-544. (Pubitemid 351591463)
22. Prunet-Marcassus B, Cousin B, Caton D et al. From heterogeneity to plasticity in adipose tissues: Site-specific differences. Exp Cell Res 2006;312:727-736.
23. Seale P, Bjork B, Yang W et al. Prdm16 controls a brown fat/skeletal muscle switch. Nature 2008;454:961-967.
24. Zimmerlin L, Donnenberg VS, Pfeifer ME et al. Stromal vascular progenitors in adult human adipose tissue. Cytometry A 2010;77: 22-30.
25. Bailey AM, Kapur S, Katz AJ. Characterization of adipose-derived stem cells: An update. Curr Stem Cell Res Ther 2010;5:95-102.
26. Basciano L, Nemos C, Foliguet B et al. Long term culture of mesenchymal stem cells in hypoxia promotes a genetic program maintaining their undifferentiated and multipotent status. BMC Cell Biol 2011;12:12.
27. Bernardo ME, Zaffaroni N, Novara F et al. Human bone marrow derived mesenchymal stem cells do not undergo transformation after long-term in vitro culture and do not exhibit telomere maintenance mechanisms. Cancer Res 2007;67:9142-9149. (Pubitemid 47535900)
28. Deans RJ, Moseley AB. Mesenchymal stem cells: Biology and potential clinical uses. Exp Hematol 2000;28:875-884.
29. Folgiero V, Migliano E, Tedesco M et al. Purification and characterization of adipose-derived stem cells from patients with lipoaspirate transplant. Cell Transplant 2010;19:1225-1235.
30. Freitas CS, Dalmau SR. Multiple sources of non-embryonic multipotent stem cells: Processed lipoaspirates and dermis as promising alternatives to bone-marrow-derived cell therapies. Cell Tissue Res 2006;325:403-411. (Pubitemid 44126155)
31. Gronthos S, Franklin DM, Leddy HA et al. Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 2001;189:54-63.
32. Jones EA, English A, Kinsey SE et al. Optimization of a flow cytometry-based protocol for detection and phenotypic characterization of multipotent mesenchymal stromal cells from human bone marrow. Cytometry B Clin Cytom 2006;70:391-399. (Pubitemid 44652075)
33. Katz AJ, Tholpady A, Tholpady SS et al. Cell surface and transcriptional characterization of human adipose-derived adherent stromal (hadas) cells. Stem Cells 2005;23:412-423. (Pubitemid 40404460)
34. Meyerrose TE, De Ugarte DA, Hofling AA et al. In vivo distribution of human adipose-derived mesenchymal stem cells in novel xenotransplantation models. Stem Cells 2007;25:220-227. (Pubitemid 46052993)
35. Mitchell JB, McIntosh K, Zvonic S et al. Immunophenotype of human adipose-derived cells: Temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 2006;24:376-385. (Pubitemid 44464807)
36. Yoshimura K, Shigeura T, Matsumoto D et al. Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates. J Cell Physiol 2006;208:64-76. (Pubitemid 43848990)
37. Alipour R, Sadeghi F, Hashemi-Beni B et al. Phenotypic characterizations and comparison of adult dental stem cells with adiposederived stem cells. Int J Prev Med 2010;1:164-171.
38. Delorme B, Ringe J, Gallay N et al. Specific plasma membrane protein phenotype of culture-amplified and native human bone marrow mesenchymal stem cells. Blood 2008;111:2631-2635.
39. Kim YJ, Yu JM, Joo HJ et al. Role of cd9 in proliferation and proangiogenic action of human adipose-derived mesenchymal stem cells. Pflugers Arch 2007;455:283-296. (Pubitemid 47546793)
40. Wagner W, Wein F, Seckinger A et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005;33:1402-1416. (Pubitemid 41541969)
41. Suga H, Matsumoto D, Eto H et al. Functional implications of cd34 expression in human adipose-derived stem/progenitor cells. Stem Cells Dev 2009;18:1201-1210.
42. Tang W, Zeve D, Suh JM et al. White fat progenitor cells reside in the adipose vasculature. Science 2008;322:583-586.
43. Traktuev DO, Merfeld-Clauss S, Li J et al. A population of multipotent cd34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res 2008;102:77-85.
