Skip to main content
SpringerLink
Log in

Isolation, Characterization, Differentiation, and Application of Adipose-Derived Stem Cells

  • Chapter
  • First Online:
Bioreactor Systems for Tissue Engineering II

Part of the book series: Advances in Biochemical Engineering / Biotechnology ((ABE,volume 123))

Abstract

While bone marrow-derived mesenchymal stem cells are known and have been investigated for a long time, mesenchymal stem cells derived from the adipose tissue were identified as such by Zuk et al. in 2001. However, as subcutaneous fat tissue is a rich source which is much more easily accessible than bone marrow and thus can be reached by less invasive procedures, adipose-derived stem cells have moved into the research spotlight over the last 8 years.

Isolation of stromal cell fractions involves centrifugation, digestion, and filtration, resulting in an adherent cell population containing mesenchymal stem cells; these can be subdivided by cell sorting and cultured under common conditions.

They seem to have comparable properties to bone marrow-derived mesenchymal stem cells in their differentiation abilities as well as a favorable angiogenic and anti-inflammatory cytokine secretion profile and therefore have become widely used in tissue engineering and clinical regenerative medicine.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal-Ginard B, Anversa P (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763–776

    CAS  Google Scholar 

  2. van VP S, JP DPA, Goumans MJ (2007) Isolation and expansion of resident cardiac progenitor cells. Expert Rev Cardiovasc Ther 5:33–43

    Google Scholar 

  3. Dhawan J, Rando TA (2005) Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol 15:666–673

    CAS  Google Scholar 

  4. Peault B, Rudnicki M, Torrente Y, Cossu G, Tremblay JP, Partridge T, Gussoni E, Kunkel LM, Huard J (2007) Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 15:867–877

    CAS  Google Scholar 

  5. Griffiths MJ, Bonnet D, Janes SM (2005) Stem cells of the alveolar epithelium. Lancet 366:249–260

    Google Scholar 

  6. Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, Crowley D, Bronson RT, Jacks T (2005) Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121:823–835

    CAS  Google Scholar 

  7. Brittan M, Wright NA (2002) Gastrointestinal stem cells. J Pathol 197:492–509

    Google Scholar 

  8. Bussolati B, Bruno S, Grange C, Buttiglieri S, Deregibus MC, Cantino D, Camussi G (2005) Isolation of renal progenitor cells from adult human kidney. Am J Pathol 166:545–555

    CAS  Google Scholar 

  9. Herrera MB, Bruno S, Buttiglieri S, Tetta C, Gatti S, Deregibus MC, Bussolati B, Camussi G (2006) Isolation and characterization of a stem cell population from adult human liver. Stem Cells 24:2840–2850

    CAS  Google Scholar 

  10. Koblas T, Zacharovova K, Berkova Z, Mindlova M, Girman P, Dovolilova E, Karasova L, Saudek F (2007) Isolation and characterization of human CXCR4-positive pancreatic cells. Folia Biol (Praha) 53:13–22

    CAS  Google Scholar 

  11. Levy V, Lindon C, Zheng Y, Harfe BD, Morgan BA (2007) Epidermal stem cells arise from the hair follicle after wounding. FASEB J 21:1358–1366

    CAS  Google Scholar 

  12. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino T, Nakafuku M (2002) Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110:429–441

    CAS  Google Scholar 

  13. Ourednik J, Ourednik V, Lynch WP, Schachner M, Snyder EY (2002) Neural stem cells display an inherent mechanism for rescuing dysfunctional neurons. Nat Biotechnol 20:1103–1110

    CAS  Google Scholar 

  14. Mimeault M, Hauke R, Batra SK (2007) 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 82:252–264

    CAS  Google Scholar 

  15. Schaffler A, Buchler C (2007) Concise review: adipose tissue-derived stromal cells–basic and clinical implications for novel cell-based therapies. Stem Cells 25:818–827

    Google Scholar 

  16. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211–228

    CAS  Google Scholar 

  17. Fruebis J, Tsao TS, Javorschi S, Ebbets-Reed D, Erickson MR, Yen FT, Bihain BE, Lodish HF (2001) Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc Natl Acad Sci USA 98:2005–2010

    CAS  Google Scholar 

  18. Trayhurn P, Hoggard N, Mercer JG, Rayner DV (1999) Leptin: fundamental aspects. Int J Obes Relat Metab Disord 23(Suppl 1):22–28

    CAS  Google Scholar 

  19. Mizuno H, Hyakusoku H (2003) Mesengenic potential and future clinical perspective of human processed lipoaspirate cells. J Nippon Med Sch 70:300–306

    Google Scholar 

  20. Rodriguez AM, Elabd C, Amri EZ, Ailhaud G, Dani C (2005) The human adipose tissue is a source of multipotent stem cells. Biochimie 87:125–128

    CAS  Google Scholar 

  21. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295

    CAS  Google Scholar 

  22. Planat-Benard V, Silvestre JS, Cousin B, Andre M, Nibbelink M, Tamarat R, Clergue M, Manneville C, Saillan-Barreau C, Duriez M, Tedgui A, Levy B, Penicaud L, Casteilla L (2004) Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 109:656–663

    Google Scholar 

  23. Ashjian PH, Elbarbary AS, Edmonds B, DeUgarte D, Zhu M, Zuk PA, Lorenz HP, Benhaim P, Hedrick MH (2003) In vitro differentiation of human processed lipoaspirate cells into early neural progenitors. Plast Reconstr Surg 111:1922–1931

    Google Scholar 

  24. Fujimura J, Ogawa R, Mizuno H, Fukunaga Y, Suzuki H (2005) Neural differentiation of adipose-derived stem cells isolated from GFP transgenic mice. Biochem Biophys Res Commun 333:116–121

    CAS  Google Scholar 

  25. Safford KM, Hicok KC, Safford SD, Halvorsen YD, Wilkison WO, Gimble JM, Rice HE (2002) Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem Biophys Res Commun 294:371–379

    CAS  Google Scholar 

  26. Safford KM, Safford SD, Gimble JM, Shetty AK, Rice HE (2004) Characterization of neuronal/glial differentiation of murine adipose-derived adult stromal cells. Exp Neurol 187:319–328

    CAS  Google Scholar 

  27. Banas A, Teratani T, Yamamoto Y, Tokuhara M, Takeshita F, Quinn G, Okochi H, Ochiya T (2007) Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. Hepatology 46:219–228

    CAS  Google Scholar 

  28. Seo MJ, Suh SY, Bae YC, Jung JS (2005) Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem Biophys Res Commun 328:258–264

    CAS  Google Scholar 

  29. Timper K, Seboek D, Eberhardt M, Linscheid P, Christ-Crain M, Keller U, Muller B, Zulewski H (2006) Human adipose tissue-derived mesenchymal stem cells differentiate into insulin, somatostatin, and glucagon expressing cells. Biochem Biophys Res Commun 341:1135–1140

    CAS  Google Scholar 

  30. Corre J, Barreau C, Cousin B, Chavoin JP, Caton D, Fournial G, Penicaud L, Casteilla L, Laharrague P (2006) Human subcutaneous adipose cells support complete differentiation but not self-renewal of hematopoietic progenitors. J Cell Physiol 208:282–288

    CAS  Google Scholar 

  31. Kilroy GE, Foster SJ, Wu X, Ruiz J, Sherwood S, Heifetz A, Ludlow JW, Stricker DM, Potiny S, Green P, Halvorsen YD, Cheatham B, Storms RW, Gimble JM (2007) Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors. J Cell Physiol 212:702–709

