Skip to main content

Human Adipose Tissue as a Source of Multipotent Stem Cells

  • Chapter
  • First Online:
  • 1844 Accesses

Abstract

To the reconstructive surgeon, the stem cell is a powerful tool that may be used to regenerate and maintain tissues while minimizing secondary morbidities and complications. With the description of human adipose-derived stem cells (ASCs) in 2001, the reconstructive surgeon has been given another stem cell source by which tissue regeneration can be accomplished. To the aesthetic surgeon, this is an exciting opportunity, as ASCs may be used in the regeneration of a wide variety of tissues such as skin, fat, bone, and cartilage. This chapter discusses the use of ASCs in the regeneration of such tissues and explores how these stem cells may participate in this process.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   299.99
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

Learn about institutional subscriptions

References

  1. Young HE, Mancini ML, Wright RP, Smith JC, Black Jr AC, Reagan CR, Lucas PA. Mesenchymal stem cells reside within the connective tissues of many organs. Dev Dyn. 1995;202(2):137–44.

    CAS  PubMed  Google Scholar 

  2. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143–7.

    CAS  PubMed  Google Scholar 

  3. Broxmeyer HE, Gluckman E, Auerbach A, Douglas GW, Friedman H, Cooper S, Hangoc G, Kurtzberg J, Bard J, Boyse EA. Human umbilical cord blood: a clinically useful source of transplantable hematopoietic stem/progenitor cells. Int J Cell Cloning. 1990;8 Suppl 1:76–89.

    PubMed  Google Scholar 

  4. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992;255(5052):1707–10.

    CAS  PubMed  Google Scholar 

  5. Ulmer FL, Winkel A, Kohorst P, Stiesch M. Stem cells–prospects in dentistry. Schweiz Monatsschr Zahnmed. 2010;120(10):860–83.

    PubMed  Google Scholar 

  6. Robey PG, Termine JD. Human bone cells in vitro. Calcif Tissue Int. 1985;37(5):453–60.

    CAS  PubMed  Google Scholar 

  7. Wergedal JE, Baylink DJ. Characterization of cells isolated and cultured from human bone. Proc Soc Exp Biol Med. 1984;176(1):60–9.

    CAS  PubMed  Google Scholar 

  8. Orbay H, Tobita M, Mizuno H. Mesenchymal stem cells isolated from adipose and other tissues: basic biological properties and clinical applications. Stem Cells Int. 2012;2012:461718.

    PubMed Central  PubMed  Google Scholar 

  9. De Bari C, Dell'Accio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 2001;44(8):1928–42.

    PubMed  Google Scholar 

  10. Zuk PA, Zhu M, Mizuno H, Huang JI, Futrell WJ, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multi-lineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7(2):211–26.

    CAS  PubMed  Google Scholar 

  11. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell. 2002;13(12):4279–95.

    CAS  PubMed Central  PubMed  Google Scholar 

  12. Rodbell M. Metabolism of isolated fat cells: I. Effects of hormones on glucose metabolism and lipolysis. J Biol Chem. 1964;239:375–80.

    CAS  PubMed  Google Scholar 

  13. Pozanski WJ, Waheed I, Van R. Human fat cell precursors: morphologic and metabolic differentiation in culture. Lab Invest. 1973;29(5):570–6.

    Google Scholar 

  14. Koenig WJ, Donovan JM, Pensler JM. Cranial bone grafting in children. Plast Reconstr Surg. 1995;95(1):1–4.

    CAS  PubMed  Google Scholar 

  15. Grant GA, Jolley M, Ellenbogen RG, Roberts TS, Gruss JR, Loeser JD. Failure of autologous bone-assisted cranioplasty following decompressive craniectomy in children and adolescents. J Neurosurg. 2004;100(2 Suppl Pediatrics):163–68.

    Google Scholar 

  16. Mulliken JB, Glowacki J. Induced osteogenesis for repair and construction in the craniofacial region. Plast Reconstr Surg. 1980;65(5):553–60.

    CAS  PubMed  Google Scholar 

  17. Friedenstein AJ, Petrakova KV, Kurolesova AI, Frolova GP. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation. 1968;6(2):230–47.

    CAS  PubMed  Google Scholar 

  18. Charbord P. Bone marrow mesenchymal stem cells: historical overview and concepts. Hum Gene Ther. 2010;21(9):1045–56.

    CAS  PubMed  Google Scholar 

  19. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature. 2002;418(6893):41–9.

    CAS  PubMed  Google Scholar 

  20. Woodbury D, Reynolds K, Black IB. Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal genes prior to neurogenesis. J Neurosci Res. 2002;69(6):908–17.

    CAS  PubMed  Google Scholar 

  21. Irving I, Cooper M, Durrant S. Sciatic nerve compression following bone marrow harvest. Bone Marrow Transplant. 2000;26(6):705–6.

    CAS  PubMed  Google Scholar 

  22. De Ugarte DA, Morizono K, Elbarbary A, Alfonso ZC, Zuk PA, Zhu M, Dragoo JL, Ashjian PH, Thomas B, Benhaim P, Chen I, Fraser JK, Hedrick MH. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs. 2003;174(3):101–9.

    PubMed  Google Scholar 

  23. Oedayrajsingh-Varma MJ, van Ham SM, Knippenberg M, Helder MN, Klein-Nulend J, Schouten TE, Ritt MJ, van Milligen FJ. Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy. 2006;8(2):166–77.

    CAS  PubMed  Google Scholar 

  24. Aust L, Devlin B, Foster SJ, Halvorsen YD, Hicok K, du Laney T, Sen A, Willingmyre GD, Gimble JM. Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy. 2004;6(1):7–14.

    CAS  PubMed  Google Scholar 

  25. Safwani WK, Makpol S, Sathapan S, Chua KH. Long-term in vitro expansion of human adipose-derived stem cells showed low risk of tumourigenicity. J Tissue Eng Regen Med. 2012;2:1–11.

    Google Scholar 

  26. Safwani WK, Makpol S, Sathapan S, Chua KH. The impact of long-term in vitro expansion on the senescence-associated markers of human adipose-derived stem cells. Appl Biochem Biotechnol. 2012;166(8):2101–13.

    CAS  PubMed  Google Scholar 

  27. Danoviz ME, Bassaneze V, Nakamuta JS, dos Santos-Junior GR, Saint-Clair D, Bajgelman MC, Fae KC, Kalil J, Miyakawa AA, Krieger JE. Adipose tissue-derived stem cells from humans and mice differ in proliferative capacity and genome stability in long-term cultures. Stem Cells Dev. 2011;20(4):661–70.

    CAS  PubMed  Google Scholar 

  28. Zaman WS, Makpol S, Santhapan S, Chua KH. Stemness gene expression profile of human adipose derived stem cells in long-term culture. Med J Malaysia. 2008;63(Suppl A):61–2.