44. Jeon BG, Kumar BM, Kang EJ et al. Characterization and comparison of telomere length, telomerase and reverse transcriptase activity and gene expression in human mesenchymal stem cells and cancer cells of various origins. Cell Tissue Res 2011;345:149-161.
45. Puissant B, Barreau C, Bourin P et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: Comparison with bone marrow mesenchymal stem cells. Br J Haematol 2005;129: 118-129. (Pubitemid 40524060)
46. Fang B, Song Y, Liao L et al. Favorable response to human adipose tissue-derived mesenchymal stem cells in steroid-refractory acute graft-versus-host disease. Transplant Proc 2007;39:3358-3362. (Pubitemid 350251475)
47. Boquest AC, Shahdadfar A, Brinchmann JE et al. Isolation of stromal stem cells from human adipose tissue. Methods Mol Biol 2006; 325:35-46.
48. Strem BM, Hicok KC, Zhu M et al. Multipotential differentiation of adipose tissue-derived stem cells. Keio J Med 2005;54:132-141. (Pubitemid 41542713)
49. Sterodimas A, de Faria J, Nicaretta B et al. Tissue engineering with adipose-derived stem cells (adscs): Current and future applications. J Plast Reconstr Aesthet Surg 2010;63:1886-1892.
50. Van Poll D, Parekkadan B, Borel Rinkes I et al. Mesenchymal stem cell therapy for protection and repair of injured vital organs. Cell Mol Bioeng 2008;1:42-50.
51. Kim WS, Park BS, Sung JH. Protective role of adipose-derived stem cells and their soluble factors in photoaging. Arch Dermatol Res 2009;301:329-336.
52. Rehman J, Traktuev D, Li J et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 2004; 109:1292-1298. (Pubitemid 38372789)
53. Salgado AJ, Reis RL, Sousa NJ et al. Adipose tissue derived stem cells secretome: Soluble factors and their roles in regenerative medicine. Curr Stem Cell Res Ther 2010;5:103-110.
54. Kilroy GE, Foster SJ, Wu X et al. Cytokine profile of human adipose-derived stem cells: Expression of angiogenic, hematopoietic, and pro-inflammatory factors. J Cell Physiol 2007;212:702-709. (Pubitemid 47271882)
55. De Ugarte DA, Morizono K, Elbarbary A et al. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 2003;174:101-109. (Pubitemid 36819010)
56. Izadpanah R, Trygg C, Patel B et al. Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem 2006;99:1285-1297.
57. Rodriguez AM, Elabd C, Delteil F et al. Adipocyte differentiation of multipotent cells established from human adipose tissue. Biochem Biophys Res Commun 2004;315:255-263. (Pubitemid 38183102)
58. Rubio D, Garcia-Castro J, Martin MC et al. Spontaneous human adult stem cell transformation. Cancer Res 2005;65:3035-3039. (Pubitemid 40524580)
59. Garcia S, Bernad A, Martin MC et al. Pitfalls in spontaneous in vitro transformation of human mesenchymal stem cells. Exp Cell Res 2010;316:1648-1650.
60. Torsvik A, Rosland GV, Svendsen A et al. Spontaneous malignant transformation of human mesenchymal stem cells reflects cross-contamination: Putting the research field on track-letter. Cancer Res 2010;70:6393-6396.
61. Hebert TL, Wu X, Yu G et al. Culture effects of epidermal growth factor (egf) and basic fibroblast growth factor (bfgf) on cryopreserved human adipose-derived stromal/stem cell proliferation and adipogenesis. J Tissue Eng Regen Med 2009;3:553-561.
62. Kras KM, Hausman DB, Martin RJ. Tumor necrosis factor-alpha stimulates cell proliferation in adipose tissue-derived stromal-vascular cell culture: Promotion of adipose tissue expansion by paracrine growth factors. Obes Res 2000;8:186-193.