    CAS  Google Scholar 

  32. Rehman J, Traktuev D, Li J, Merfeld-Clauss S, Temm-Grove CJ, Bovenkerk JE, Pell CL, Johnstone BH, Considine RV, March KL (2004) Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109:1292–1298

    Google Scholar 

  33. Kitagawa Y, Korobi M, Toriyama K, Kamei Y, Torii S (2006) History of discovery of human adipose-deived stem cells and their clinical applications. Jpn J Plast Reconstr Surg 49:1097–1104

    Google Scholar 

  34. Fraser JK, Wulur I, Alfonso Z, Hedrick MH (2006) Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol 24:150–154

    CAS  Google Scholar 

  35. Oedayrajsingh-Varma MJ, van Ham SM, Knippenberg M, Helder MN, Klein-Nulend J, Schouten TE, Ritt MJ, van Milligen FJ (2006) Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy 8:166–177

    CAS  Google Scholar 

  36. Prunet-Marcassus B, Cousin B, Caton D, Andre M, Penicaud L, Casteilla L (2006) From heterogeneity to plasticity in adipose tissues: site-specific differences. Exp Cell Res 312:727–736

    CAS  Google Scholar 

  37. Peptan IA, Hong L, Mao JJ (2006) Comparison of osteogenic potentials of visceral and subcutaneous adipose-derived cells of rabbits. Plast Reconstr Surg 117:1462–1470

    CAS  Google Scholar 

  38. Pettersson P, Van R, Karlsson M, Bjorntorp P (1985) Adipocyte precursor cells in obese and nonobese humans. Metabolism 34:808–812

    CAS  Google Scholar 

  39. Roncari DA, Lau DC, Kindler S (1981) Exaggerated replication in culture of adipocyte precursors from massively obese persons. Metabolism 30:425–427

    CAS  Google Scholar 

  40. Schipper BM, Marra KG, Zhang W, Donnenberg AD, Rubin JP (2008) Regional anatomic and age effects on cell function of human adipose-derived stem cells. Ann Plast Surg 60:538–544

    CAS  Google Scholar 

  41. Shahparaki A, Grunder L, Sorisky A (2002) Comparison of human abdominal subcutaneous versus omental preadipocyte differentiation in primary culture. Metabolism 51:1211–1215

    CAS  Google Scholar 

  42. Shi YY, Nacamuli RP, Salim A, Longaker MT (2005) The osteogenic potential of adipose-derived mesenchymal cells is maintained with aging. Plast Reconstr Surg 116:1686–1696

    CAS  Google Scholar 

  43. Zhu M, Kohan E, Bradley J, Hedrick M, Benhaim P, Zuk P (2009) The effect of age on osteogenic, adipogenic and proliferative potential of female adipose-derived stem cells. J Tissue Eng Regen Med 3:290–301

    CAS  Google Scholar 

  44. van Harmelen V, Rohrig K, Hauner H (2004) Comparison of proliferation and differentiation capacity of human adipocyte precursor cells from the omental and subcutaneous adipose tissue depot of obese subjects. Metabolism 53:632–637

    Google Scholar 

  45. Hutley LJ, Herington AC, Shurety W, Cheung C, Vesey DA, Cameron DP, Prins JB (2001) Human adipose tissue endothelial cells promote preadipocyte proliferation. Am J Physiol Endocrinol Metab 281:E1037–E1044

    CAS  Google Scholar 

  46. Fang B, Song YP, Li N, Li J, Han Q, Zhao RC (2009) Resolution of refractory chronic autoimmune thrombocytopenic purpura following mesenchymal stem cell transplantation: a case report. Transplant Proc 41:1827–1830

    CAS  Google Scholar 

  47. Khan WS, Adesida AB, Tew SR, Andrew JG, Hardingham TE (2009) The epitope characterisation and the osteogenic differentiation potential of human fat pad-derived stem cells is maintained with ageing in later life. Injury 40:150–157

    CAS  Google Scholar 

  48. Weinzierl K, Hemprich A, Frerich B (2006) Bone engineering with adipose tissue derived stromal cells. J Craniomaxillofac Surg 34:466–471

    Google Scholar 

  49. Ferguson RE, Cui X, Fink BF, Vasconez HC, Pu LL (2008) The viability of autologous fat grafts harvested with the LipiVage system: a comparative study. Ann Plast Surg 60:594–597

    CAS  Google Scholar 

  50. Jurgens WJ, Oedayrajsingh-Varma MJ, Helder MN, Zandiehdoulabi B, Schouten TE, Kuik DJ, Ritt MJ, van Milligen FJ (2008) Effect of tissue-harvesting site on yield of stem cells derived from adipose tissue: implications for cell-based therapies. Cell Tissue Res 332:415–426

    Google Scholar 

  51. Tchkonia T, Giorgadze N, Pirtskhalava T, Tchoukalova Y, Karagiannides I, Forse RA, DePonte M, Stevenson M, Guo W, Han J, Waloga G, Lash TL, Jensen MD, Kirkland JL (2002) Fat depot origin affects adipogenesis in primary cultured and cloned human preadipocytes. Am J Physiol Regul Integr Comp Physiol 282:R1286–R1296

    CAS  Google Scholar 

  52. Hauner H, Entenmann G (1991) Regional variation of adipose differentiation in cultured stromal-vascular cells from the abdominal and femoral adipose tissue of obese women. Int J Obes 15:121–126

    CAS  Google Scholar 

  53. Vasconez LG, de la Torre JI (2006) Abdominoplasty. In: Mathes (ed) Plastic Surgery. Saunders Elsevier, Philadelphia, pp 87–117

    Google Scholar 

  54. Pitanguy I (1967) Abdominal lipectomy – an approach to it through an analysis of 300 consecutive cases. Plast Reconstr Surg 30:384–391

    Google Scholar 

  55. Pitanguy I (1964) Dermolipectomy of the abdominal wall, thighs, buttocks, and upper extremity. In: Converse JM (ed) Reconstructive plastic surgery. Saunders, Philadelphia

    Google Scholar 

  56. Pitanguy I (1971) Surgical reduction of the abdomen, thigh, and buttocks. Surg Clin North Am 51:479–489

    CAS  Google Scholar 

  57. Psillakis JM (1984) Plastic surgery of the abdomen with improvement in the body contour. Physiopathology and treatment of the aponeurotic musculature. Clin Plast Surg 11:465–477

    CAS  Google Scholar 

  58. Regnault P (1975) Abdominoplasty by the W technique. Plast Reconstr Surg 55:265–274

    CAS  Google Scholar 

  59. VERNON S (1957) Umbilical transplantation upward and abdominal contouring in lipectomy. Am J Surg 94:490–492

    CAS  Google Scholar 

  60. Smith P, Adams WP Jr, Lipschitz AH, Chau B, Sorokin E, Rohrich RJ, Brown SA (2006) Autologous human fat grafting: effect of harvesting and preparation techniques on adipocyte graft survival. Plast Reconstr Surg 117:1836–1844

    CAS  Google Scholar 

  61. Coleman SR (1997) Facial recontouring with lipostructure. Clin Plast Surg 24:347–367

    CAS  Google Scholar 

  62. Coleman SR (2001) Structural fat grafts: the ideal filler? Clin Plast Surg 28:111–119

    CAS  Google Scholar 

  63. Coleman SR (2002) Hand rejuvenation with structural fat grafting. Plast Reconstr Surg 110:1731–1744

    Google Scholar 

  64. Pu LL, Coleman SR, Cui X, Ferguson RE Jr, Vasconez HC (2008) Autologous fat grafts harvested and refined by the Coleman technique: a comparative study. Plast Reconstr Surg 122:932–937

