Expanded Adipose Tissue-Derived Stem Cells for Articular Cartilage Injury Treatment: A Safety and Efficacy Evaluation

  • Phuc Van Pham
  • Khanh Hong Thien Bui
  • Dat Quoc Ngo
  • Thao Thi-Phuong Doan
  • Ngoc Bich Vu
  • Nhung Hai Truong
  • Dung Minh Le
  • Ngoc Kim Phan


Non-expanded adipose tissue-derived stem cells (ADSCs) are commonly used in preclinical and clinical articular cartilage injury treatment; however, there are usually insufficient non-expanded ADSCs for transplantation. This research aims to evaluate the safety and efficacy of expanded ADSC transplantation in a mouse model. The stromal vascular fraction from abdominal adipose tissue was subcultured for ten passages to enrich for and expand the number of ADSCs. The safety of expanded ADSCs was assessed by evaluating their “stemness” via ADSC-specific marker expression, the expression of two tumorigenesis-related genes (Oct-3/4 and Nanog) using real-time RT-PCR, and in vivo tumor formation in NOD/SCID mice. ADSC efficacy was determined by assessing their chondrocytic differentiative potential in vitro in cartilage-inducing medium as well as in vivo via injection into a NOD/SCID mice joint failure model. The results showed that expanded ADSCs were negative for Oct-3/4 and Nanog and did not induce tumor formation in mice. Furthermore, ADSCs differentiated into chondrocytes, both in vitro and in vivo, and enhanced the regeneration of articular cartilage in NOD/SCID mice as compared with the control. These results confirm that expanded ADSCs are safe and effective for the treatment of injured articular cartilage and offer a promising therapy for degenerative cartilaginous diseases.


Articular Cartilage Graft Versus Host Disease Stromal Vascular Fraction Fetal Bovine Serum Medium Stromal Vascular Fraction Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Conflicts of Interest

The authors have no conflicts of interest.


  1. 1.
    Black LL, Gaynor J, Adams C, Dhupa S, Sams AE, Taylor R, Harman S, Gingerich DA, Harman R. Effect of intraarticular injection of autologous adipose-derived mesenchymal stem and regenerative cells on clinical signs of chronic osteoarthritis of the elbow joint in dogs. Vet Ther. 2008;9:192–200.PubMedGoogle Scholar
  2. 2.
    Black LL, Gaynor J, Gahring D, Adams C, Aron D, Harman S, Gingerich DA, Harman R. Effect of adipose-derived mesenchymal stem and regenerative cells on lameness in dogs with chronic osteoarthritis of the coxofemoral joints: a randomized, double-blinded, multicenter, controlled trial. Vet Ther. 2007;8:272–84.PubMedGoogle Scholar
  3. 3.
    Blande IS, Bassaneze V, Lavini-Ramos C, Fae KC, Kalil J, Miyakawa AA, Schettert IT, Krieger JE. Adipose tissue mesenchymal stem cell expansion in animal serum-free medium supplemented with autologous human platelet lysate. Transfusion. 2009;49(12):2680–5.PubMedCrossRefGoogle Scholar
  4. 4.
    Borrione P, Gianfrancesco AD, Pereira MT, Pigozzi F. Platelet-rich plasma in muscle healing. Am J Phys Med Rehabil. 2010;89(10):854–61.PubMedCrossRefGoogle Scholar
  5. 5.
    Buckwalter JA, Saltzman C, Brown T. The impact of osteoarthritis: implications for research. Clin Orthop Relat Res. 2004;427:S6–15.PubMedCrossRefGoogle Scholar
  6. 6.
    Caimi PF, Reese J, Lee Z, Lazarus HM. Emerging therapeutic approaches for multipotent mesenchymal stromal cells. Curr Opin Hematol. 2010;17(6):505–13.PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Centeno CJ, Busse D, Kisiday J, Keohan C, Freeman M, Karli D. Regeneration of meniscus cartilage in a knee treated with percutaneously implanted autologous mesenchymal stem cells. Med Hypotheses. 2008;71(6):900–8.PubMedCrossRefGoogle Scholar
  8. 8.
    Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell. 2003;113(5):643–55.PubMedCrossRefGoogle Scholar
  9. 9.