63. Zaragosi LE, Ailhaud G, Dani C. Autocrine fibroblast growth factor 2 signaling is critical for self-renewal of human multipotent adipose-derived stem cells. Stem Cells 2006;24:2412-2419. (Pubitemid 44674301)
64. Kang YJ, Jeon ES, Song HY et al. Role of c-jun N-terminal kinase in the pdgf-induced proliferation and migration of human adipose tissue-derived mesenchymal stem cells. J Cell Biochem 2005;95: 1135-1145. (Pubitemid 41420121)
65. Song HY, Jeon ES, Jung JS et al. Oncostatin m induces proliferation of human adipose tissue-derived mesenchymal stem cells. Int J Biochem Cell Biol 2005;37:2357-2365. (Pubitemid 41207407)
66. Kakudo N, Minakata T, Mitsui T et al. Proliferation-promoting effect of platelet-rich plasma on human adipose-derived stem cells and human dermal fibroblasts. Plast Reconstr Surg 2008;122:1352-1360.
67. Blande IS, Bassaneze V, Lavini-Ramos C et al. Adipose tissue mesenchymal stem cell expansion in animal serum-free medium supplemented with autologous human platelet lysate. Transfusion 2009;49: 2680-2685.
68. Freyberg S, Song YH, Muehlberg F et al. Thrombin peptide (tp508) promotes adipose tissue-derived stem cell proliferation via pi3 kinase/akt pathway. J Vasc Res 2009;46:98-102.
69. Mizuno H. Adipose-derived stem and stromal cells for cell-based therapy: Current status of preclinical studies and clinical trials. Curr Opin Mol Ther 2010;12:442-449.
70. Zuk PA. The adipose-derived stem cell: Looking back and looking ahead. Mol Biol Cell 2010;21:1783-1787.
71. Garcia-Olmo D, Herreros D, Pascual I et al. Expanded adipose-derived stem cells for the treatment of complex perianal fistula: A phase ii clinical trial. Dis Colon Rectum 2009;52:79-86.
72. Garcia-Olmo D, Herreros D, Pascual M et al. Treatment of enterocutaneous fistula in Crohn's disease with adipose-derived stem cells: A comparison of protocols with and without cell expansion. Int J Colorectal Dis 2009;24:27-30.
73. Yoshimura K, Sato K, Aoi N et al. Cell-assisted lipotransfer for cosmetic breast augmentation: Supportive use of adipose-derived stem/stromal cells. Aesthetic Plast Surg 2008;32:48-55; discussion 56-47.
74. Yoshimura K, Sato K, Aoi N et al. Cell-assisted lipotransfer for facial lipoatrophy: Efficacy of clinical use of adipose-derived stem cells. Dermatol Surg 2008;34:1178-1185.
75. Rigotti G, Marchi A, Galie M et al. Clinical treatment of radiotherapy tissue damage by lipoaspirate transplant: A healing process mediated by adipose-derived adult stem cells. Plast Reconstr Surg 2007;119:1409-1422; discussion 1423-1404.
76. Akita S, Akino K, Hirano A et al. Mesenchymal stem cell therapy for cutaneous radiation syndrome. Health Phys 2010;98:858-862.
77. Mesimaki K, Lindroos B, Tornwall J et al. Novel maxillary reconstruction with ectopic bone formation by gmp adipose stem cells. Int J Oral Maxillofac Surg 2009;38:201-209.
78. Lendeckel S, Jodicke A, Christophis P et al. Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: Case report. J Craniomaxillofac Surg 2004;32:370-373. (Pubitemid 40045639)
79. Brayfield CA, Marra KG, Rubin JP. Adipose tissue regeneration. Curr Stem Cell Res Ther 2010;5:116-121.
80. Cherubino M, Marra KG. Adipose-derived stem cells for soft tissue reconstruction. Regen Med 2009;4:109-117.
81. Rubin JP, Marra KG. Soft tissue reconstruction. Methods Mol Biol 2011;702:395-400.
82. Dragoo JL, Samimi B, Zhu M et al. Tissue-engineered cartilage and bone using stem cells from human infrapatellar fat pads. J Bone Joint Surg Br 2003;85:740-747. (Pubitemid 36927045)
83. Estes BT, Diekman BO, Gimble JM et al. Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype. Nat Protoc 2010;5:1294-1311.
84. Estes BT, Guilak F. Three-dimensional culture systems to induce chondrogenesis of adipose-derived stem cells. Methods Mol Biol 2011;702:201-217.
85. Mizuno H, Zuk PA, Zhu M et al. Myogenic differentiation by human processed lipoaspirate cells. Plast Reconstr Surg 2002;109:199-209; discussion 210-191.