    CAS  Google Scholar 

  65. Gonzalez AM, Lobocki C, Kelly CP, Jackson IT (2007) An alternative method for harvest and processing fat grafts: an in vitro study of cell viability and survival. Plast Reconstr Surg 120:285–294

    CAS  Google Scholar 

  66. Jackson IT, Simman R, Tholen R, DiNick VD (2001) A successful long-term method of fat grafting: recontouring of a large subcutaneous postradiation thigh defect with autologous fat transplantation. Aesthetic Plast Surg 25:165–169

    CAS  Google Scholar 

  67. Coleman SR, Saboeiro AP (2007) Fat grafting to the breast revisited: safety and efficacy. Plast Reconstr Surg 119:775–785

    CAS  Google Scholar 

  68. Lalikos JF, Li YQ, Roth TP, Doyle JW, Matory WE, Lawrence WT (1997) Biochemical assessment of cellular damage after adipocyte harvest. J Surg Res 70:95–100

    CAS  Google Scholar 

  69. Moore JH Jr, Kolaczynski JW, Morales LM, Considine RV, Pietrzkowski Z, Noto PF, Caro JF (1995) Viability of fat obtained by syringe suction lipectomy: effects of local anesthesia with lidocaine. Aesthetic Plast Surg 19:335–339

    Google Scholar 

  70. Rodbell M (1966) Metabolism of isolated fat cells. II. The similar effects of phospholipase C (Clostridium perfringens alpha toxin) and of insulin on glucose and amino acid metabolism. J Biol Chem 241:130–139

    CAS  Google Scholar 

  71. Rodbell M (1966) The metabolism of isolated fat cells. IV. Regulation of release of protein by lipolytic hormones and insulin. J Biol Chem 241:3909–3917

    CAS  Google Scholar 

  72. Rodbell M, Jones AB (1966) Metabolism of isolated fat cells. 3. The similar inhibitory action of phospholipase C (Clostridium perfringens alpha toxin) and of insulin on lipolysis stimulated by lipolytic hormones and theophylline. J Biol Chem 241:140–142

    CAS  Google Scholar 

  73. Pilgaard L, Lund P, Rasmussen JG, Fink T, Zachar V (2008) Comparative analysis of highly defined proteases for the isolation of adipose tissue-derived stem cells. Regen Med 3:705–715

    CAS  Google Scholar 

  74. Zhu Y, Liu T, Song K, Fan X, Ma X, Cui Z (2008) Adipose-derived stem cell: a better stem cell than BMSC. Cell Biochem Funct 26:664–675

    CAS  Google Scholar 

  75. Hattori H, Masuoka K, Sato M, Ishihara M, Asazuma T, Takase B, Kikuchi M, Nemoto K, Ishihara M (2006) Bone formation using human adipose tissue-derived stromal cells and a biodegradable scaffold. J Biomed Mater Res B Appl Biomater 76:230–239

    Google Scholar 

  76. Lee RH, Kim B, Choi I, Kim H, Choi HS, Suh K, Bae YC, Jung JS (2004) Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem 14:311–324

    CAS  Google Scholar 

  77. Pu LL, Cui X, Fink BF, Gao D, Vasconez HC (2006) Adipose aspirates as a source for human processed lipoaspirate cells after optimal cryopreservation. Plast Reconstr Surg 117:1845–1850

    CAS  Google Scholar 

  78. Dominici M, Le BK, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 8:315–317

    CAS  Google Scholar 

  79. Dragoo JL, Choi JY, Lieberman JR, Huang J, Zuk PA, Zhang J, Hedrick MH, Benhaim P (2003) Bone induction by BMP-2 transduced stem cells derived from human fat. J Orthop Res 21:622–629

    CAS  Google Scholar 

  80. Miyazaki M, Zuk PA, Zou J, Yoon SH, Wei F, Morishita Y, Sintuu C, Wang JC (2008) Comparison of human mesenchymal stem cells derived from adipose tissue and bone marrow for ex vivo gene therapy in rat spinal fusion model. Spine (Phila Pa 1976) 33:863–869

    Google Scholar 

  81. Galie M, Pignatti M, Scambi I, Sbarbati A, Rigotti G (2008) Comparison of different centrifugation protocols for the best yield of adipose-derived stromal cells from lipoaspirates. Plast Reconstr Surg 122:233e–234e

    CAS  Google Scholar 

  82. Kim WS, Park BS, Kim HK, Park JS, Kim KJ, Choi JS, Chung SJ, Kim DD, Sung JH (2008) Evidence supporting antioxidant action of adipose-derived stem cells: protection of human dermal fibroblasts from oxidative stress. J Dermatol Sci 49:133–142

    CAS  Google Scholar 

  83. Kim WS, Park BS, Park SH, Kim HK, Sung JH (2009) Antiwrinkle effect of adipose-derived stem cell: activation of dermal fibroblast by secretory factors. J Dermatol Sci 53:96–102

    CAS  Google Scholar 

  84. Kim WS, Park BS, Sung JH (2009) Protective role of adipose-derived stem cells and their soluble factors in photoaging. Arch Dermatol Res 301:329–336

    Google Scholar 

  85. Kim WS, Park BS, Sung JH, Yang JM, Park SB, Kwak SJ, Park JS (2007) Wound healing effect of adipose-derived stem cells: a critical role of secretory factors on human dermal fibroblasts. J Dermatol Sci 48:15–24

    CAS  Google Scholar 

  86. Kim WS, Park SH, Ahn SJ, Kim HK, Park JS, Lee GY, Kim KJ, Whang KK, Kang SH, Park BS, Sung JH (2008) Whitening effect of adipose-derived stem cells: a critical role of TGF-beta 1. Biol Pharm Bull 31:606–610

    CAS  Google Scholar 

  87. Martinez-Lorenzo MJ, Royo-Canas M, Alegre-Aguaron E, Desportes P, Castiella T, Garcia-Alvarez F, Larrad L (2009) Phenotype and chondrogenic differentiation of mesenchymal cells from adipose tissue of different species. J Orthop Res 27:1499–1507

    Google Scholar 

  88. Gonzalez MA, Gonzalez-Rey E, Rico L, Buscher D, Delgado M (2009) Adipose-derived mesenchymal stem cells alleviate experimental colitis by inhibiting inflammatory and autoimmune responses. Gastroenterology 136:978–989

    Google Scholar 

  89. Gonzalez MA, Gonzalez-Rey E, Rico L, Buscher D, Delgado M (2009) Treatment of experimental arthritis by inducing immune tolerance with human adipose-derived mesenchymal stem cells. Arthritis Rheum 60:1006–1019

    CAS  Google Scholar 

  90. Dragoo JL, Carlson G, McCormick F, Khan-Farooqi H, Zhu M, Zuk PA, Benhaim P (2007) Healing full-thickness cartilage defects using adipose-derived stem cells. Tissue Eng 13:1615–1621

    CAS  Google Scholar 

  91. Estes BT, Wu AW, Guilak F (2006) Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenetic protein 6. Arthritis Rheum 54:1222–1232

    CAS  Google Scholar 

  92. Nakagami H, Maeda K, Morishita R, Iguchi S, Nishikawa T, Takami Y, Kikuchi Y, Saito Y, Tamai K, Ogihara T, Kaneda Y (2005) Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arterioscler Thromb Vasc Biol 25:2542–2547