    Chen HT, Lee MJ, Chen CH, Chuang SC, Chang LF, Ho ML, Hung SH, Fu YC, Wang YH, Wang HI, Wang GJ, Kang L, Chang JK. Proliferation and differentiation potential of human adipose-derived mesenchymal stem cells isolated from elderly patients with osteoporotic fractures. J Cell Mol Med. 2012;16(3):582–93.PubMedCrossRefGoogle Scholar
  10. 10.
    Chen L, Ling PX, Jin Y, Zhang TM. Hyaluronic acid in combination with chondroitin sulfate and hyaluronic acid improved the degeneration of synovium and cartilage equally in rabbits with osteoarthritis. Drug Discov Ther. 2011;5(4):190–4.PubMedCrossRefGoogle Scholar
  11. 11.
    Chen YC, Hsu HS, Chen YW, Tsai TH, How CK, Wang CY, Hung SC, Chang YL, Tsai ML, Lee YY, Ku HH, Chiou SH. Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS One. 2008;3(7):e2637.PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Chiou SH, Yu CC, Huang CY, Lin SC, Liu CJ, Tsai TH, Chou SH, Chien CS, Ku HH, Lo JF. Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clin Cancer Res. 2008;14(13):4085–95.PubMedCrossRefGoogle Scholar
  13. 13.
    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.PubMedCrossRefGoogle Scholar
  14. 14.
    Davatchi F, Abdollahi BS, Mohyeddin M, Shahram F, Nikbin B. Mesenchymal stem cell therapy for knee osteoarthritis. Preliminary report of four patients. Int J Rheum Dis. 2011;14(2):211–5.PubMedCrossRefGoogle Scholar
  15. 15.
    Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315–7.PubMedCrossRefGoogle Scholar
  16. 16.
    Dougados M. The role of anti-inflammatory drugs in the treatment of osteoarthritis: a European viewpoint. Clin Exp Rheumatol. 2001;19:S9–14.PubMedGoogle Scholar
  17. 17.
    Dromard C, Bourin P, André M, De Barros S, Casteilla L, Planat-Benard V. Human adipose derived stroma/stem cells grow in serum-free medium as floating spheres. Exp Cell Res. 2011;317(6):770–80.PubMedCrossRefGoogle Scholar
  18. 18.
    Erickson GR, Gimble JM, Franklin DM, Rice HE, Awad H, Guilak F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun. 2002;290:763–9.PubMedCrossRefGoogle Scholar
  19. 19.
    Estes BT, Diekman BO, Gimble JM, Guilak F. Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype. Nat Protoc. 2010;5(7):1294–311.PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Eyigor S, Hepguler S, Sezak M, Oztop F, Capaci K. Effects of intra-articular hyaluronic acid and corticosteroid therapies on articular cartilage in experimental severe osteoarthritis. Clin Exp Rheumatol. 2006;24:724.PubMedGoogle Scholar
  21. 21.
    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.PubMedCrossRefGoogle Scholar
  22. 22.
    Fang B, Song Y, Zhao RC, Han Q, Lin Q. Using human adipose tissue-derived mesenchymal stem cells as salvage therapy for hepatic graft-versus-host disease resembling acute hepatitis. Transplant Proc. 2007;39(5):1710–3.PubMedCrossRefGoogle Scholar
  23. 23.
    Farias VA, Linares-Fernández JL, Peñalver JL, Payá Colmenero JA, Ferrón GO, Duran EL, Fernández RM, Olivares EG, O’Valle F, Puertas A, Oliver FJ, Ruiz de Almodóvar JM. Human umbilical cord stromal stem cell express CD10 and exert contractile properties. Placenta. 2011;32(1):86–95.PubMedCrossRefGoogle Scholar
  24. 24.
    Fraser JK, Wulur I, Alfonso Z, Hedrick MH. Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol. 2006;24:150–4.PubMedCrossRefGoogle Scholar
  25. 25.
    Friedenstein AJ, Petrakova KV, Kurolesova AI, Frolova GP. Heterotopic transplants of bone marrow: analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation. 1968;6:230–47.PubMedCrossRefGoogle Scholar
  26. 26.
    Frisbie DD, Kisiday JD, Kawcak CE, Werpy NM, McIlwraith CW. Evaluation of adipose-derived stromal vascular fraction or bone marrow-derived mesenchymal stem cells for treatment of osteoarthritis. J Orthop Res. 2009;27(12):1675–80.PubMedCrossRefGoogle Scholar
  27. 27.