86. Lee WC, Sepulveda JL, Rubin JP et al. Cardiomyogenic differentiation potential of human adipose precursor cells. Int J Cardiol 2009; 133:399-401.
87. Planat-Benard V, Menard C, Andre M et al. Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circ Res 2004; 94:223-229. (Pubitemid 38197455)
88. Cherubino M, Rubin JP, Miljkovic N et al. Adipose-derived stem cells for wound healing applications. Ann Plast Surg 2011;66:210-215.
89. Uysal AC, Mizuno H. Tendon regeneration and repair with adipose derived stem cells. Curr Stem Cell Res Ther 2010;5:161-167.
90. Tobita M, Mizuno H. Periodontal disease and periodontal tissue regeneration. Curr Stem Cell Res Ther 2010;5:168-174.
91. Brzoska M, Geiger H, Gauer S et al. Epithelial differentiation of human adipose tissue-derived adult stem cells. Biochem Biophys Res Commun 2005;330:142-150. (Pubitemid 40394946)
92. Long JL, Zuk P, Berke GS et al. Epithelial differentiation of adipose-derived stem cells for laryngeal tissue engineering. Laryngoscope 2010;120:125-131.
93. Vossmerbaeumer U, Ohnesorge S, Kuehl S et al. Retinal pigment epithelial phenotype induced in human adipose tissue-derived mesenchymal stromal cells. Cytotherapy 2009;11:177-188.
94. Safford KM, Safford SD, Gimble JM et al. Characterization of neuronal/ glial differentiation of murine adipose-derived adult stromal cells. Exp Neurol 2004;187:319-328. (Pubitemid 38610278)
95. Ikegame Y, Yamashita K, Hayashi S et al. Comparison of mesenchymal stem cells from adipose tissue and bone marrow for ischemic stroke therapy. Cytotherapy 2011;13:675-685.
96. Kim JM, Lee ST, Chu K et al. Systemic transplantation of human adipose stem cells attenuated cerebral inflammation and degeneration in a hemorrhagic stroke model. Brain Res 2007;1183:43-50. (Pubitemid 350103784)
97. Kang SK, Shin MJ, Jung JS et al. Autologous adipose tissue-derived stromal cells for treatment of spinal cord injury. Stem Cells Dev 2006;15:583-594. (Pubitemid 44701177)
98. Aurich H, Sgodda M, Kaltwasser P et al. Hepatocyte differentiation of mesenchymal stem cells from human adipose tissue in vitro promotes hepatic integration in vivo. Gut 2009;58:570-581.
99. Banas A, Teratani T, Yamamoto Y et al. Rapid hepatic fate specification of adipose-derived stem cells and their therapeutic potential for liver failure. J Gastroenterol Hepatol 2009;24:70-77.
100. Chandra V, Swetha G, Phadnis S et al. Generation of pancreatic hormone-expressing islet-like cell aggregates from murine adipose tissue-derived stem cells. Stem Cells 2009;27:1941-1953.
101. Timper K, Seboek D, Eberhardt M et al. Human adipose tissuederived mesenchymal stem cells differentiate into insulin, somatostatin, and glucagon expressing cells. Biochem Biophys Res Commun 2006;341:1135-1140. (Pubitemid 43221783)
102. Nambu M, Kishimoto S, Nakamura S et al. Accelerated wound healing in healing-impaired db/db mice by autologous adipose tissue-derived stromal cells combined with atelocollagen matrix. Ann Plast Surg 2009;62:317-321.
103. Cho KS, Roh HJ. Immunomodulatory effects of adipose-derived stem cells in airway allergic diseases. Curr Stem Cell Res Ther 2010;5:111-115.
104. Gonzalez MA, Gonzalez-Rey E, Rico L et al. Treatment of experimental arthritis by inducing immune tolerance with human adipose-derived mesenchymal stem cells. Arthritis Rheum 2009;60:1006-1019.
105. Gimble JM, Guilak F, Bunnell BA. Clinical and preclinical translation of cell-based therapies using adipose tissue-derived cells. Stem Cell Res Ther 2010;1:19.
106. Gimble JM, Bunnell BA, Chiu ES et al. Concise review: Adipose-derived stromal vascular fraction cells and stem cells: Let's not get lost in translation. Stem Cells 2011;29:749-754.