    CAS  Google Scholar 

  93. 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. J Atheroscler Thromb 13:77–81

    Google Scholar 

  94. Bjorntorp P, Karlsson M, Pertoft H, Pettersson P, Sjostrom L, Smith U (1978) Isolation and characterization of cells from rat adipose tissue developing into adipocytes. J Lipid Res 19:316–324

    CAS  Google Scholar 

  95. Iwashima S, Ozaki T, Maruyama S, Saka Y, Kobori M, Omae K, Yamaguchi H, Niimi T, Toriyama K, Kamei Y, Torii S, Murohara T, Yuzawa Y, Kitagawa Y, Matsuo S (2009) Novel culture system of mesenchymal stromal cells from human subcutaneous adipose tissue. Stem Cells Dev 18:533–543

    CAS  Google Scholar 

  96. Chiou M, Xu Y, Longaker MT (2006) Mitogenic and chondrogenic effects of fibroblast growth factor-2 in adipose-derived mesenchymal cells. Biochem Biophys Res Commun 343:644–652

    CAS  Google Scholar 

  97. Jeon ES, Moon HJ, Lee MJ, Song HY, Kim YM, Bae YC, Jung JS, Kim JH (2006) Sphingosylphosphorylcholine induces differentiation of human mesenchymal stem cells into smooth-muscle-like cells through a TGF-beta-dependent mechanism. J Cell Sci 119:4994–5005

    CAS  Google Scholar 

  98. Kang YJ, Jeon ES, Song HY, Woo JS, Jung JS, Kim YK, Kim JH (2005) 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 95:1135–1145

    CAS  Google Scholar 

  99. Song HY, Jeon ES, Jung JS, Kim JH (2005) Oncostatin M induces proliferation of human adipose tissue-derived mesenchymal stem cells. Int J Biochem Cell Biol 37:2357–2365

    CAS  Google Scholar 

  100. Haynesworth SE, Baber MA, Caplan AI (1992) Cell surface antigens on human marrow-derived mesenchymal cells are detected by monoclonal antibodies. Bone 13:69–80

    CAS  Google Scholar 

  101. Gronthos S, Graves SE, Ohta S, Simmons PJ (1994) The STRO-1+ fraction of adult human bone marrow contains the osteogenic precursors. Blood 84:4164–4173

    CAS  Google Scholar 

  102. McIntosh K, Zvonic S, Garrett S, Mitchell JB, Floyd ZE, Hammill L, Kloster A, Di HY, Ting JP, Storms RW, Goh B, Kilroy G, Wu X, Gimble JM (2006) The immunogenicity of human adipose-derived cells: temporal changes in vitro. Stem Cells 24:1246–1253

    CAS  Google Scholar 

  103. Katz AJ, Tholpady A, Tholpady SS, Shang H, Ogle RC (2005) Cell surface and transcriptional characterization of human adipose-derived adherent stromal (hADAS) cells. Stem Cells 23:412–423

    CAS  Google Scholar 

  104. Kershaw EE, Flier JS (2004) Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89:2548–2556

    CAS  Google Scholar 

  105. de Villiers JA, Houreld N, Abrahamse H (2009) Adipose derived stem cells and smooth muscle cells: implications for regenerative medicine. Stem Cell Rev Rep 5:256–265

    Google Scholar 

  106. Wang B, Han J, Gao Y, Xiao Z, Chen B, Wang X, Zhao W, Dai J (2007) The differentiation of rat adipose-derived stem cells into OEC-like cells on collagen scaffolds by co-culturing with OECs. Neurosci Lett 421:191–196

    CAS  Google Scholar 

  107. Fraser JK, Schreiber R, Strem B, Zhu M, Alfonso Z, Wulur I, Hedrick MH (2006) Plasticity of human adipose stem cells toward endothelial cells and cardiomyocytes. Nat Clin Pract Cardiovasc Med 3(Suppl 1):S33–S37

    CAS  Google Scholar 

  108. Tang QQ, Otto TC, Lane MD (2004) Commitment of C3H10T1/2 pluripotent stem cells to the adipocyte lineage. Proc Natl Acad Sci USA 101:9607–9611

    CAS  Google Scholar 

  109. Otto TC, Lane MD (2005) Adipose development: from stem cell to adipocyte. Crit Rev Biochem Mol Biol 40:229–242

    CAS  Google Scholar 

  110. Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, MacDougald OA (2000) Inhibition of adipogenesis by Wnt signaling. Science 289:950–953

    CAS  Google Scholar 

  111. Park JR, Jung JW, Lee YS, Kang KS (2008) The roles of Wnt antagonists Dkk1 and sFRP4 during adipogenesis of human adipose tissue-derived mesenchymal stem cells. Cell Prolif 41:859–874

    CAS  Google Scholar 

  112. Gregoire FM, Smas CM, Sul HS (1998) Understanding adipocyte differentiation. Physiol Rev 78:783–809

    CAS  Google Scholar 

  113. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6:483–495

    CAS  Google Scholar 

  114. Pairault J, Green H (1979) A study of the adipose conversion of suspended 3T3 cells by using glycerophosphate dehydrogenase as differentiation marker. Proc Natl Acad Sci USA 76:5138–5142

    CAS  Google Scholar 

  115. Kakudo N, Shimotsuma A, Kusumoto K (2007) Fibroblast growth factor-2 stimulates adipogenic differentiation of human adipose-derived stem cells. Biochem Biophys Res Commun 359:239–244

    CAS  Google Scholar 

  116. Spiegelman BM (1998) PPAR-gamma: adipogenic regulator and thiazolidinedione receptor. Diabetes 47:507–514

    CAS  Google Scholar 

  117. Hong L, Colpan A, Peptan IA, Daw J, George A, Evans CA (2007) 17-Beta estradiol enhances osteogenic and adipogenic differentiation of human adipose-derived stromal cells. Tissue Eng 13:1197–1203

    CAS  Google Scholar 

  118. Cooke PS, Naaz A (2004) Role of estrogens in adipocyte development and function. Exp Biol Med (Maywood) 229:1127–1135

    CAS  Google Scholar 

  119. Urist MR (1965) Bone: formation by autoinduction. Science 150:893–899

    CAS  Google Scholar 

  120. Hamid AA, Ruszymah BH, Aminuddin BS, Sathappan S, Chua KH (2008) Differential gene expression of human adipose-derived stem cells in osteogenic induction. Med J Malaysia 63(Suppl A):9–10

    Google Scholar 

  121. Mischen BT, Follmar KE, Moyer KE, Buehrer B, Olbrich KC, Levin LS, Klitzman B, Erdmann D (2008) Metabolic and functional characterization of human adipose-derived stem cells in tissue engineering. Plast Reconstr Surg 122:725–738

    CAS  Google Scholar 

  122. Tjabringa GS, Vezeridis PS, Zandieh-Doulabi B, Helder MN, Wuisman PI, Klein-Nulend J (2006) Polyamines modulate nitric oxide production and COX-2 gene expression in response to mechanical loading in human adipose tissue-derived mesenchymal stem cells. Stem Cells 24:2262–2269

    CAS  Google Scholar 

  123. Al-Salleeh F, Beatty MW, Reinhardt RA, Petro TM, Crouch L (2008) Human osteogenic protein-1 induces osteogenic differentiation of adipose-derived stem cells harvested from mice. Arch Oral Biol 53:928–936

    CAS  Google Scholar 

  124. Yang M, Ma QJ, Dang GT, Ma K, Chen P, Zhou CY (2005) In vitro and in vivo induction of bone formation based on ex vivo gene therapy using rat adipose-derived adult stem cells expressing BMP-7. Cytotherapy 7:273–281