    Gimble JM, Guilak F. Differentiation potential of adipose derived adult stem cell (ADAS) cells. Curr Top Dev Biol. 2003;58:137–60.PubMedCrossRefGoogle Scholar
  28. 28.
    Goedecke A, Wobus M, Krech M, Münch N, Richter K, Hölig K, Bornhauser M. Differential effect of platelet-rich plasma and fetal calf serum on bone marrow-derived human mesenchymal stromal cells expanded in vitro. J Tissue Eng Regen Med. 2011;5(8):648–54.PubMedCrossRefGoogle Scholar
  29. 29.
    Gosset M, Berenbaum F, Thirion S, Jacques C. Primary culture and phenotyping of murine chondrocytes. Nat Protoc. 2008;3(8):1253–60.PubMedCrossRefGoogle Scholar
  30. 30.
    Guercio A, Di Marco P, Casella S, Cannella V, Russotto L, Purpari G, Di Bella S, Piccione G. Production of canine mesenchymal stem cells from adipose tissue and their application in dogs with chronic osteoarthritis of the humeroradial joints. Cell Biol Int. 2012;36(2):189–94.PubMedCrossRefGoogle Scholar
  31. 31.
    Guo Y, Liu S, Wang P, Zhao S, Wang F, Bing L, Zhang Y, Ling EA, Gao J, Hao A. Expression profile of embryonic stem cell-associated genes Oct4, Sox2 and Nanog in human gliomas. Histopathology. 2011;59(4):763–75.PubMedCrossRefGoogle Scholar
  32. 32.
    Halvorsen YD, Franklin D, Bond AL, Hitt DC, Auchter C, Boskey AL, Paschalis EP, Wilkison WO, Gimble JM. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng. 2001;7:729–41.PubMedCrossRefGoogle Scholar
  33. 33.
    Hochedlinger K, Yamada Y, Beard C, Jaenisch R. Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell. 2005;121(3):465–77.PubMedCrossRefGoogle Scholar
  34. 34.
    Izadpanah R, Trygg C, Patel B, Kriedt C, Dufour J, Gimble JM, Bunnel BA. Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem. 2006;99:1285–97.PubMedCentralPubMedCrossRefGoogle Scholar
  35. 35.
    Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res. 1998;238:265–72.PubMedCrossRefGoogle Scholar
  36. 36.
    Kakudo N, Minakata T, Mitsui T, Kushida S, Notodihardjo FZ, Kusumoto K. Proliferation-promoting effect of platelet-rich plasma on human adipose-derived stem cells and human dermal fibroblasts. Plast Reconstr Surg. 2008;122(5):1352–60.PubMedCrossRefGoogle Scholar
  37. 37.
    Karatosun V, Unver B, Ozden A, Ozay Z, Gunal I. Intra-articular hyaluronic acid compared to exercise therapy in osteoarthritis of the ankle. A prospective randomized trial with long-term follow-up. Clin Exp Rheumatol. 2008;26:288–94.PubMedGoogle Scholar
  38. 38.
    Kasemkijwattana C, Hongeng S, Kesprayura S, Rungsinaporn V, Chaipinyo K, Chansiri K. Autologous bone marrow mesenchymal stem cells implantation for cartilage defects: two cases report. J Med Assoc Thai. 2011;94(3):395–400.PubMedGoogle Scholar
  39. 39.
    Kern S, Eichler H, Stoeve J, Klüter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells. 2006;24:1294–301.PubMedCrossRefGoogle Scholar
  40. 40.
    Kitagawa YKM, Toriyama K, Kamei Y, Torii S. History of discovery of human adipose-derived stem cells and their clinical applications. Jpn J Plast Reconstr Surg. 2006;49:1097–104.Google Scholar
  41. 41.
    Kocaoemer A, Kern S, Klüter H, Bieback K. Human AB serum and thrombin-activated platelet-rich plasma are suitable alternatives to fetal calf serum for the expansion of mesenchymal stem cells from adipose tissue. Stem Cells. 2007;25(5):1270–8.PubMedCrossRefGoogle Scholar
  42. 42.