    PubMed  Google Scholar 

  29. Zuk PA. Adipose-derived stem cells in tissue regeneration: a review. ISRN Stem Cells. 2013;2013:2013. Article ID 713959. http://dx.doi.org/10.1155/2013/713959. Accessed 5 Dec 2013.

  30. Mitchell JB, McIntosh K, Zvonic S, Garrett S, Floyd ZE, Kloster A, Di Halvorsen Y, Storms RW, Goh B, Kilroy G, Wu X, Gimble JM. Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells. 2006;24(2):376–85.

    PubMed  Google Scholar 

  31. 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. 2006;208(1):64–76.

    CAS  PubMed  Google Scholar 

  32. Oedayrajsingh-Varma MJ, Breuls RG, Schouten TE, Jurgens WJ, Bontkes HJ, Schuurhuis GJ, van Ham SM, van Milligen FJ. Phenotypical and functional characterization of freshly isolated adipose tissue-derived stem cells. Stem Cells Dev. 2007;16(1):91–104.

    CAS  Google Scholar 

  33. Zannettino AC, Paton S, Arthur A, Khor F, Itescu S, Gimble JM, Gronthos S. Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol. 2008;214(2):413–21.

    CAS  PubMed  Google Scholar 

  34. Katz AJ, Tholpady A, Tholpady SS, Shang H, Ogle RC. Cell surface and transcriptional characterization of human adipose-derived adherent stromal (hADAS) cells. Stem Cells. 2005;23(3):412–23.

    CAS  PubMed  Google Scholar 

  35. Amos PJ, Shang H, Bailey AM, Taylor A, Katz AJ, Peirce SM. IFATS collection: the role of human adipose-derived stromal cells in inflammatory microvascular remodeling and evidence of a perivascular phenotype. Stem Cells. 2008;26(10):2682–90.

    CAS  PubMed Central  PubMed  Google Scholar 

  36. Cai X, Lin Y, Hauschka PV, Grottkau BE. Adipose stem cells originate from perivascular cells. Biol Cell. 2011;103(9):435–47.

    PubMed  Google Scholar 

  37. Feng J, Mantesso A, Sharpe PT. Perivascular cells as mesenchymal stem cells. Expert Opin Biol Ther. 2010;10(10):1441–51.

    PubMed  Google Scholar 

  38. Levi B, James AW, Nelson ER, Hu S, Sun N, Peng M, Wu J, Longaker MT. Studies in adipose-derived stromal cells: migration and participation in repair of cranial injury after systemic injection. Plast Reconstr Surg. 2011;127(3):1130–40.

    CAS  PubMed Central  PubMed  Google Scholar 

  39. Rhee SC, Ji YH, Gharibjanian NA, Dhong ES, Park SH, Yoon ES. In vivo evaluation of mixtures of uncultured freshly isolated adipose-derived stem cells and demineralized bone matrix for bone regeneration in a rat critically sized calvarial defect model. Stem Cells Dev. 2010;20(2):233–42.

    PubMed  Google Scholar 

  40. Yoon E, Dhar S, Chun DE, Gharibjanian NA, Evans GR. In vivo osteogenic potential of human adipose-derived stem cells/poly lactide-co-glycolic acid constructs for bone regeneration in a rat critical-sized calvarial defect model. Tissue Eng. 2007;13(3):619–27.

    CAS  PubMed  Google Scholar 

  41. Kang H, Peng J, Lu S, Liu S, Zhang L, Huang J, Sui X, Zhao B, Wang A, Xu W, Luo Z, Guo Q. In vivo cartilage repair using adipose-derived stem cell-loaded decellularized cartilage ECM scaffolds. J Tissue Eng Regen Med. 2012. doi:10.1002/term.1538.

    Google Scholar 

  42. Dragoo JL, Carlson G, McCormick F, Khan-Farooqi H, Zhu M, Zuk PA, Benhaim P. Healing full-thickness cartilage defects using adipose-derived stem cells. Tissue Eng. 2007;13(7):1615–21.

    CAS  PubMed  Google Scholar 

  43. Ghoreishian M, Rezaei M, Beni BH, Javanmard SH, Attar BM, Zalzali H. Facial nerve repair with Gore-Tex tube and adipose-derived stem cells: an animal study in dogs. J Oral Maxillofac Surg. 2013;71(3):577–87.

    PubMed  Google Scholar 

  44. Shokrgozar MA, Fattahi M, Bonakdar S, Ragerdi Kashani I, Majidi M, Haghighipour N, Bayati V, Sanati H, Saeedi SN. Healing potential of mesenchymal stem cells cultured on a collagen-based scaffold for skin regeneration. Iran Biomed J. 2012;16(2):68–76.

    PubMed Central  PubMed  Google Scholar 

  45. Uysal CA, Tobita M, Hyakusoku H, Mizuno H. Adipose-derived stem cells enhance primary tendon repair: biomechanical and immunohistochemical evaluation. J Plast Reconstr Aesthet Surg. 2012;65(12):1712–9.

    PubMed  Google Scholar 

  46. Gray AW, Boothroyd LG. Female facial appearance and health. Evol Psychol. 2012;10(1):66–77.

    PubMed  Google Scholar 

  47. Elder Jr GH. Appearance and education in marriage mobility. Am Sociol Rev. 1969;34(4):519–33.

    PubMed  Google Scholar 

  48. Sigall H, Ostrove N. The aye of the beholder: susceptibility to sexism and beautyism in the evaluation of managerial applicants. J Appl Soc Pyschol. 1975;15:591–605.

    Google Scholar 

  49. Downs AC, Lyons PM. Natural observations of the links between attractiveness and initial legal judgements. Pers Soc Psychol. 1991;31:410–4.

    Google Scholar 

  50. Marlowe CM, Schneider SL, Nelson CE. Gender and attractiveness biases in hiring decisions: are more experienced managers liess biased? J Appl Pyschol. 1996;81:11–21.

    Google Scholar 

  51. Zouhary KJ. Bone graft harvesting from distant sites: concepts and techniques. Oral Maxillofac Surg Clin North Am. 2010;22(3):301–16.

    PubMed  Google Scholar 

  52. Dimitriou R, Mataliotakis GI, Angoules AG, Kanakaris NK, Giannoudis PV. Complications following autologous bone graft harvesting from the iliac crest and using the RIA: a systematic review. Injury. 2011;42 Suppl 2:S3–15.

    PubMed  Google Scholar 

  53. Lissenberg-Thunnissen SN, de Gorter DJ, Sier CF, Schipper IB. Use and efficacy of bone morphogenetic proteins in fracture healing. Int Orthop. 2011;35(9):1271–80.

    PubMed Central  PubMed  Google Scholar 

  54. Epstein NE. Pros, cons, and costs of INFUSE in spinal surgery. Surg Neurol Int. 2011;2:10.

    PubMed Central  PubMed  Google Scholar 

  55. Glassman SD, Carreon LY, Campbell MJ, Johnson JR, Puno RM, Djurasovic M, Dimar JR. The perioperative cost of Infuse bone graft in posterolateral lumbar spine fusion. Spine J. 2008;8(3):443–8.