    CAS  Google Scholar 

  125. Zhang X, Yang M, Lin L, Chen P, Ma KT, Zhou CY, Ao YF (2006) Runx2 overexpression enhances osteoblastic differentiation and mineralization in adipose–derived stem cells in vitro and in vivo. Calcif Tissue Int 79:169–178

    CAS  Google Scholar 

  126. Knippenberg M, Helder MN, Zandieh DB, Wuisman PI, Klein-Nulend J (2006) Osteogenesis versus chondrogenesis by BMP-2 and BMP-7 in adipose stem cells. Biochem Biophys Res Commun 342:902–908

    CAS  Google Scholar 

  127. Boeuf S, Borger M, Hennig T, Winter A, Kasten P, Richter W (2009) Enhanced ITM2A expression inhibits chondrogenic differentiation of mesenchymal stem cells. Differentiation 78:108–115

    CAS  Google Scholar 

  128. Awad HA, Halvorsen YD, Gimble JM, Guilak F (2003) Effects of transforming growth factor beta1 and dexamethasone on the growth and chondrogenic differentiation of adipose-derived stromal cells. Tissue Eng 9:1301–1312

    CAS  Google Scholar 

  129. Buxton P, Edwards C, Archer CW, Francis-West P (2001) Growth/differentiation factor-5 (GDF-5) and skeletal development. J Bone Joint Surg Am 83-A(Suppl 1):S23–S30

    Google Scholar 

  130. Feng G, Wan Y, Balian G, Laurencin CT, Li X (2008) Adenovirus-mediated expression of growth and differentiation factor-5 promotes chondrogenesis of adipose stem cells. Growth Factors 26:132–142

    CAS  Google Scholar 

  131. Pilgaard L, Lund P, Duroux M, Fink T, Ulrich-Vinther M, Soballe K, Zachar V (2009) Effect of oxygen concentration, culture format and donor variability on in vitro chondrogenesis of human adipose tissue-derived stem cells. Regen Med 4:539–548

    CAS  Google Scholar 

  132. Lin Y, Luo E, Chen X, Liu L, Qiao J, Yan Z, Li Z, Tang W, Zheng X, Tian W (2005) Molecular and cellular characterization during chondrogenic differentiation of adipose tissue-derived stromal cells in vitro and cartilage formation in vivo. J Cell Mol Med 9:929–939

    CAS  Google Scholar 

  133. Xu Y, Balooch G, Chiou M, Bekerman E, Ritchie RO, Longaker MT (2007) Analysis of the material properties of early chondrogenic differentiated adipose-derived stromal cells (ASC) using an in vitro three-dimensional micromass culture system. Biochem Biophys Res Commun 359:311–316

    CAS  Google Scholar 

  134. Lu Z, Zandieh-Doulabi B, Huang C, Bank RA, Helder M (2009) Collagen Type II enhances chondrogenesis in adipose tissue-derived stem cells by affecting cell shape. Tissue Eng Part A [Epub ahead of print]

    Google Scholar 

  135. Han Y, Wei Y, Wang S, Song Y (2009) Enhanced chondrogenesis of adipose-derived stem cells by the controlled release of transforming growth factor-beta1 from hybrid microspheres. Gerontology 55:592–599

    CAS  Google Scholar 

  136. Estes BT, Wu AW, Storms RW, Guilak F (2006) Extended passaging, but not aldehyde dehydrogenase activity, increases the chondrogenic potential of human adipose-derived adult stem cells. J Cell Physiol 209:987–995

    CAS  Google Scholar 

  137. Kim JM, Lee ST, Chu K, Jung KH, Song EC, Kim SJ, Sinn DI, Kim JH, Park DK, Kang KM, Hyung HN, Park HK, Won CH, Kim KH, Kim M, Kun LS, Roh JK (2007) Systemic transplantation of human adipose stem cells attenuated cerebral inflammation and degeneration in a hemorrhagic stroke model. Brain Res 1183:43–50

    CAS  Google Scholar 

  138. Gimble JM, Katz AJ, Bunnell BA (2007) Adipose-derived stem cells for regenerative medicine. Circ Res 100:1249–1260

    CAS  Google Scholar 

  139. Cho SW, Kim I, Kim SH, Rhie JW, Choi CY, Kim BS (2006) Enhancement of adipose tissue formation by implantation of adipogenic-differentiated preadipocytes. Biochem Biophys Res Commun 345:588–594

    CAS  Google Scholar 

  140. Bhang SH, Kim JH, Yang HS, La WG, Lee TJ, Sun AY, Kim GH, Lee M, Kim BS (2009) Combined delivery of heme oxygenase-1 gene and fibroblast growth factor-2 protein for therapeutic angiogenesis. Biomaterials 30:6247–6256

    CAS  Google Scholar 

  141. Wei X, Du Z, Zhao L, Feng D, Wei G, He Y, Tan J, Lee WH, Hampel H, Dodel R, Johnstone BH, March KL, Farlow MR, Du Y (2009) IFATS collection: the conditioned media of adipose stromal cells protect against hypoxia-ischemia-induced brain damage in neonatal rats. Stem Cells 27:478–488

    CAS  Google Scholar 

  142. Kang JW, Kang KS, Koo HC, Park JR, Choi EW, Park YH (2008) Soluble factors-mediated immunomodulatory effects of canine adipose tissue-derived mesenchymal stem cells. Stem Cells Dev 17:681–693

    CAS  Google Scholar 

  143. Neels JG, Thinnes T, Loskutoff DJ (2004) Angiogenesis in an in vivo model of adipose tissue development. FASEB J 18:983–985

    CAS  Google Scholar 

  144. Moon MH, Kim SY, Kim YJ, Kim SJ, Lee JB, Bae YC, Sung SM, Jung JS (2006) Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Cell Physiol Biochem 17:279–290

    CAS  Google Scholar 

  145. Kim Y, Kim H, Cho H, Bae Y, Suh K, Jung J (2007) Direct comparison of human mesenchymal stem cells derived from adipose tissues and bone marrow in mediating neovascularization in response to vascular ischemia. Cell Physiol Biochem 20:867–876

    CAS  Google Scholar 

  146. Kondo K, Shintani S, Shibata R, Murakami H, Murakami R, Imaizumi M, Kitagawa Y, Murohara T (2009) Implantation of adipose-derived regenerative cells enhances ischemia-induced angiogenesis. Arterioscler Thromb Vasc Biol 29:61–66

    CAS  Google Scholar 

  147. Wang L, Deng J, Tian W, Xiang B, Yang T, Li G, Wang J, Gruwel M, Kashour T, Rendell J, Glogowski M, Tomanek B, Freed D, Deslauriers R, Arora RC, Tian G (2009) Adipose-derived stem cells are an effective cell candidate for treatment of heart failure – an MR imaging study of rat hearts. Am J Physiol Heart Circ Physiol 297:H1020–H1031

    CAS  Google Scholar 

  148. Schenke-Layland K, Strem BM, Jordan MC, Deemedio MT, Hedrick MH, Roos KP, Fraser JK, Maclellan WR (2009) Adipose tissue-derived cells improve cardiac function following myocardial infarction. J Surg Res 153:217–223