    Kon E, Mandelbaum B, Buda R, Filardo G, Delcogliano M, Timoncini A, Fornasari PM, Giannini S, Marcacci M. Platelet-rich plasma intra-articular injection versus hyaluronic acid viscosupplementation as treatments for cartilage pathology: from early degeneration to osteoarthritis. Arthroscopy. 2011;27(11):1490–501.PubMedCrossRefGoogle Scholar
  43. 43.
    Laharrague P, Larrouy D, Fontanilles AM, Truel N, Campfield A, Tenenbaum R, Galitzky J, Corberand JX, Pénicaud L, Casteilla L. High expression of leptin by human bone marrow adipocytes in primary culture. FASEB J. 1998;12(9):747–52.PubMedGoogle Scholar
  44. 44.
    Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I, Lanino E, Sundberg B, Bernardo ME, Remberger M, Dini G, Egeler RM, Bacigalupo A, Fibbe W, Ringdén O. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet. 2008;371(9624):1579–86.PubMedCrossRefGoogle Scholar
  45. 45.
    Lee JM, Im GI. SOX trio-co-transduced adipose stem cells in fibrin gel to enhance cartilage repair and delay the progression of osteoarthritis in the rat. Biomaterials. 2012;33(7):2016–24.PubMedCrossRefGoogle Scholar
  46. 46.
    Lindroos B, Suuronen R, Miettinen S. The potential of adipose stem cells in regenerative medicine. Stem Cell Rev. 2011;7(2):269–91.PubMedCrossRefGoogle Scholar
  47. 47.
    Liu C, Cao X, Zhang Y, Xu H, Zhang R, Wu Y, Lu P, Jin F. Co-expression of Oct-4 and Nestin in human breast cancers. Mol Biol Rep. 2012;39(5):5875–81.PubMedCrossRefGoogle Scholar
  48. 48.
    Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–8.PubMedCrossRefGoogle Scholar
  49. 49.
    Lubis AM, Lubis VK. Adult bone marrow stem cells in cartilage therapy. Acta Med Indones. 2012;44(1):62–8.PubMedGoogle Scholar
  50. 50.
    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. The immunophenotype of human adipose derived cells: temporal changes in stromal- and stem cell-associated markers. Stem Cells. 2006;24:376–85.PubMedCrossRefGoogle Scholar
  51. 51.
    Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell. 2003;113(5):631–42.PubMedCrossRefGoogle Scholar
  52. 52.
    Mizuno H, Zuk PA, Zhu M, Lorenz HP, Benhaim P, Hedrick MH. Myogenic differentiation by human processed lipoaspirate cells. Plast Reconstr Surg. 2002;109:199–209.PubMedCrossRefGoogle Scholar
  53. 53.
    Murphy JM, Fink DJ, Hunziker EB, Barry FP. Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum. 2003;48(12):3464–74.PubMedCrossRefGoogle Scholar
  54. 54.
    Musumeci G, Lo Furno D, Loreto C, Giuffrida R, Caggia S, Leonardi R, Cardile V. Mesenchymal stem cells from adipose tissue which have been differentiated into chondrocytes in three-dimensional culture express lubricin. Exp Biol Med (Maywood). 2011;236(11):1333–41.CrossRefGoogle Scholar
  55. 55.
    Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet. 2000;24(4):372–6.PubMedCrossRefGoogle Scholar
  56. 56.
    Pak J. Regeneration of human bones in hip osteonecrosis and human cartilage in knee osteoarthritis with autologous adipose-tissue-derived stem cells: a case series. J Med Case Reports. 2011;5:296.PubMedCentralCrossRefGoogle Scholar
  57. 57.
    Patel AN, Yochman J, Vargas V, Bull DA. Putative population of adipose derived stem cells isolated from mediastinal tissue during cardiac surgery. Cell Transplant. 2012. doi: 10.3727/096368912X636849.PubMedCentralGoogle Scholar
  58. 58.
    Peng J, Wang Y, Zhang L, Zhao B, Zhao Z, Chen J, Guo Q, Liu S, Sui X, Xu W, Lu S. Human umbilical cord Wharton’s jelly-derived mesenchymal stem cells differentiate into a Schwann-cell phenotype and promote neurite outgrowth in vitro. Brain Res Bull. 2011;84(3):235–43.PubMedCrossRefGoogle Scholar
  59. 59.