    PubMed  Google Scholar 

  56. Buttermann GR. Prospective nonrandomized comparison of an allograft with bone morphogenic protein versus an iliac-crest autograft in anterior cervical discectomy and fusion. Spine J. 2008;8(3):426–35.

    PubMed  Google Scholar 

  57. Garrett MP, Kakarla UK, Porter RW, Sonntag VK. Formation of painful seroma and edema after the use of recombinant human bone morphogenetic protein-2 in posterolateral lumbar spine fusions. Neurosurgery. 2010;66(6):1044–9.

    PubMed  Google Scholar 

  58. Abe Y, Ohtsuji M, Ohtsuji N, Lin Q, Tsurui H, Nakae S, Shirai T, Sudo K, Hirose S. Ankylosing enthesitis associated with up-regulated IFN-gamma and IL-17 production in (BXSB x NZB) F(1) male mice: a new mouse model. Mod Rheumatol. 2009;19(3):316–22.

    CAS  PubMed  Google Scholar 

  59. Shah MM, Smyth MD, Woo AS. Adverse facial edema associated with off-label use of recombinant human bone morphogenetic protein-2 in cranial reconstruction for craniosynostosis. Case report. J Neurosurg Pediatr. 2008;1(3):255–7.

    PubMed  Google Scholar 

  60. Hicok KC, Du Laney TV, Zhou YS, Halvorsen YD, Hitt DC, Cooper LF, Gimble JM. Human adipose-derived adult stem cells produce osteoid in vivo. Tissue Eng. 2004;10(3–4):371–80.

    CAS  PubMed  Google Scholar 

  61. Jeon O, Rhie JW, Kwon IK, Kim JH, Kim BS, Lee SH. In vivo bone formation following transplantation of human adipose-derived stromal cells that are not differentiated osteogenically. Tissue Eng Part A. 2008;14(8):1285–94.

    CAS  PubMed  Google Scholar 

  62. Dragoo JL, Choi JY, Lieberman JR, Huang J, Zuk PA, Zhang J, Hedrick MH, Benhaim P. Bone induction by BMP-2 transduced stem cells derived from human fat. J Orthop Res. 2003;21(4):622–9.

    CAS  PubMed  Google Scholar 

  63. Dudas JR, Marra KG, Cooper GM, Penascino VM, Mooney MP, Jiang S, Rubin JP, Losee JE. The osteogenic potential of adipose-derived stem cells for the repair of rabbit calvarial defects. Ann Plast Surg. 2006;56(5):543–8.

    CAS  PubMed  Google Scholar 

  64. Peterson B, Zhang J, Iglesias R, Kabo M, Hedrick M, Benhaim P, Lieberman JR. Healing of critically sized femoral defects, using genetically modified mesenchymal stem cells from human adipose tissue. Tissue Eng. 2005;11(1–2):120–9.

    CAS  PubMed  Google Scholar 

  65. Sheyn D, Kallai I, Tawackoli W, Cohn Yakubovich D, Oh A, Su S, Da X, Lavi A, Kimelman-Bleich N, Zilberman Y, Li N, Bae H, Gazit Z, Pelled G, Gazit D. Gene-modified adult stem cells regenerate vertebral bone defect in a rat model. Mol Pharm. 2011;8(5):1592–601.

    CAS  PubMed Central  PubMed  Google Scholar 

  66. Yang M, Ma QJ, Dang GT, Ma K, Chen P, Zhou CY. 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. 2005;7(3):273–81.

    CAS  PubMed  Google Scholar 

  67. Smith DM, Cooper GM, Afifi AM, Mooney MP, Cray J, Rubin JP, Marra KG, Losee JE. Regenerative surgery in cranioplasty revisited: the role of adipose-derived stem cells and BMP-2. Plast Reconstr Surg. 2011;128(5):1053–60.

    CAS  PubMed  Google Scholar 

  68. Zuk P, Chou YF, Mussano F, Benhaim P, Wu BM. Adipose-derived stem cells and BMP2: part 2. BMP2 may not influence the osteogenic fate of human adipose-derived stem cells. Connect Tissue Res. 2011;52(2):119–32.

    CAS  PubMed  Google Scholar 

  69. Miyazono K, Kusanagi K, Inoue H. Divergence and convergence of TGF-beta/BMP signaling. J Cell Physiol. 2001;187(3):265–76.

    CAS  PubMed  Google Scholar 

  70. Gonzalez-Ulloa M, Castillo A, Stevens E, Alvarez Fuertes G, Leonelli F, Ubaldo F. Preliminary study of the total restoration of the facial skin. Plast Reconstr Surg (1946). 1954;13(3):151–61.

    CAS  Google Scholar 

  71. Constantian MB. Functional effects of alar cartilage malposition. Ann Plast Surg. 1993;30(6):487–99.

    CAS  PubMed  Google Scholar 

  72. Sajjadian A, Naghshineh N, Rubinstein R. Current status of grafts and implants in rhinoplasty: Part II. Homologous grafts and allogenic implants. Plast Reconstr Surg. 2010;125(3):99e–109.

    CAS  PubMed  Google Scholar 

  73. Sajjadian A, Rubinstein R, Naghshineh N. Current status of grafts and implants in rhinoplasty: part I. Autologous grafts. Plast Reconstr Surg. 2009;125(2):40e-–9.

    Google Scholar 

  74. Rohrich RJ, Liu JH. The dorsal columellar strut: innovative use of dorsal hump removal for a columellar strut. Aesthet Surg J. 2010;30(1):30–5.

    PubMed  Google Scholar 

  75. Bottini DJ, Gentile P, Donfrancesco A, Fiumara L, Cervelli V. Augmentation rhinoplasty with autologous grafts. Aesthetic Plast Surg. 2008;32(1):136–42.

    CAS  PubMed  Google Scholar 

  76. Gunter JP, Rohrich RJ. Augmentation rhinoplasty: dorsal onlay grafting using shaped autogenous septal cartilage. Plast Reconstr Surg. 1990;86(1):39–45.

    CAS  PubMed  Google Scholar 

  77. Juri J, Juri C, Elias JC. Ear cartilage grafts to the nose. Plast Reconstr Surg. 1979;63(3):377–82.

    CAS  PubMed  Google Scholar 

  78. Mischkowski RA, Domingos-Hadamitzky C, Siessegger M, Zinser MJ, Zoller JE. Donor-site morbidity of ear cartilage autografts. Plast Reconstr Surg. 2008;121(1):79–87.

    CAS  PubMed  Google Scholar 

  79. Cochran CS, DeFatta RJ. Tragal cartilage grafts in rhinoplasty: a viable alternative in the graft-depleted patient. Otolaryngol Head Neck Surg. 2008;138(2):166–9.