    CAS  Google Scholar 

  149. Okura H, Matsuyama A, Lee CM, Saga A, Kakuta-Yamamoto A, Nagao A, Sougawa N, Sekiya N, Takekita K, Shudo Y, Miyagawa S, Komoda H, Okano T, Sawa Y (2009) Cardiomyoblast-like cells differentiated from human adipose tissue-derived mesenchymal stem cells improve left ventricular dysfunction and survival in a rat myocardial infarction model. Tissue Eng Part C Methods [Epub ahead of print]

    Google Scholar 

  150. van der Bogt KE, Schrepfer S, Yu J, Sheikh AY, Hoyt G, Govaert JA, Velotta JB, Contag CH, Robbins RC, Wu JC (2009) Comparison of transplantation of adipose tissue- and bone marrow-derived mesenchymal stem cells in the infarcted heart. Transplantation 87:642–652

    Google Scholar 

  151. Bailey AM, Lawrence MB, Shang H, Katz AJ, Peirce SM (2009) Agent-based model of therapeutic adipose-derived stromal cell trafficking during ischemia predicts ability to roll on P-selectin. PLoS Comput Biol 5:e1000294

    Google Scholar 

  152. Kang SK, Lee DH, Bae YC, Kim HK, Baik SY, Jung JS (2003) Improvement of neurological deficits by intracerebral transplantation of human adipose tissue-derived stromal cells after cerebral ischemia in rats. Exp Neurol 183:355–366

    CAS  Google Scholar 

  153. Lee TH, Yoon JG (2008) Intracerebral transplantation of human adipose tissue stromal cells after middle cerebral artery occlusion in rats. J Clin Neurosci 15:907–912

    Google Scholar 

  154. Rice HE, Hsu EW, Sheng H, Evenson DA, Freemerman AJ, Safford KM, Provenzale JM, Warner DS, Johnson GA (2007) Superparamagnetic iron oxide labeling and transplantation of adipose-derived stem cells in middle cerebral artery occlusion-injured mice. AJR Am J Roentgenol 188:1101–1108

    Google Scholar 

  155. Zhao L, Wei X, Ma Z, Feng D, Tu P, Johnstone BH, March KL, Du Y (2009) Adipose stromal cells-conditional medium protected glutamate-induced CGNs neuronal death by BDNF. Neurosci Lett 452:238–240

    CAS  Google Scholar 

  156. Kulikov AV, Stepanova MS, Stvolinsky SL, Hudoerkov RM, Voronkov DN, Rzhaninova AA, Goldstein DV, Boldyrev AA (2008) Application of multipotent mesenchymal stromal cells from human adipose tissue for compensation of neurological deficiency induced by 3-nitropropionic acid in rats. Bull Exp Biol Med 145:514–519

    CAS  Google Scholar 

  157. Kang SK, Shin MJ, Jung JS, Kim YG, Kim CH (2006) Autologous adipose tissue-derived stromal cells for treatment of spinal cord injury. Stem Cells Dev 15:583–594

    CAS  Google Scholar 

  158. Riordan NH, Ichim TE, Min WP, Wang H, Solano F, Lara F, Alfaro M, Rodriguez JP, Harman RJ, Patel AN, Murphy MP, Lee RR, Minev B (2009) Non-expanded adipose stromal vascular fraction cell therapy for multiple sclerosis. J Transl Med 7:29

    Google Scholar 

  159. Lendeckel S, Jodicke A, Christophis P, Heidinger K, Wolff J, Fraser JK, Hedrick MH, Berthold L, Howaldt HP (2004) Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. J Craniomaxillofac Surg 32:370–373

    Google Scholar 

  160. Cowan CM, Shi YY, Aalami OO, Chou YF, Mari C, Thomas R, Quarto N, Contag CH, Wu B, Longaker MT (2004) Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat Biotechnol 22:560–567

    CAS  Google Scholar 

  161. Follmar KE, Prichard HL, Decroos FC, Wang HT, Levin LS, Klitzman B, Olbrich KC, Erdmann D (2007) Combined bone allograft and adipose-derived stem cell autograft in a rabbit model. Ann Plast Surg 58:561–565

    CAS  Google Scholar 

  162. Peterson B, Zhang J, Iglesias R, Kabo M, Hedrick M, Benhaim P, Lieberman JR (2005) Healing of critically sized femoral defects, using genetically modified mesenchymal stem cells from human adipose tissue. Tissue Eng 11:120–129

    CAS  Google Scholar 

  163. Zhang HN, Li L, Leng P, Wang YZ, Lv CY (2009) Uninduced adipose-derived stem cells repair the defect of full-thickness hyaline cartilage. Chin J Traumatol 12:92–97

    Google Scholar 

  164. Rigotti G, Marchi A, Galie M, Baroni G, Benati D, Krampera M, Pasini A, Sbarbati A (2007) Clinical treatment of radiotherapy tissue damage by lipoaspirate transplant: a healing process mediated by adipose-derived adult stem cells. Plast Reconstr Surg 119:1409–1422

    CAS  Google Scholar 

  165. Perbeck LG, Celebioglu F, Danielsson R, Bone B, Aastrup M, Svensson L (2001) Circulation in the breast after radiotherapy and breast conservation. Eur J Surg 167:497–500

    CAS  Google Scholar 

  166. Parker AM, Rodeheaver G, Salopek L, Shang H, Khurgel M, Katz A (2006) Accelerated wound healing in a murine model with the application of multipotent human adipose derived stem cells. J Am Coll Surg 203:S43

    Google Scholar 

  167. Nambu M, Ishihara M, Nakamura S, Mizuno H, Yanagibayashi S, Kanatani Y, Hattori H, Takase B, Ishizuka T, Kishimoto S, Amano Y, Yamamoto N, Azuma R, Kiyosawa T (2007) Enhanced healing of mitomycin C-treated wounds in rats using inbred adipose tissue-derived stromal cells within an atelocollagen matrix. Wound Repair Regen 15:505–510

    Google Scholar 

  168. Nambu M, Kishimoto S, Nakamura S, Mizuno H, Yanagibayashi S, Yamamoto N, Azuma R, Nakamura S, Kiyosawa T, Ishihara M, Kanatani Y (2009) Accelerated wound healing in healing-impaired db/db mice by autologous adipose tissue-derived stromal cells combined with atelocollagen matrix. Ann Plast Surg 62:317–321

    CAS  Google Scholar 

  169. Kim WS, Park BS, Sung JH (2009) The wound-healing and antioxidant effects of adipose-derived stem cells. Expert Opin Biol Ther 9:879–887

    CAS  Google Scholar 

  170. Puissant B, Barreau C, Bourin P, Clavel C, Corre J, Bousquet C, Taureau C, Cousin B, Abbal M, Laharrague P, Penicaud L, Casteilla L, Blancher A (2005) Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 129:118–129

    Google Scholar 

  171. Keyser KA, Beagles KE, Kiem HP (2007) Comparison of mesenchymal stem cells from different tissues to suppress T-cell activation. Cell Transplant 16:555–562

    Google Scholar 

  172. Yanez R, Lamana ML, Garcia-Castro J, Colmenero I, Ramirez M, Bueren JA (2006) Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 24:2582–2591

    CAS  Google Scholar 

  173. Le BK, Rasmusson I, Sundberg B, Gotherstrom C, Hassan M, Uzunel M, Ringden O (2004) Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363:1439–1441

    Google Scholar 

  174. Fang B, Song Y, Li N, Li J, Han Q, Zhao RC (2009) Mesenchymal stem cells for the treatment of refractory pure red cell aplasia after major ABO-incompatible hematopoietic stem cell transplantation. Ann Hematol 88:261–266