    Phadnis SM, Joglekar MV, Dalvi MP, Muthyala S, Nair PD, Ghaskadbi SM, Bhonde RR, Hardikar AA. Human bone marrow-derived mesenchymal cells differentiate and mature into endocrine pancreatic lineage in vivo. Cytotherapy. 2011;13(3):279–93.PubMedCrossRefGoogle Scholar
  60. 60.
    Phuc PV, Nhung TH, Loan DT, Chung DC, Ngoc PK. Differentiating of banked human umbilical cord blood-derived mesenchymal stem cells into insulin-secreting cells. In Vitro Cell Dev Biol Anim. 2011;47:54–63.PubMedCrossRefGoogle Scholar
  61. 61.
    Pilz GA, Ulrich C, Ruh M, Abele H, Schäfer R, Kluba T, Bühring HJ, Rolauffs B, Aicher WK. Human term placenta-derived mesenchymal stromal cells are less prone to osteogenic differentiation than bone marrow-derived mesenchymal stromal cells. Stem Cells Dev. 2011;20:635–46.PubMedCrossRefGoogle Scholar
  62. 62.
    Pincus T, Koch GG, Sokka T, Lefkowith J, Wolfe F, Jordan JM, Luta G, Callahan LF, Wang X, Schwartz T, Abramson SB, Caldwell JR, Harrell RA, Kremer JM, Lautzenheiser RL, Markenson JA, Schnitzer TJ, Weaver A, Cummins P, Wilson A, Morant S, Fort J. A randomized, double-blind, crossover clinical trial of diclofenac plus misoprostol versus acetaminophen in patients with osteoarthritis of the hip or knee. Arthritis Rheum. 2001;44:1587–98.PubMedCrossRefGoogle Scholar
  63. 63.
    Prockop DJ. Marrow stromal cells as stem cells for non-hematopoietic tissues. Science. 1997;276:71–4.PubMedCrossRefGoogle Scholar
  64. 64.
    Rebelatto CK, Aguiar AM, Moretão MP, Senegaglia AC, Hansen P, Barchiki F, Oliveira J, Martins J, Kuligovski C, Mansur F, Christofis A, Amaral VF, Brofman PS, Goldenberg S, Nakao LS, Correa A. Dissimilar differentiation of mesenchymal stem cells from bone marrow, umbilical cord blood, and adipose tissue. Exp Biol Med (Maywood). 2008;233(7):901–13.CrossRefGoogle Scholar
  65. 65.
    Reinisch A, Bartmann C, Rohde E, Schallmoser K, Bjelic-Radisic V, Lanzer G, Linkesch W, Strunk D. Humanized system to propagate cord blood-derived multipotent mesenchymal stromal cells for clinical application. Regen Med. 2007;2(4):371–82.PubMedCrossRefGoogle Scholar
  66. 66.
    Ringdén O, Uzunel M, Rasmusson I, Remberger M, Sundberg B, Lönnies H, Marschall HU, Dlugosz A, Szakos A, Hassan Z, Omazic B, Aschan J, Barkholt L, Le Blanc K. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation. 2006;81(10):1390–7.PubMedCrossRefGoogle Scholar
  67. 67.
  68. 68.
    Safford KM, Hicok KC, Safford SD, Halvorsen Y-DC, Wilkinson WO, Gimble JM, Rice HE. Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem Biophys Res Commun. 2002;294:371–9.PubMedCrossRefGoogle Scholar
  69. 69.
    Schroeppel JP, Crist JD, Anderson HC, Wang J. Molecular regulation of articular chondrocyte function and its significance in osteoarthritis. Histol Histopathol. 2011;26:377–94.PubMedGoogle Scholar
  70. 70.
    Shih DT, Chen JC, Chen WY, Kuo YP, Su CY, Burnouf T. Expansion of adipose tissue mesenchymal stromal progenitors in serum-free medium supplemented with virally inactivated allogeneic human platelet lysate. Transfusion. 2011;51(4):770–8.PubMedCrossRefGoogle Scholar
  71. 71.
    Singer NG, Caplan AI. Mesenchymal stem cells: mechanisms of inflammation. Annu Rev Pathol. 2011;6:457–78.PubMedCrossRefGoogle Scholar
  72. 72.
    Spaková T, Rosocha J, Lacko M, Harvanová D, Gharaibeh A. Treatment of Knee Joint Osteoarthritis with Autologous Platelet-Rich Plasma in Comparison with Hyaluronic Acid. Am J Phys Med Rehabil. 2012;91(5):411–7.Google Scholar
  73. 73.
    Spath L, Rotilio V, Alessandrini M, Gambara G, De Angelis L, Mancini M, Mitsiadis TA, Vivarelli E, Naro F, Filippini A, Papaccio G. Explant-derived human dental pulp stem cells enhance differentiation and proliferation potentials. J Cell Mol Med. 2010;14(6B):1635–44.PubMedCrossRefGoogle Scholar
  74. 74.
    Ter Huurne MC, van Lent PLEM, Blom AB, Blattes R, Jeanson Y, Casteilla L. A single injection of adipose-derived stem cells protects against cartilage damage and lowers synovial activation in experimental osteoarthritis. Arthritis Rheum. 2011;63(S10):1784 [abstract].Google Scholar
  75. 75.
    Toghraie FS, Chenari N, Gholipour MA, Faghih Z, Torabinejad S, Dehghani S, Ghaderi A. Treatment of osteoarthritis with infrapatellar fat pad derived mesenchymal stem cells in Rabbit. Knee. 2011;18:71–5.PubMedCrossRefGoogle Scholar
  76. 76.
    Tsai LL, Yu CC, Chang YC, Yu CH, Chou MY. Markedly increased Oct4 and Nanog expression correlates with cisplatin resistance in oral squamous cell carcinoma. J Oral Pathol Med. 2011;40(8):621–8.PubMedCrossRefGoogle Scholar
  77. 77.
    Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W, Ho AD. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol. 2005;33:1402–16.PubMedCrossRefGoogle Scholar
  78. 78.
    Wieland HA, Michaelis M, Kirschbaum BJ, Rudolphi KA. Osteoarthritis—an untreatable disease? Nat Rev Drug Discov. 2005;4:331–44.PubMedCrossRefGoogle Scholar
  79. 79.
    Yang S, Pilgaard L, Chase LG, Boucher S, Vemuri MC, Fink T, Zachar V. Defined xenogeneic-free and hypoxic environment provides superior conditions for long-term expansion of human adipose-derived stem cells. Tissue Eng Part C Methods. 2012;18:593–602.PubMedCrossRefGoogle Scholar
  80. 80.
    Yoo JU, Barthel TS, Nishimura K, Solchaga L, Caplan AI, Goldberg VM, Johnstone B. The chondrogenic potential of human bone-marrow-derived mesenchymal progenitor cells. J Bone Joint Surg Am. 1998;80:1745–57.PubMedGoogle Scholar
  81. 81.
    Yu W, Wang J, Yin J. Platelet-rich plasma: a promising product for treatment of peripheral nerve regeneration after nerve injury. Int J Neurosci. 2011;121(4):176–80.PubMedCrossRefGoogle Scholar
  82. 82.
    Zachar V, Rasmussen JG, Fink T. Isolation and growth of adipose tissue-derived stem cells. Methods Mol Biol. 2011;698:37–49.PubMedCrossRefGoogle Scholar
  83. 83.
    Zuk PA, Zhu M, Mizuno H, Huang JI, Futrell WJ, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7:211–26.PubMedCrossRefGoogle Scholar
  84. 84.
    Gronthos S, Franklin DM, Leddy HA, Robey PG, Storms RW, Gimble JM. Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol. 2001;189(1):54–63.PubMedCrossRefGoogle Scholar
  85. 85.
    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.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag London 2015

Authors and Affiliations

  • Phuc Van Pham
    • 1
  • Khanh Hong Thien Bui
    • 2
  • Dat Quoc Ngo
    • 3
  • Thao Thi-Phuong Doan
    • 3
  • Ngoc Bich Vu
    • 1
  • Nhung Hai Truong
    • 1
  • Dung Minh Le
    • 1
  • Ngoc Kim Phan
    • 1
  1. 1.Laboratory of Stem Cell Research and ApplicationUniversity of Science¸ Vietnam National University, Ho Chi Minh CityHo Chi Minh CityVietnam
  2. 2.Orthopaedic DepartmentUniversity Medical Center, Ho Chi Minh City, University of Medicine and Pharmacology, Ho Chi Minh CityHo Chi Minh CityVietnam
  3. 3.Department of PathologyUniversity of Medicine and Pharmacy, Ho Chi Minh CityHo Chi Minh CityVietnam

Personalised recommendations