    PubMed  Google Scholar 

  80. Gunter JP, Clark CP, Friedman RM. Internal stabilization of autogenous rib cartilage grafts in rhinoplasty: a barrier to cartilage warping. Plast Reconstr Surg. 1997;100(1):161–9.

    CAS  PubMed  Google Scholar 

  81. Jung DH, Choi SH, Moon HJ, Chung IH, Im JH, Lam SM. A cadaveric analysis of the ideal costal cartilage graft for Asian rhinoplasty. Plast Reconstr Surg. 2004;114(2):545–50.

    PubMed  Google Scholar 

  82. Gunter JP, Cochran CS. Management of intraoperative fractures of the nasal septal “L-strut”: percutaneous Kirschner wire fixation. Plast Reconstr Surg. 2006;117(2):395–402.

    CAS  PubMed  Google Scholar 

  83. Janz BA, Cole P, Hollier Jr LH, Stal S. Treatment of prominent and constricted ear anomalies. Plast Reconstr Surg. 2009;124(1 Suppl):27e–37.

    CAS  PubMed  Google Scholar 

  84. Cronin TD, Ascough BM. Silastic ear construction. Clin Plast Surg. 1978;5(3):367–78.

    CAS  PubMed  Google Scholar 

  85. Romo 3rd T, Morris LG, Reitzen SD, Ghossaini SN, Wazen JJ, Kohan D. Reconstruction of congenital microtia-atresia: outcomes with the Medpor/bone-anchored hearing aid-approach. Ann Plast Surg. 2009;62(4):384–9.

    CAS  PubMed  Google Scholar 

  86. Sage A, Chang AA, Schumacher BL, Sah RL, Watson D. Cartilage outgrowth in fibrin scaffolds. Am J Rhinol Allergy. 2009;23(5):486–91.

    PubMed  Google Scholar 

  87. Naumann A. Cartilage grafts generated by tissue engineering. Histomorphological, immunochemical and biomechanical properties. HNO. 2008;56(2):109–21.

    CAS  PubMed  Google Scholar 

  88. Zhou G, Liu W, Cui L, Wang X, Liu T, Cao Y. Repair of porcine articular osteochondral defects in non-weightbearing areas with autologous bone marrow stromal cells. Tissue Eng. 2006;12(11):3209–21.

    CAS  PubMed  Google Scholar 

  89. Liu Y, Chen F, Liu W, Cui L, Shang Q, Xia W, Wang J, Cui Y, Yang G, Liu D, Wu J, Xu R, Buonocore SD, Cao Y. Repairing large porcine full-thickness defects of articular cartilage using autologous chondrocyte-engineered cartilage. Tissue Eng. 2002;8(4):709–21.

    CAS  PubMed  Google Scholar 

  90. Rubio D, Garcia-Castro J, Martin MC, de la Fuente R, Cigudosa JC, Lloyd AC, Bernad A. Spontaneous human adult stem cell transformation. Cancer Res. 2005;65(8):3035–9.

    CAS  PubMed  Google Scholar 

  91. Huang JI, Zuk PA, Jones NF, Zhu M, Lorenz HP, Hedrick MH, Benhaim P. Chondrogenic potential of multipotential cells from human adipose tissue. Plast Reconstr Surg. 2004;113(2):585–94.

    PubMed  Google Scholar 

  92. Awad HA, Halvorsen YD, Gimble JM, Guilak F. Effects of transforming growth factor beta1 and dexamethasone on the growth and chondrogenic differentiation of adipose-derived stromal cells. Tissue Eng. 2003;9(6):1301–12.

    CAS  PubMed  Google Scholar 

  93. Ogawa R, Mizuno H, Hyakusoku H, Watanabe A, Migita M, Shimada T. Chondrogenic and osteogenic differentiation of adipose-derived stem cells isolated from GFP transgenic mice. J Nippon Med Sch. 2004;71(4):240–1.

    PubMed  Google Scholar 

  94. Jin X, Sun Y, Zhang K, Wang J, Shi T, Ju X, Lou S. Ectopic neocartilage formation from predifferentiated human adipose derived stem cells induced by adenoviral-mediated transfer of hTGF beta2. Biomaterials. 2007;28(19):2994–3003.

    CAS  PubMed  Google Scholar 

  95. Lu CH, Lin KJ, Chiu HY, Chen CY, Yen TC, Hwang SM, Chang YH, Hu YC. Improved chondrogenesis and engineered cartilage formation from TGF-beta3-expressing adipose-derived stem cells cultured in the rotating-shaft bioreactor. Tissue Eng Part A. 2012;18(19–20):2114–24.

    CAS  PubMed  Google Scholar 

  96. Awad HA, Wickham MQ, Leddy HA, Gimble JM, Guilak F. Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials. 2004;25(16):3211–22.

    CAS  PubMed  Google Scholar 

  97. Betre H, Ong SR, Guilak F, Chilkoti A, Fermor B, Setton LA. Chondrocytic differentiation of human adipose-derived adult stem cells in elastin-like polypeptide. Biomaterials. 2006;27(1):91–9.

    CAS  PubMed  Google Scholar 

  98. 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. 2005;9(4):929–39.

    CAS  PubMed  Google Scholar 

  99. Yoon IS, Chung CW, Sung JH, Cho HJ, Kim JS, Shim WS, Shim CK, Chung SJ, Kim DD. Proliferation and chondrogenic differentiation of human adipose-derived mesenchymal stem cells in porous hyaluronic acid scaffold. J Biosci Bioeng. 2011;112(4):402–8.

    CAS  PubMed  Google Scholar 

  100. Dragoo JL, Samimi B, Zhu M, Hame SL, Thomas BJ, Lieberman JR, Hedrick MH, Benhaim P. Tissue-engineered cartilage and bone using stem cells from human infrapatellar fat pads. J Bone Joint Surg Br. 2003;85(5):740–7.

    CAS  PubMed  Google Scholar 

  101. Jin XB, Sun YS, Zhang K, Wang J, Ju XD, Lou SQ. Neocartilage formation from predifferentiated human adipose derived stem cells in vivo. Acta Pharmacol Sin. 2007;28(5):663–71.

    CAS  PubMed  Google Scholar 

  102. Mehlhorn AT, Zwingmann J, Finkenzeller G, Niemeyer P, Dauner M, Stark B, Sudkamp NP, Schmal H. Chondrogenesis of adipose-derived adult stem cells in a poly-lactide-co-glycolide scaffold. Tissue Eng Part A. 2009;15(5):1159–67.

    CAS  PubMed  Google Scholar 

  103. Orbay H, Tobita M, Hyakusoku H, Mizuno H. Effects of adipose-derived stem cells on improving the viability of diced cartilage grafts. Plast Reconstr Surg. 2012;129(2):369–77.