    Google Scholar 

  175. Fang B, Song Y, Liao L, Zhang Y, Zhao RC (2007) Favorable response to human adipose tissue-derived mesenchymal stem cells in steroid-refractory acute graft-versus-host disease. Transplant Proc 39:3358–3362

    CAS  Google Scholar 

  176. Fang B, Song Y, Lin Q, Zhang Y, Cao Y, Zhao RC, Ma Y (2007) Human adipose tissue-derived mesenchymal stromal cells as salvage therapy for treatment of severe refractory acute graft-vs.-host disease in two children. Pediatr Transplant 11:814–817

    CAS  Google Scholar 

  177. Fang B, Song Y, Zhao RC, Han Q, Lin Q (2007) Using human adipose tissue-derived mesenchymal stem cells as salvage therapy for hepatic graft-versus-host disease resembling acute hepatitis. Transplant Proc 39:1710–1713

    CAS  Google Scholar 

  178. Fang B, Song YP, Liao LM, Han Q, Zhao RC (2006) Treatment of severe therapy-resistant acute graft-versus-host disease with human adipose tissue-derived mesenchymal stem cells. Bone Marrow Transplant 38:389–390

    CAS  Google Scholar 

  179. Gonzalez-Rey E, Anderson P, Gonzalez MA, Rico L, Buscher D, Delgado M (2009) Human adult stem cells derived from adipose tissue protect against experimental colitis and sepsis. Gut 58:929–939

    CAS  Google Scholar 

  180. Gonzalez-Rey E, Gonzalez MA, Varela N, O’Valle F, Hernandez-Cortes P, Rico L, Buscher D, Delgado M (2009) Human adipose-derived mesenchymal stem cells reduce inflammatory and T-cell responses and induce regulatory T cells in vitro in rheumatoid arthritis. Ann Rheum Dis 69(1):241–248

    Google Scholar 

  181. Garcia-Olmo D, Garcia-Arranz M, Garcia LG, Cuellar ES, Blanco IF, Prianes LA, Montes JA, Pinto FL, Marcos DH, Garcia-Sancho L (2003) Autologous stem cell transplantation for treatment of rectovaginal fistula in perianal Crohn’s disease: a new cell-based therapy. Int J Colorectal Dis 18:451–454

    Google Scholar 

  182. Garcia-Olmo D, Garcia-Arranz M, Herreros D, Pascual I, Peiro C, Rodriguez-Montes JA (2005) A phase I clinical trial of the treatment of Crohn’s fistula by adipose mesenchymal stem cell transplantation. Dis Colon Rectum 48:1416–1423

    Google Scholar 

  183. Garcia-Olmo D, Herreros D, Pascual I, Pascual JA, Del-Valle E, Zorrilla J, De-La-Quintana P, Garcia-Arranz M, Pascual M (2009) Expanded adipose-derived stem cells for the treatment of complex perianal fistula: a phase II clinical trial. Dis Colon Rectum 52:79–86

    Google Scholar 

  184. Garcia-Olmo D, Herreros D, Pascual M, Pascual I, De-La-Quintana P, Trebol J, Garcia-Arranz M (2009) 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 24:27–30

    Google Scholar 

  185. Alvarez PD, Garcia-Arranz M, Georgiev-Hristov T, Garcia-Olmo D (2008) A new bronchoscopic treatment of tracheomediastinal fistula using autologous adipose-derived stem cells. Thorax 63:374–376

    Google Scholar 

  186. Matsumoto D, Sato K, Gonda K, Takaki Y, Shigeura T, Sato T, Iba-Kojima E, Iizuka F, Inoue K, Suga H, Yoshimura K (2006) Cell-assisted lipotransfer: supportive use of human adipose-derived cells for soft tissue augmentation with lipoinjection. Tissue Eng 12:3375–3382

    CAS  Google Scholar 

  187. Yoshimura K, Sato K, Aoi N, Kurita M, Hirohi T, Harii K (2008) Cell-assisted lipotransfer for cosmetic breast augmentation: supportive use of adipose-derived stem/stromal cells. Aesthetic Plast Surg 32:48–55

    Google Scholar 

  188. Yoshimura K, Sato K, Aoi N, Kurita M, Inoue K, Suga H, Eto H, Kato H, Hirohi T, Harii K (2008) Cell-assisted lipotransfer for facial lipoatrophy: efficacy of clinical use of adipose-derived stem cells. Dermatol Surg 34:1178–1185

    CAS  Google Scholar 

  189. Pulagam SR, Poulton T, Mamounas EP (2006) Long-term clinical and radiologic results with autologous fat transplantation for breast augmentation: case reports and review of the literature. Breast J 12:63–65

    Google Scholar 

  190. Patrick CW Jr, Chauvin PB, Hobley J, Reece GP (1999) Preadipocyte seeded PLGA scaffolds for adipose tissue engineering. Tissue Eng 5:139–151

    CAS  Google Scholar 

  191. Lee JA, Parrett BM, Conejero JA, Laser J, Chen J, Kogon AJ, Nanda D, Grant RT, Breitbart AS (2003) Biological alchemy: engineering bone and fat from fat-derived stem cells. Ann Plast Surg 50:610–617

    Google Scholar 

  192. von Heimburg D, Zachariah S, Low A, Pallua N (2001) Influence of different biodegradable carriers on the in vivo behavior of human adipose precursor cells. Plast Reconstr Surg 108:411–420

    Google Scholar 

  193. Hemmrich K, von Heimburg D, Rendchen R, Di BC, Milella E, Pallua N (2005) Implantation of preadipocyte-loaded hyaluronic acid-based scaffolds into nude mice to evaluate potential for soft tissue engineering. Biomaterials 26:7025–7037

    CAS  Google Scholar 

  194. Huss FR, Kratz G (2001) Mammary epithelial cell and adipocyte co-culture in a 3-D matrix: the first step towards tissue-engineered human breast tissue. Cells Tissues Organs 169:361–367

    CAS  Google Scholar 

  195. Hong L, Peptan IA, Colpan A, Daw JL (2006) Adipose tissue engineering by human adipose-derived stromal cells. Cells Tissues Organs 183:133–140

    CAS  Google Scholar 

  196. Clark CP III (2007) Animal-based hyaluronic acid fillers: scientific and technical considerations. Plast Reconstr Surg 120:27S–32S

    CAS  Google Scholar 

  197. Scuderi N, Onesti MG, Bistoni G, Ceccarelli S, Rotolo S, Angeloni A, Marchese C (2008) The clinical application of autologous bioengineered skin based on a hyaluronic acid scaffold. Biomaterials 29:1620–1629

    CAS  Google Scholar 

  198. Halbleib M, Skurk T, de Luca C, von Heimburg D, Hauner H (2003) Tissue engineering of white adipose tissue using hyaluronic acid-based scaffolds. I: In vitro differentiation of human adipocyte precursor cells on scaffolds. Biomaterials 24:3125–3132

    CAS  Google Scholar 

  199. Vallée M, Côté JF, Fradette J. (2009) Adipose-tissue engineering: taking advantage of the properties of human adipose-derived stem/stromal cells. Pathol Biol 57(4): 309–317

    Google Scholar 

  200. Gabbay JS, Heller JB, Mitchell SA, Zuk PA, Spoon DB, Wasson KL, Jarrahy R, Benhaim P, Bradley JP (2006) Osteogenic potentiation of human adipose-derived stem cells in a 3-dimensional matrix. Ann Plast Surg 57:89–93