    CAS  PubMed  Google Scholar 

  104. Cui L, Wu Y, Cen L, Zhou H, Yin S, Liu G, Liu W, Cao Y. Repair of articular cartilage defect in non-weight bearing areas using adipose derived stem cells loaded polyglycolic acid mesh. Biomaterials. 2009;30(14):2683–93.

    CAS  PubMed  Google Scholar 

  105. Yoon HH, Bhang SH, Shin JY, Shin J, Kim BS. Enhanced cartilage formation via three-dimensional cell engineering of human adipose-derived stem cells. Tissue Eng Part A. 2012;18(19–20):1945–56.

    Google Scholar 

  106. Im GI, Kim HJ, Lee JH. Chondrogenesis of adipose stem cells in a porous PLGA scaffold impregnated with plasmid DNA containing SOX trio (SOX-5,-6 and -9) genes. Biomaterials. 2011;32(19):4385–92.

    CAS  PubMed  Google Scholar 

  107. Tabit CJ, Slack GC, Fan K, Wan DC, Bradley JP. Fat grafting versus adipose-derived stem cell therapy: distinguishing indications, techniques, and outcomes. Aesthetic Plast Surg. 2011;36(3):704–13.

    PubMed  Google Scholar 

  108. Mizuno H, Itoi Y, Kawahara S, Ogawa R, Akaishi S, Hyakusoku H. In vivo adipose tissue regeneration by adipose-derived stromal cells isolated from GFP transgenic mice. Cells Tissues Organs. 2008;187(3):177–85.

    PubMed  Google Scholar 

  109. Lu F, Gao JH, Ogawa R, Mizuro H, Hykusoku H. Adipose tissues differentiated by adipose-derived stem cells harvested from transgenic mice. Chin J Traumatol. 2006;9(6):359–64.

    PubMed  Google Scholar 

  110. Hong L, Peptan I, Clark P, Mao JJ. Ex vivo adipose tissue engineering by human marrow stromal cell seeded gelatin sponge. Ann Biomed Eng. 2005;33(4):511–7.

    PubMed  Google Scholar 

  111. Hong L, Peptan IA, Colpan A, Daw JL. Adipose tissue engineering by human adipose-derived stromal cells. Cells Tissues Organs. 2006;183(3):133–40.

    CAS  PubMed  Google Scholar 

  112. Mauney JR, Nguyen T, Gillen K, Kirker-Head C, Gimble JM, Kaplan DL. 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. 2007;28(35):5280–90.

    CAS  PubMed Central  PubMed  Google Scholar 

  113. Ito R, Morimoto N, Liem PH, Nakamura Y, Kawai K, Taira T, Tsuji W, Toi M, Suzuki S. Adipogenesis using human adipose tissue-derived stromal cells combined with a collagen/gelatin sponge sustaining release of basic fibroblast growth factor. J Tissue Eng Regen Med. 2012 (in publication).

    Google Scholar 

  114. Tsuji W, Inamoto T, Yamashiro H, Ueno T, Kato H, Kimura Y, Tabata Y, Toi M. Adipogenesis induced by human adipose tissue-derived stem cells. Tissue Eng Part A. 2009;15(1):83–93.

    CAS  PubMed  Google Scholar 

  115. Handel M, Hammer TR, Hoefer D. Adipogenic differentiation of scaffold-bound human adipose tissue-derived stem cells (hASC) for soft tissue engineering. Biomed Mater. 2012;7(5):054107.

    CAS  PubMed  Google Scholar 

  116. Vermette M, Trottier V, Menard V, Saint-Pierre L, Roy A, Fradette J. Production of a new tissue-engineered adipose substitute from human adipose-derived stromal cells. Biomaterials. 2007;28(18):2850–60.

    CAS  PubMed  Google Scholar 

  117. Zhu M, Zhou Z, Chen Y, Schreiber R, Ransom JT, Fraser JK, Hedrick MH, Pinkernell K, Kuo HC. Supplementation of fat grafts with adipose-derived regenerative cells improves long-term graft retention. Ann Plast Surg. 2010;64(2):222–8.

    CAS  PubMed  Google Scholar 

  118. Sterodimas A, de Faria J, Nicaretta B, Boriani F. Autologous fat transplantation versus adipose-derived stem cell-enriched lipografts: a study. Aesthet Surg J. 2011;31(6):682–93.

    PubMed  Google Scholar 

  119. Matsumoto D, Sato K, Gonda K, Takaki Y, Shigeura T, Sato T, Aiba-Kojima E, Iizuka F, Inoue K, Suga H, Yoshimura K. Cell-assisted lipotransfer: supportive use of human adipose-derived cells for soft tissue augmentation with lipoinjection. Tissue Eng. 2006;12(12):3375–82.

    CAS  PubMed  Google Scholar 

  120. Yoshimura K, Sato K, Aoi N, Kurita M, Hirohi T, Harii K. Cell-assisted lipotransfer for cosmetic breast augmentation: supportive use of adipose-derived stem/stromal cells. Aesthetic Plast Surg. 2008;32(1):48–55.

    PubMed Central  PubMed  Google Scholar 

  121. Ko SH, Nauta A, Wong V, Glotzbach J, Gurtner GC, Longaker MT. The role of stem cells in cutaneous wound healing: what do we really know? Plast Reconstr Surg. 2011;127 Suppl 1:10S–20.

    CAS  PubMed  Google Scholar 

  122. Orbay H, Takami Y, Hyakusoku H, Mizuno H. Acellular dermal matrix seeded with adipose-derived stem cells as a subcutaneous implant. Aesthetic Plast Surg. 2011;35(5):756–63.

    PubMed  Google Scholar 

  123. Trottier V, Marceau-Fortier G, Germain L, Vincent C, Fradette J. IFATS collection: using human adipose-derived stem/stromal cells for the production of new skin substitutes. Stem Cells. 2008;26(10):2713–23.

    PubMed  Google Scholar 

  124. Chan RK, Zamora DO, Wrice NL, Baer DG, Renz EM, Christy RJ, Natesan S. Development of a vascularized skin construct using adipose-derived stem cells from debrided burned skin. Stem Cells Int. 2012;2012:841203.

    PubMed Central  PubMed  Google Scholar 

  125. Sumi M, Sata M, Toya N, Yanaga K, Ohki T, Nagai R. Transplantation of adipose stromal cells, but not mature adipocytes, augments ischemia-induced angiogenesis. Life Sci. 2007;80(6):559–65.

    CAS  PubMed  Google Scholar 

  126. 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. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation. 2004;109(5):656–63.

    PubMed  Google Scholar 

  127. Kondo K, Shintani S, Shibata R, Murakami H, Murakami R, Imaizumi M, Kitagawa Y, Murohara T. Implantation of adipose-derived regenerative cells enhances ischemia-induced angiogenesis. Arterioscler Thromb Vasc Biol. 2009;29(1):61–6.

    CAS  PubMed  Google Scholar 

  128. Miranville A, Heeschen C, Sengenes C, Curat CA, Busse R, Bouloumie A. Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation. 2004;110(3):349–55.

    CAS  PubMed  Google Scholar 

  129. Koh YJ, Koh BI, Kim H, Joo HJ, Jin HK, Jeon J, Choi C, Lee DH, Chung JH, Cho CH, Park WS, Ryu JK, Suh JK, Koh GY. Stromal vascular fraction from adipose tissue forms profound vascular network through the dynamic reassembly of blood endothelial cells. Arterioscler Thromb Vasc Biol. 2011;31(5):1141–50.

    CAS  PubMed  Google Scholar 

  130. Moon MH, Kim SY, Kim YJ, Kim SJ, Lee JB, Bae YC, Sung SM, Jung JS. Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Cell Physiol Biochem. 2006;17(5–6):279–90.

    CAS  PubMed  Google Scholar 

  131. Cao Y, Sun Z, Liao L, Meng Y, Han Q, Zhao RC. Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochem Biophys Res Commun. 2005;332(2):370–9.

    CAS  PubMed  Google Scholar 

  132. Mazo M, Hernandez S, Gavira JJ, Abizanda G, Arana M, Lopez-Martinez T, Moreno C, Merino J, Martino-Rodriguez A, Uixeira A, de Jalon JA, Pastrana J, Martinez-Caro D, Prosper F. Treatment of reperfused ischemia with adipose-derived stem cells in a preclinical Swine model of myocardial infarction. Cell Transplant. 2012;21(12):2723–33.

    PubMed  Google Scholar 

  133. Sun CK, Yen CH, Lin YC, Tsai TH, Chang LT, Kao YH, Chua S, Fu M, Ko SF, Leu S, Yip HK. Autologous transplantation of adipose-derived mesenchymal stem cells markedly reduced acute ischemia-reperfusion lung injury in a rodent model. J Transl Med. 2011;9:118.

    PubMed Central  PubMed  Google Scholar 

  134. Furuichi K, Shintani H, Sakai Y, Ochiya T, Matsushima K, Kaneko S, Wada T. Effects of adipose-derived mesenchymal cells on ischemia-reperfusion injury in kidney. Clin Exp Nephrol. 2012;16(5):679–89.

    CAS  PubMed  Google Scholar 

  135. Liu K, Liu R, Cao G, Sun H, Wang X, Wu S. Adipose-derived stromal cell autologous transplantation ameliorates pulmonary arterial hypertension induced by shunt flow in rat models. Stem Cells Dev. 2011;20(6):1001–10.

    CAS  PubMed  Google Scholar 

  136. Otto Beitnes J, Oie E, Shahdadfar A, Karlsen T, Muller RM, Aakhus S, Reinholt FP, Brinchmann JE. Intramyocardial injections of human mesenchymal stem cells following acute myocardial infarction modulate scar formation and improve left ventricular function. Cell Transplant. 2012;21(8):1697–709.

    PubMed  Google Scholar 

  137. Leobon B, Roncalli J, Joffre C, Mazo M, Boisson M, Barreau C, Calise D, Arnaud E, Andre M, Puceat M, Penicaud L, Prosper F, Planat-Benard V, Casteilla L. Adipose-derived cardiomyogenic cells: in vitro expansion and functional improvement in a mouse model of myocardial infarction. Cardiovasc Res. 2009;83(4):757–67.

    CAS  PubMed  Google Scholar 

  138. Yang JJ, Liu ZQ, Zhang JM, Wang HB, Hu SY, Liu JF, Wang CY, Chen YD. Real-time tracking of adipose tissue-derived stem cells with injectable scaffolds in the infarcted heart. Heart Vessels. 2012;28(3):385–96.

    CAS  PubMed  Google Scholar 

  139. Zhang X, Wang H, Ma X, Adila A, Wang B, Liu F, Chen B, Wang C, Ma Y. Preservation of the cardiac function in infarcted rat hearts by the transplantation of adipose-derived stem cells with injectable fibrin scaffolds. Exp Biol Med (Maywood). 2010;235(12):1505–15.

    CAS  Google Scholar 

  140. Gao W, Qiao X, Ma S, Cui L. Adipose-derived stem cells accelerate neovascularization in ischaemic diabetic skin flap via expression of hypoxia-inducible factor-1alpha. J Cell Mol Med. 2010;15(12):2575–85.

    Google Scholar 

  141. Reichenberger MA, Mueller W, Schafer A, Heimer S, Leimer U, Lass U, Germann G, Kollensperger E. Fibrin-embedded adipose derived stem cells enhance skin flap survival. Stem Cell Rev. 2012;8(3):844–53.

    PubMed  Google Scholar 

  142. Dumont DJ, Fong GH, Puri MC, Gradwohl G, Alitalo K, Breitman ML. Vascularization of the mouse embryo: a study of flk-1, tek, tie, and vascular endothelial growth factor expression during development. Dev Dyn. 1995;203(1):80–92.

    CAS  PubMed  Google Scholar 

  143. Jakeman LB, Armanini M, Phillips HS, Ferrara N. Developmental expression of binding sites and messenger ribonucleic acid for vascular endothelial growth factor suggests a role for this protein in vasculogenesis and angiogenesis. Endocrinology. 1993;133(2):848–59.

    CAS  PubMed  Google Scholar 

  144. Rehman J, Traktuev D, Li J, Merfeld-Clauss S, Temm-Grove CJ, Bovenkerk JE, Pell CL, Johnstone BH, Considine RV, March KL. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation. 2004;109(10):1292–8.

    PubMed  Google Scholar 

  145. Grewal N, Yacomotti L, Melkonyan V, Massey M, Bradley JP, Zuk PA. Freezing adipose tissue grafts may damage their ability to integrate into the host. Connect Tissue Res. 2009;50(1):14–28.

    CAS  PubMed  Google Scholar 

  146. Salgado AJ, Reis RL, Sousa NJ, Gimble JM. Adipose tissue derived stem cells secretome: soluble factors and their roles in regenerative medicine. Curr Stem Cell Res Ther. 2010;5(2):103–10.

    CAS  PubMed  Google Scholar 

  147. Rubina K, Kalinina N, Efimenko A, Lopatina T, Melikhova V, Tsokolaeva Z, Sysoeva V, Tkachuk V, Parfyonova Y. Adipose stromal cells stimulate angiogenesis via promoting progenitor cell differentiation, secretion of angiogenic factors, and enhancing vessel maturation. Tissue Eng Part A. 2009;15(8):2039–50.

    CAS  PubMed  Google Scholar 

  148. Zografou A, Tsigris C, Papadopoulos O, Kavantzas N, Patsouris E, Donta I, Perrea D. Improvement of skin-graft survival after autologous transplantation of adipose-derived stem cells in rats. J Plast Reconstr Aesthet Surg. 2011;64(12):1647–56.