    CAS  Google Scholar 

  201. Scherberich A, Galli R, Jaquiery C, Farhadi J, Martin I (2007) Three-dimensional perfusion culture of human adipose tissue-derived endothelial and osteoblastic progenitors generates osteogenic constructs with intrinsic vascularization capacity. Stem Cells 25:1823–1829

    CAS  Google Scholar 

  202. de GL S, MF AE, Rimondini L, Albisetti W, Weinstein RL, Brini AT (2008) Human adipose-derived stem cells as future tools in tissue regeneration: osteogenic differentiation and cell-scaffold interaction. Int J Artif Organs 31:467–479

    Google Scholar 

  203. Lee JH, Rhie JW, Oh DY, Ahn ST (2008) Osteogenic differentiation of human adipose tissue-derived stromal cells (hASCs) in a porous three-dimensional scaffold. Biochem Biophys Res Commun 370:456–460

    CAS  Google Scholar 

  204. McCullen SD, Zhu Y, Bernacki SH, Narayan RJ, Pourdeyhimi B, Gorga RE, Loboa EG (2009) Electrospun composite poly(l-lactic acid)/tricalcium phosphate scaffolds induce proliferation and osteogenic differentiation of human adipose-derived stem cells. Biomed Mater 4:35002

    CAS  Google Scholar 

  205. Shen FH, Zeng Q, Lv Q, Choi L, Balian G, Li X, Laurencin CT (2006) Osteogenic differentiation of adipose-derived stromal cells treated with GDF-5 cultured on a novel three-dimensional sintered microsphere matrix. Spine J 6:615–623

    Google Scholar 

  206. Hao W, Hu YY, Wei YY, Pang L, Lv R, Bai JP, Xiong Z, Jiang M (2008) Collagen I gel can facilitate homogenous bone formation of adipose-derived stem cells in PLGA-beta-TCP scaffold. Cells Tissues Organs 187:89–102

    CAS  Google Scholar 

  207. Kakudo N, Shimotsuma A, Miyake S, Kushida S, Kusumoto K (2008) Bone tissue engineering using human adipose-derived stem cells and honeycomb collagen scaffold. J Biomed Mater Res A 84:191–197

    Google Scholar 

  208. Marino G, Rosso F, Cafiero G, Tortora C, Moraci M, Barbarisi M, Barbarisi A (2009) beta-Tricalcium phosphate 3D scaffold promote alone osteogenic differentiation of human adipose stem cells: in vitro study. J Mater Sci Mater Med [Epub ahead of print]

    Google Scholar 

  209. Liu Q, Cen L, Yin S, Chen L, Liu G, Chang J, Cui L (2008) A comparative study of proliferation and osteogenic differentiation of adipose-derived stem cells on akermanite and beta-TCP ceramics. Biomaterials 29:4792–4799

    CAS  Google Scholar 

  210. van GM, Diederichs S, Roeker S, Boehm S, Peterbauer A, Wolbank S, Riechers D, Stahl F, Kasper C (2009) Mechanical strain using 2D and 3D bioreactors induces osteogenesis: implications for bone tissue engineering. Adv Biochem Eng Biotechnol 112:95–123

    Google Scholar 

  211. Jeon O, Rhie JW, Kwon IK, Kim JH, Kim BS, Lee SH (2008) In vivo bone formation following transplantation of human adipose-derived stromal cells that are not differentiated osteogenically. Tissue Eng Part A 14:1285–1294

    CAS  Google Scholar 

  212. Jin XB, Sun YS, Zhang K, Wang J, Shi TP, Ju XD, Lou SQ (2008) Tissue engineered cartilage from hTGF beta2 transduced human adipose derived stem cells seeded in PLGA/alginate compound in vitro and in vivo. J Biomed Mater Res A 86:1077–1087

    Google Scholar 

  213. Jung Y, Chung YI, Kim SH, Tae G, Kim YH, Rhie JW, Kim SH, Kim SH (2009) In situ chondrogenic differentiation of human adipose tissue-derived stem cells in a TGF-beta1 loaded fibrin-poly(lactide-caprolactone) nanoparticulate complex. Biomaterials 30:4657–4664

    CAS  Google Scholar 

  214. Mehlhorn AT, Zwingmann J, Finkenzeller G, Niemeyer P, Dauner M, Stark B, Sudkamp NP, Schmal H (2009) Chondrogenesis of adipose-derived adult stem cells in a poly-lactide-co-glycolide scaffold. Tissue Eng Part A 15:1159–1167

    CAS  Google Scholar 

  215. Jin X, Sun Y, Zhang K, Wang J, Shi T, Ju X, Lou S (2007) Ectopic neocartilage formation from predifferentiated human adipose derived stem cells induced by adenoviral-mediated transfer of hTGF beta2. Biomaterials 28:2994–3003

    CAS  Google Scholar 

  216. Sittinger M, Bujia J, Rotter N, Reitzel D, Minuth WW, Burmester GR (1996) Tissue engineering and autologous transplant formation: practical approaches with resorbable biomaterials and new cell culture techniques. Biomaterials 17:237–242

    CAS  Google Scholar 

  217. Chang JC, Hsu SH, Chen DC (2009) The promotion of chondrogenesis in adipose-derived adult stem cells by an RGD-chimeric protein in 3D alginate culture. Biomaterials 30:6265–6275

    CAS  Google Scholar 

  218. Cheng NC, Estes BT, Awad HA, Guilak F (2009) Chondrogenic differentiation of adipose-derived adult stem cells by a porous scaffold derived from native articular cartilage extracellular matrix. Tissue Eng Part A 15:231–241

    CAS  Google Scholar 

  219. Hildner F, Concaro SE, Peterbauer A, Wolbank S, Danzer M, Lindahl A, Gatenholm P, Redl H, van GM (2009) Human adipose derived stem cells contribute to chondrogenesis in co-culture with human articular chondrocytes. Tissue Eng Part A 15(12):3961–3969

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plastic, Hand and Reconstructive Surgery, Podbielskistrasse 380, 30659, Hannover, Germany

    Jörn W. Kuhbier

  2. Department of Plastic, Hand and Reconstructive Surgery, Medical School Hannover, Podbielskistrasse 380, 30659, Hannover, Germany

    Birgit Weyand, Christine Radtke, Peter M. Vogt, Cornelia Kasper & Kerstin Reimers

Authors
  1. Jörn W. Kuhbier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Birgit Weyand
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christine Radtke
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peter M. Vogt
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cornelia Kasper
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kerstin Reimers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jörn W. Kuhbier .

Editor information

Editors and Affiliations

  1. Inst. Technische Chemie, Universität Hannover, Callinstr. 3, Hannover, 30167, Germany

    Cornelia Kasper

  2. Klinische und Experimentelle, Traumatologie, Ludwig Boltzmann Institut für, Donaueschingenstr. 13, Wien, 1200, Austria

    Martijn van Griensven

  3. Inst.Biotechnologie u. Verfahrenstechnik, TU Hamburg-Harburg, Denickestr. 15, Hamburg, 21073, Germany

    Ralf Pörtner

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Kuhbier, J.W., Weyand, B., Radtke, C., Vogt, P.M., Kasper, C., Reimers, K. (2010). Isolation, Characterization, Differentiation, and Application of Adipose-Derived Stem Cells. In: Kasper, C., van Griensven, M., Pörtner, R. (eds) Bioreactor Systems for Tissue Engineering II. Advances in Biochemical Engineering / Biotechnology, vol 123. Springer, Berlin, Heidelberg. https://doi.org/10.1007/10_2009_24

Download citation

Publish with us

Policies and ethics

Search

Navigation