    CAS  PubMed  Google Scholar 

  149. Kim EK, Li G, Lee TJ, Hong JP. The effect of human adipose-derived stem cells on healing of ischemic wounds in a diabetic nude mouse model. Plast Reconstr Surg. 2011;128(2):387–94.

    CAS  PubMed  Google Scholar 

  150. Nie C, Yang D, Xu J, Si Z, Jin X, Zhang J. Locally administered adipose-derived stem cells accelerate wound healing through differentiation and vasculogenesis. Cell Transplant. 2011;20(2):205–16.

    PubMed  Google Scholar 

  151. Chen YT, Sun CK, Lin YC, Chang LT, Chen YL, Tsai TH, Chung SY, Chua S, Kao YH, Yen CH, Shao PL, Chang KC, Leu S, Yip HK. Adipose-derived mesenchymal stem cell protects kidneys against ischemia-reperfusion injury through suppressing oxidative stress and inflammatory reaction. J Transl Med. 2011;9:51.

    CAS  PubMed Central  PubMed  Google Scholar 

  152. Olutoye OO, Zhu X, Cass DL, Smith CW. Neutrophil recruitment by fetal porcine endothelial cells: implications in scarless fetal wound healing. Pediatr Res. 2005;58(6):1290–4.

    PubMed  Google Scholar 

  153. Shumakov VI, Onishchenko NA, Rasulov MF, Krasheninnikov ME, Zaidenov VA. Mesenchymal bone marrow stem cells more effectively stimulate regeneration of deep burn wounds than embryonic fibroblasts. Bull Exp Biol Med. 2003;136(2):192–5.

    CAS  PubMed  Google Scholar 

  154. Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002;99(10):3838–43.

    PubMed  Google Scholar 

  155. Djouad F, Plence P, Bony C, Tropel P, Apparailly F, Sany J, Noel D, Jorgensen C. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 2003;102(10):3837–44.

    CAS  PubMed  Google Scholar 

  156. Krampera M, Glennie S, Dyson J, Scott D, Laylor R, Simpson E, Dazzi F. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood. 2003;101(9):3722–9.

    CAS  PubMed  Google Scholar 

  157. Banas A, Teratani T, Yamamoto Y, Tokuhara M, Takeshita F, Osaki M, Kawamata M, Kato T, Okochi H, Ochiya T. IFATS collection: in vivo therapeutic potential of human adipose tissue mesenchymal stem cells after transplantation into mice with liver injury. Stem Cells. 2008;26(10):2705–12.

    CAS  PubMed  Google Scholar 

  158. Cui L, Yin S, Liu W, Li N, Zhang W, Cao Y. Expanded adipose-derived stem cells suppress mixed lymphocyte reaction by secretion of prostaglandin E2. Tissue Eng. 2007;13(6):1185–95.

    CAS  PubMed  Google Scholar 

  159. Wolbank S, Peterbauer A, Fahrner M, Hennerbichler S, van Griensven M, Stadler G, Redl H, Gabriel C. Dose-dependent immunomodulatory effect of human stem cells from amniotic membrane: a comparison with human mesenchymal stem cells from adipose tissue. Tissue Eng. 2007;13(6):1173–83.

    CAS  PubMed  Google Scholar 

  160. 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. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol. 2005;129(1):118–29.

    PubMed  Google Scholar 

  161. Peng W, Gao T, Yang ZL, Zhang SC, Ren ML, Wang ZG, Zhang B. Adipose-derived stem cells induced dendritic cells undergo tolerance and inhibit Th1 polarization. Cell Immunol. 2012;278(1–2):152–7.

    CAS  PubMed  Google Scholar 

  162. ter Huurne M, Schelbergen R, Blattes R, Blom A, de Munter W, Grevers L, Jeanson J, Noel D, Casteilla L, Jorgensen C, van den Berg W, van Lent P. Antiinflammatory and chondroprotective effects of intraarticular injection of adipose-derived stem cells in experimental osteoarthritis. Arthritis Rheum. 2012;64(11):3604–13.

    PubMed  Google Scholar 

  163. Cho KS, Roh HJ. Immunomodulatory effects of adipose-derived stem cells in airway allergic diseases. Curr Stem Cell Res Ther. 2010;5(2):111–5.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  165. Gonzalez-Rey E, Gonzalez MA, Varela N, O'Valle F, Hernandez-Cortes P, Rico L, Buscher D, Delgado M. 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. 2010;69(1):241–8.

    CAS  PubMed  Google Scholar 

  166. Gonzalez MA, Gonzalez-Rey E, Rico L, Buscher D, Delgado M. Adipose-derived mesenchymal stem cells alleviate experimental colitis by inhibiting inflammatory and autoimmune responses. Gastroenterology. 2009;136(3):978–89.

    PubMed  Google Scholar 

  167. Schweitzer KS, Johnstone BH, Garrison J, Rush NI, Cooper S, Traktuev DO, Feng D, Adamowicz JJ, Van Demark M, Fisher AJ, Kamocki K, Brown MB, Presson Jr RG, Broxmeyer HE, March KL, Petrache I. Adipose stem cell treatment in mice attenuates lung and systemic injury induced by cigarette smoking. Am J Respir Crit Care Med. 2011;183(2):215–25.

    PubMed Central  PubMed  Google Scholar 

  168. Yun IS, Jeon YR, Lee WJ, Lee JW, Rah DK, Tark KC, Lew DH. Effect of human adipose derived stem cells on scar formation and remodeling in a pig model: a pilot study. Dermatol Surg. 2012;38(10):1678–88.

    CAS  PubMed  Google Scholar 

  169. Kumai Y, Kobler JB, Herrera VL, Zeitels SM. Perspectives on adipose-derived stem/stromal cells as potential treatment for scarred vocal folds: opportunity and challenges. Curr Stem Cell Res Ther. 2010;5(2):175–81.

    CAS  PubMed  Google Scholar 

  170. Zhou Y, Yuan J, Zhou B, Lee AJ, Ghawji Jr M, Yoo TJ. The therapeutic efficacy of human adipose tissue-derived mesenchymal stem cells on experimental autoimmune hearing loss in mice. Immunology. 2011;133(1):133–40.

    CAS  PubMed Central  PubMed  Google Scholar 

  171. Donizetti-Oliveira C, Semedo P, Burgos-Silva M, Cenedeze MA, Malheiros DM, Reis MA, Pacheco-Silva A, Camara NO. Adipose tissue-derived stem cell treatment prevents renal disease progression. Cell Transplant. 2012;21(8):1727–41.

    PubMed  Google Scholar 

  172. Pinheiro CH, de Queiroz JC, Guimaraes-Ferreira L, Vitzel KF, Nachbar RT, de Sousa LG, de Souza-Jr AL, Nunes MT, Curi R. Local injections of adipose-derived mesenchymal stem cells modulate inflammation and increase angiogenesis ameliorating the dystrophic phenotype in dystrophin-deficient skeletal muscle. Stem Cell Rev. 2012;8(2):363–74.

    PubMed  Google Scholar 

  173. Lin CS, Lin G, Lue TF. Allogeneic and xenogeneic transplantation of adipose-derived stem cells in immunocompetent recipients without immunosuppressants. Stem Cells Dev. 2012;21(15):2770–8.

    PubMed Central  PubMed  Google Scholar 

  174. De Rosa A, De Francesco F, Tirino V, Ferraro GA, Desiderio V, Paino F, Pirozzi G, D'Andrea F, Papaccio G. A new method for cryopreserving adipose-derived stem cells: an attractive and suitable large-scale and long-term cell banking technology. Tissue Eng Part C Methods. 2009;15(4):659–67.

    PubMed  Google Scholar 

  175. Lendeckel S, Jodicke A, Christophis P, Heidinger K, Wolff J, Fraser JK, Hedrick MH, Berthold L, Howaldt HP. Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. J Craniomaxillofac Surg. 2004;32(6):370–3.

    PubMed  Google Scholar 

  176. Rigotti G, Marchi A, Galie M, Baroni G, Benati D, Krampera M, Pasini A, Sbarbati A. Clinical treatment of radiotherapy tissue damage by lipoaspirate transplant: a healing process mediated by adipose-derived adult stem cells. Plast Reconstr Surg. 2007;119(5):1409–22.

    CAS  PubMed  Google Scholar 

  177. Garcia-Olmo D, Garcia-Arranz M, Garcia LG, Cuellar ES, Blanco IF, Prianes LA, Montes JA, Pinto FL, Marcos DH, Garcia-Sancho L. Autologous stem cell transplantation for treatment of rectovaginal fistula in perianal Crohn's disease: a new cell-based therapy. Int J Colorectal Dis. 2003;18(5):451–4.

    PubMed  Google Scholar 

  178. Garcia-Olmo D, Garcia-Arranz M, Herreros D. Expanded adipose-derived stem cells for the treatment of complex perianal fistula including Crohn's disease. Expert Opin Biol Ther. 2008;8(9):1417–23.

    CAS  PubMed  Google Scholar 

  179. Garcia-Olmo D, Garcia-Arranz M, Herreros D, Pascual I, Peiro C, Rodriguez-Montes JA. A phase I clinical trial of the treatment of Crohn's fistula by adipose mesenchymal stem cell transplantation. Dis Colon Rectum. 2005;48(7):1416–23.

    PubMed  Google Scholar 

  180. Garcia-Olmo D, Herreros D, De-La-Quintana P, Guadalajara H, Trebol J, Georgiev-Hristov T, Garcia-Arranz M. Adipose-derived stem cells in Crohn's rectovaginal fistula. Case Report Med. 2010;2010:961758.

    CAS  Google Scholar 

  181. Garcia-Olmo D, Herreros D, Pascual I, Pascual JA, Del-Valle E, Zorrilla J, De-La-Quintana P, Garcia-Arranz M, Pascual M. Expanded adipose-derived stem cells for the treatment of complex perianal fistula: a phase II clinical trial. Dis Colon Rectum. 2009;52(1):79–86.

    PubMed  Google Scholar 

  182. Garcia-Olmo D, Herreros D, Pascual M, Pascual I, De-La-Quintana P, Trebol J, Garcia-Arranz M. 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(1):27–30.

    PubMed  Google Scholar 

  183. Guadalajara H, Herreros D, De-La-Quintana P, Trebol J, Garcia-Arranz M, Garcia-Olmo D. Long-term follow-up of patients undergoing adipose-derived adult stem cell administration to treat complex perianal fistulas. Int J Colorectal Dis. 2012;27(5):595–600.

    PubMed  Google Scholar 

  184. Herreros MD, Garcia-Arranz M, Guadalajara H, De-La-Quintana P, Garcia-Olmo D. Autologous expanded adipose-derived stem cells for the treatment of complex cryptoglandular perianal fistulas: a phase III randomized clinical trial (FATT 1: fistula Advanced Therapy Trial 1) and long-term evaluation. Dis Colon Rectum. 2012;55(7):762–72.

    CAS  PubMed  Google Scholar 

  185. 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. Non-expanded adipose stromal vascular fraction cell therapy for multiple sclerosis. J Transl Med. 2009;7:29.

    PubMed Central  PubMed  Google Scholar 

  186. Ra JC, Kang SK, Shin IS, Park HG, Joo SA, Kim JG, Kang BC, Lee YS, Nakama K, Piao M, Sohl B, Kurtz A. Stem cell treatment for patients with autoimmune disease by systemic infusion of culture-expanded autologous adipose tissue derived mesenchymal stem cells. J Transl Med. 2011;9:181.

    PubMed Central  PubMed  Google Scholar 

  187. Fang B, Song Y, Liao L, Zhang Y, Zhao RC. Favorable response to human adipose tissue-derived mesenchymal stem cells in steroid-refractory acute graft-versus-host disease. Transplant Proc. 2007;39(10):3358–62.

    CAS  PubMed  Google Scholar 

  188. Fang B, Song Y, Lin Q, Zhang Y, Cao Y, Zhao RC, Ma Y. 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. 2007;11(7):814–7.

    CAS  PubMed  Google Scholar 

  189. Fang B, Song YP, Liao LM, Han Q, Zhao RC. Treatment of severe therapy-resistant acute graft-versus-host disease with human adipose tissue-derived mesenchymal stem cells. Bone Marrow Transplant. 2006;38(5):389–90.

    CAS  PubMed  Google Scholar 

  190. Yanez R, Lamana ML, Garcia-Castro J, Colmenero I, Ramirez M, Bueren JA. Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells. 2006;24(11):2582–91.

    CAS  PubMed  Google Scholar 

  191. Karaaltin MV, Akpinar AC, Baghaki S, Akpinar F. Treatment of “en coup de sabre” deformity with adipose-derived regenerative cell-enriched fat graft. J Craniofac Surg. 2012;23(2):e103–5.

    PubMed  Google Scholar 

  192. Koh KS, Oh TS, Kim H, Chung IW, Lee KW, Lee HB, Park EJ, Chung JS, Shin IS, Ra JC, Choi JW. Clinical application of human adipose tissue-derived mesenchymal stem cells in progressive hemifacial atrophy (Parry-Romberg Disease) with microfat grafting techniques using three-dimensional computed tomography and three-dimensional camera. Ann Plast Surg. 2012;69(3):331–7.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patricia A. Zuk Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Li, A.I., Hokugo, A., Jarrahy, R., Zuk, P.A. (2014). Human Adipose Tissue as a Source of Multipotent Stem Cells. In: Shiffman, M., Di Giuseppe, A., Bassetto, F. (eds) Stem Cells in Aesthetic Procedures. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-45207-9_5

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-45207-9_5

  • Published:

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-45206-2

  • Online ISBN: 978-3-642-45207-9

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics