Regeneration of articular cartilage using adipose stem cells

Journal of Biomedical Materials Research - Part A

Volumn 104, Issue 7, 2016, Pages 1830-1844

  Im, Gun Il ^a  

^a Dongguk University Ilsan Hospital   (South Korea)

Author keywords

adipose stem cells; articular cartilage; regeneration

Indexed keywords

CELLS; CYTOLOGY; DEFECTS; STEM CELLS;

ADIPOSE STEM CELLS; ARTICULAR CARTILAGES; CARTILAGE REGENERATION; CLINICAL APPLICATION; DIFFERENTIATION PROCESS; OSTEOCHONDRAL DEFECTS; REGENERATION; TIME-CONSUMING PROCEDURE;

CARTILAGE;

ATELOCOLLAGEN; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 6; COLLAGEN TYPE 1; COLLAGEN TYPE 2; COLLAGENASE; OSTEOGENIC PROTEIN 1; POLYCAPROLACTONE; POLYLACTIC ACID; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA;

ADIPOSE DERIVED STEM CELL; ADULT STEM CELL; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CELLS; CHONDROCYTE IMPLANTATION; CHONDROGENESIS; CLINICAL ASSESSMENT; COCULTURE; COMPARATIVE STUDY; GENE TRANSFER; GENERAL SURGERY; HUMAN; HYPOXEMIA; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; LIPOSUCTION; MORBIDITY; MULTIPOTENT STEM CELL; NONHUMAN; OSTEOARTHRITIS; OSTEOCHONDRITIS; REVIEW; SUBCUTANEOUS FAT; TISSUE CULTURE; TISSUE REGENERATION; TISSUE SCAFFOLD; ADIPOSE TISSUE; ANIMAL; CLINICAL TRIAL (TOPIC); CYTOLOGY; PHYSIOLOGY; REGENERATION; STEM CELL;

ADIPOSE TISSUE; ANIMALS; CARTILAGE, ARTICULAR; CHONDROGENESIS; CLINICAL TRIALS AS TOPIC; HUMANS; REGENERATION; STEM CELLS;

EID: 84978324248     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.35705     Document Type: Review

References (107)

1. Vinatier C, Bouffi C, Merceron C, Gordeladze J, Brondello JM, Jorgensen C, Weiss P, Guicheux J, Noël D., Cartilage tissue engineering: Towards a biomaterial-assisted mesenchymal stem cell therapy. Curr Stem Cell Res Ther 2009; 4: 318.
2. Kon E, Filardo G, Roffi A, Andriolo L, Marcacci M., New trends for knee cartilage regeneration: From cell-free scaffolds to mesenchymal stem cells. Curr Rev Musculoskeletal Med 2012; 5: 236.
3. Madry H, Grün UW, Knutsen G., Cartilage repair and joint preservation: Medical and surgical treatment options. Deutsches Ärzteblatt International 2011; 108: 669.
4. Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaksson O, Peterson L., Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 1994; 331: 889.
5. Giannini S, Buda R, Cavallo M, Ruffilli A, Cenacchi A, Cavallo C, Vannini F., Cartilage repair evolution in post-traumatic osteochondral lesions of the talus: From open field autologous chondrocyte to bone-marrow-derived cells transplantation. Injury 2010; 41: 1196.
6. Caplan AI, Dennis JE., Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006; 98: 1076.
7. Lodi D, Iannitti T, Palmieri B., Stem cells in clinical practice: Applications and warnings. J Exp Clin Cancer Res 2011; 30: 1.
8. Abumaree M, Al Jumah M, Pace RA, Kalionis B., Immunosuppressive properties of mesenchymal stem cells. Stem Cell Rev Rep 2012; 8: 375.
9. Caplan AI., Review: Mesenchymal stem cells: Cell-based reconstructive therapy in orthopedics. Tissue Eng 2005; 11: 1198.
10. Chen FH, Tuan RS., Mesenchymal stem cells in arthritic diseases. Arthritis Res Ther 2008; 10: 223.
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: 4279.
12. Strioga M, Viswanathan S, Darinskas A, Slaby O, Michalek J., Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells. Stem Cells Dev 2012; 21: 2724.
13. Im GI, Shin YW, Lee KB., Do adipose tissue-derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow-derived cells? Osteoarthritis Cartilage 2005; 13: 845.
14. Fischer G., Liposculpture: The "correct" history of liposuction. Part I. J Dermatol Surg Oncol 1990; 16: 1087.
15. Illouz YG., The fat cell "graft": A new technique to fill depressions. Plast Reconstruct Surg 1986; 78: 122.
16. Coleman SR., Facial recontouring with lipostructure. Clin Plast Surg 1997; 24: 347.
17. Coleman SR., Long-term survival of fat transplants: Controlled demonstrations. Aesthetic Plast Surg 1995; 19: 421.
18. Stromps JP, Paul NE, Rath B, Nourbakhsh M, Bernhagen J, Pallua N., Chondrogenic differentiation of human adipose-derived stem cells: A new path in articular cartilage defect management? BioMed Res Int 2014; 2014: 740926.
19. Nguyen PS, Desouches C, Gay AM, Hautier A, Magalon G., Development of micro-injection as an innovative autologous fat graft technique: The use of adipose tissue as dermal filler. J Plast Reconstruct Aesthetic Surg 2012; 65: 1692.
20. Alharbi Z, Oplander C, Almakadi S, Fritz A, Vogt M, Pallua N., Conventional vs. micro-fat harvesting: How fat harvesting technique affects tissue-engineering approaches using adipose tissue-derived stem/stromal cells. J Plast Reconstruct Aesthetic Surg 2013; 66: 1271.
21. Bunnell BA, Flaat M, Gagliardi C, Patel B, Ripoll C., Adipose-derived stem cells: Isolation, expansion and differentiation. Methods 2008; 45: 115.
22. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH., Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng 2001; 7: 211.
23. Lin Y, Tian W, Chen X, Yan Z, Li Z, Qiao J, Liu L, Tang W, Zheng X., Expression of exogenous or endogenous green fluorescent protein in adipose tissue-derived stromal cells during chondrogenic differentiation. Mol Cell Biochem 2005; 277: 181.
24. Kim HJ, Im GI,. Combination of transforming growth factor-beta2 and bone morphogenetic protein 7 enhances chondrogenesis from adipose tissue-derived mesenchymal stem cells. Tissue Eng Part A 2009; 15: 1543.
25. Mehlhorn A, Niemeyer P, Kaschte K, Muller L, Finkenzeller G, Hartl D, Sudkamp N, Schmal H., Differential effects of BMP-2 and TGF-β1 on chondrogenic differentiation of adipose derived stem cells. Cell Prolifer 2007; 40: 809.
26. Sakaguchi Y, Sekiya I, Yagishita K, Muneta T., Comparison of human stem cells derived from various mesenchymal tissues: Superiority of synovium as a cell source. Arthritis Rheum 2005; 52: 2521.
27. Mochizuki T, Muneta T, Sakaguchi Y, Nimura A, Yokoyama A, Koga H, Sekiya I., Higher chondrogenic potential of fibrous synovium-and adipose synovium-derived cells compared with subcutaneous fat-derived cells: Distinguishing properties of mesenchymal stem cells in humans. Arthritis Rheum 2006; 54: 843.
28. English A, Jones E, Corscadden D, Henshaw K, Chapman T, Emery P, McGonagle D., A comparative assessment of cartilage and joint fat pad as a potential source of cells for autologous therapy development in knee osteoarthritis. Rheumatology 2007; 46: 1676.
29. 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.
30. Mackay AM, Beck SC, Murphy JM, Barry FP, Chichester CO, Pittenger MF., Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 1998; 4: 415.
31. Boeuf S, Richter W., Chondrogenesis of mesenchymal stem cells: Role of tissue source and inducing factors. Stem Cell Res Ther 2010; 1: 31.
32. Barry F, Boynton RE, Liu B, Murphy JM., Chondrogenic differentiation of mesenchymal stem cells from bone marrow: Differentiation-dependent gene expression of matrix components. Exp Cell Res 2001; 268: 189.
33. Estes BT, Wu AW, Guilak F., Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenetic protein 6. Arthritis Rheum 2006; 54: 1222.
34. Hennig T, Lorenz H, Thiel A, Goetzke K, Dickhut A, Geiger F, Richter W., Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGFβ receptor and BMP profile and is overcome by BMP-6. J Cell Physiol 2007; 211: 682.
35. Taha M, Valojerdi M, Mowla S., Effect of bone morphogenetic protein-4 (BMP-4) on adipocyte differentiation from mouse embryonic stem cells. Anatom Histol Embryol 2006; 35: 271.
36. Vicente LM, Vázquez GM, Entrena A, Olmedillas LS, García-Arranz M, García-Olmo D, Zapata A., Low doses of bone morphogenetic protein 4 increase the survival of human adipose-derived stem cells maintaining their stemness and multipotency. Stem Cells Dev 2011; 20: 1011.
37. Kim BS, Kang KS, Kang SK., Soluble factors from ASCs effectively direct control of chondrogenic fate. Cell Prolifer 2010; 43: 249.
38. Kim HJ, Im GI., Chondrogenic differentiation of adipose tissue-derived mesenchymal stem cells: Greater doses of growth factor are necessary. J Orthop Res 2009; 27: 612.
39. Malpeli M, Randazzo N, Cancedda R, Dozin B., Serum-free growth medium sustains commitment of human articular chondrocyte through maintenance of Sox9 expression. Tissue Eng 2004; 10: 145.
40. Bilgen B, Orsini E, Aaron RK, Ciombor DM., FBS suppresses TGF-β1-induced chondrogenesis in synoviocyte pellet cultures while dexamethasone and dynamic stimuli are beneficial. J Tissue Eng Regen Med 2007; 1: 436.
41. 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 School 2004; 71: 240.
42. Tsuchiya K, Chen G, Ushida T, Matsuno T, Tateishi T., The effect of coculture of chondrocytes with mesenchymal stem cells on their cartilaginous phenotype in vitro. Mater Sci Eng: C 2004; 24: 391.
43. Mo XT, Guo SC, Xie HQ, Deng L, Zhi W, Xiang Z, Li XQ, Yang ZM., Variations in the ratios of co-cultured mesenchymal stem cells and chondrocytes regulate the expression of cartilaginous and osseous phenotype in alginate constructs. Bone 2009; 45: 42.
44. Hendriks JA, Miclea RL, Schotel R, de Bruijn E, Moroni L, Karperien M, Riesle J, van Blitterswijk CA., Primary chondrocytes enhance cartilage tissue formation upon co-culture with a range of cell types. Soft Matter 2010; 6: 5080.
45. Lee JS, Im GI., Influence of chondrocytes on the chondrogenic differentiation of adipose stem cells. Tissue Eng A 2010; 16: 3569.
46. Hildner F, Concaro S, Peterbauer A, Wolbank S, Danzer M, Lindahl A, Gatenholm P, Redl H, van Griensven M., Human adipose-derived stem cells contribute to chondrogenesis in coculture with human articular chondrocytes. Tissue Eng A 2009; 15: 3961.
47. Vats A, Bielby RC, Tolley N, Dickinson SC, Boccaccini AR, Hollander AP, Bishop AE, Polak JM., Chondrogenic differentiation of human embryonic stem cells: The effect of the micro-environment. Tissue Eng 2006; 12: 1687.
48. Li X, Lee JP, Balian G, Greg Anderson D., Modulation of chondrocytic properties of fat-derived mesenchymal cells in co-cultures with nucleus pulposus. Connect Tissue Res 2005; 46: 75.
49. Lu Z, Doulabi BZ, Wuisman P, Bank R, Helder M., Differentiation of adipose stem cells by nucleus pulposus cells: Configuration effect. Biochem Biophys Res Commun 2007; 359: 991.
50. Lu Z, Zandieh Doulabi B, Wuisman P, Bank R, Helder M., Influence of collagen type II and nucleus pulposus cells on aggregation and differentiation of adipose tissue-derived stem cells. J Cell Mol Med 2008; 12: 2812.
51. Lennon DP, Edmison JM, Caplan AI., Cultivation of rat marrow-derived mesenchymal stem cells in reduced oxygen tension: Effects on in vitro and in vivo osteochondrogenesis. J Cell Physiol 2001; 187: 345.
52. Domm C, Schunke M, Christesen K, Kurz B., Redifferentiation of dedifferentiated bovine articular chondrocytes in alginate culture under low oxygen tension. Osteoarthritis Cartilage 2002; 10: 13.
53. Munir S, Foldager CB, Lind M, Zachar V, Soballe K, Koch TG., Hypoxia enhances chondrogenic differentiation of human adipose tissue-derived stromal cells in scaffold-free and scaffold systems. Cell Tissue Res 2014; 355: 89.
54. Choi JR, Pingguan-Murphy B, Wan Abas WA, Noor Azmi MA, Omar SZ, Chua KH, Wan Safwani WK., Impact of low oxygen tension on stemness, proliferation and differentiation potential of human adipose-derived stem cells. Biochem Biophys Res Commun 2014; 448: 218.
55. Bassett CA, Pawluk RJ, Pilla AA., Augmentation of bone repair by inductively coupled electromagnetic fields. Science 1974; 184: 575.
56. Chen CH, Lin YS, Fu YC, Wang CK, Wu SC, Wang GJ, Eswaramoorthy R, Wang YH, Wang CZ, Wang YH, Lin SY, Chang JK, Ho ML., Electromagnetic fields enhance chondrogenesis of human adipose-derived stem cells in a chondrogenic microenvironment in vitro. J Appl Physiol 2013; 114: 647.
57. Gimble JM, Grayson W, Guilak F, Lopez MJ, Vunjak-Novakovic G., Adipose tissue as a stem cell source for musculo-skeletal regeneration. Front Biosci (Scholar Edition) 2011; 3: 69.
58. Peng LH, Fung KP, Leung PC, Gao JQ., Genetically manipulated adult stem cells for wound healing. Drug Discov Today 2011; 16: 957.
59. Bing Jin X, Sheng Sun Y, Zhang K, Wang J, Ping Shi T, Dong Ju X, Quan Lou S., Ectopic neocartilage formation from predifferentiated human adipose derived stem cells induced by adenoviral-mediated transfer of hTGF beta2. Biomaterials 2007; 28: 2994.
60. Jin XB, Sun YS, Zhang K, Wang J, Shi TP, Ju XD, Lou SQ., Tissue engineered cartilage from hTGF β2 transduced human adipose derived stem cells seeded in PLGA/alginate compound in vitro and in vivo. J Biomed Mater Res A 2008; 86: 1077.
61. Yang Y, Tian H., Repair of articular cartilage defects by autologous adipose derived mesenchymal stem cell: Experiment with rabbits. Zhonghua Yi Xue Za Zhi 2008; 88: 2214.
62. 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 A 2012; 18: 2114.
63. Diekman BO, Estes BT, Guilak F., The effects of BMP6 overexpression on adipose stem cell chondrogenesis: Interactions with dexamethasone and exogenous growth factors. J Biomed Mater Res A 2010; 93: 994.
64. Garza-Veloz I, Romero-Diaz VJ, Martinez-Fierro ML, Marino-Martinez IA, Gonzalez-Rodriguez M, Martinez-Rodriguez HG, Espinoza-Juarez MA, Bernal-Garza DA, Ortiz-Lopez R, Rojas-Martinez A., Analyses of chondrogenic induction of adipose mesenchymal stem cells by combined co-stimulation mediated by adenoviral gene transfer. Arthritis Res Ther 2013; 15: R80.
65. Li J, Zhao Q, Wang E, Zhang C, Wang G, Yuan Q., Dynamic compression of rabbit adipose-derived stem cells transfected with insulin-like growth factor 1 in chitosan/gelatin scaffolds induces chondrogenesis and matrix biosynthesis. J Cell Physiol 2012; 227: 2003.
66. de Crombrugghe B, Lefebvre V, Behringer RR, Bi W, Murakami S, Huang W., Transcriptional mechanisms of chondrocyte differentiation. Matrix Biol 2000; 19: 389.
67. Lefebvre V, Huang W, Harley VR, Goodfellow PN, de Crombrugghe B., SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1 (II) collagen gene. Mol Cell Biol 1997; 17: 2336.
68. Zhao Q, Eberspaecher H, Lefebvre V, de Crombrugghe B., Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev Dyn 1997; 209: 377.
69. Yang Z, Huang CY, Candiotti KA, Zeng X, Yuan T, Li J, Yu H, Abdi S., Sox-9 facilitates differentiation of adipose tissue-derived stem cells into a chondrocyte-like phenotype in vitro. J Orthop Res 2011; 29: 1291.
70. Han Y, Lefebvre V., L-Sox5 and Sox6 drive expression of the aggrecan gene in cartilage by securing binding of Sox9 to a far-upstream enhancer. Mol Cell Biol 2008; 28: 4999.
71. Dy P, Smits P, Silvester A, Penzo-Méndez A, Dumitriu B, Han Y, Carol A, Kingsley DM, Lefebvre V., Synovial joint morphogenesis requires the chondrogenic action of Sox5 and Sox6 in growth plate and articular cartilage. Dev Biol 2010; 341: 346.
72. Yang HN, Park JS, Woo DG, Jeon SY, Do HJ, Lim HY, Kim SW, Kim JH, Park KH., Chondrogenesis of mesenchymal stem cells and dedifferentiated chondrocytes by transfection with SOX Trio genes. Biomaterials 2011; 32: 7695.
73. 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: 2016.
74. 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: 4385.
75. Shi J, Zhang X, Zhu J, Pi Y, Hu X, Zhou C, Ao Y., Nanoparticle delivery of the bone morphogenetic protein 4 gene to adipose-derived stem cells promotes articular cartilage repair in vitro and in vivo. Arthroscopy 2013; 29: 2001.
76. Winter A, Breit S, Parsch D, Benz K, Steck E, Hauner H, Weber RM, Ewerbeck V, Richter W., Cartilage-like gene expression in differentiated human stem cell spheroids: A comparison of bone marrow-derived and adipose tissue-derived stromal cells. Arthritis Rheum 2003; 48: 418.
77. Koga H, Muneta T, Nagase T, Nimura A, Ju YJ, Mochizuki T, Sekiya I., Comparison of mesenchymal tissues-derived stem cells for in vivo chondrogenesis: Suitable conditions for cell therapy of cartilage defects in rabbit. Cell Tissue Res 2008; 333: 207.
78. 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: 1675.
79. Xie X, Wang Y, Zhao C, Guo S, Liu S, Jia W, Tuan RS, Zhang C., Comparative evaluation of MSCs from bone marrow and adipose tissue seeded in PRP-derived scaffold for cartilage regeneration. Biomaterials 2012; 33: 7008.
80. Li Q, Tang J, Wang R, Bei C, Xin L, Zeng Y, Tang X., Comparing the chondrogenic potential in vivo of autogeneic mesenchymal stem cells derived from different tissues. Artif Cells Blood SubstImmobiliz Biotechnol 2011; 39: 31.
81. Oliveira JT, Gardel LS, Rada T, Martins L, Gomes ME, Reis RL., Injectable gellan gum hydrogels with autologous cells for the treatment of rabbit articular cartilage defects. J Orthop Res 2010; 28: 1193.
82. 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: 1615.
83. 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: 2683.
84. Wei Y, Hu H, Wang H, Wu Y, Deng L, Qi J., Cartilage regeneration of adipose-derived stem cells in a hybrid scaffold from fibrin-modified PLGA. Cell Transplant 2009; 18: 159.
85. Han Y, Wei Y, Wang S, Song Y., Cartilage regeneration using adipose-derived stem cells and the controlled-released hybrid microspheres. Joint Bone Spine 2010; 77: 27.
86. Masuoka K, Asazuma T, Hattori H, Yoshihara Y, Sato M, Matsumura K, Matsui T, Takase B, Nemoto K, Ishihara M., Tissue engineering of articular cartilage with autologous cultured adipose tissue-derived stromal cells using atelocollagen honeycomb-shaped scaffold with a membrane sealing in rabbits. J Biomed Mater Res B Appl Biomater 2006; 79: 25.
87. Gong L, Zhou X, Wu Y, Zhang Y, Wang C, Zhou H, Guo F, Cui L., Proteomic analysis profile of engineered articular cartilage with chondrogenic differentiated adipose tissue-derived stem cells loaded polyglycolic acid mesh for weight-bearing area defect repair. Tissue Eng A 2014; 20: 575.
88. Nathan S, De SD, Thambyah A, Fen C, Goh J, Lee EH., Cell-based therapy in the repair of osteochondral defects: A novel use for adipose tissue. Tissue Eng 2003; 9: 733.
89. Zhang HN, Lei L, Ping L, Wang YZ, Lü C., Uninduced adipose-derived stem cells repair the defect of full-thickness hyaline cartilage. Chin J Traumatol 2009; 12: 92.
90. Wang ZJ, An RZ, Zhao JY, Zhang Q, Yang J, Wang JB, Wen GY, Yuan XH, Qi XW, Li SJ, Ye XC., Repair of articular cartilage defects by tissue-engineered cartilage constructed with adipose-derived stem cells and acellular cartilaginous matrix in rabbits. Genet Mol Res GMR 2014; 13: 4599.
91. Van Pham P, Bui KH, Ngo DQ, Vu NB, Truong NH, Phan NL, Le DM, Duong TD, Nguyen TD, Le VT, Phan NK., Activated platelet-rich plasma improves adipose-derived stem cell transplantation efficiency in injured articular cartilage. Stem Cell Res Ther 2013; 4: 91.
92. Im GI, Lee JH., Repair of osteochondral defects with adipose stem cells and a dual growth factor-releasing scaffold in rabbits. J Biomed Mater Res B Appl Biomater 2010; 92: 552.
93. Murata D, Tokunaga S, Tamura T, Kawaguchi H, Miyoshi N, Fujiki M, Nakayama K, Misumi K., A preliminary study of osteochondral regeneration using a scaffold-free three-dimensional construct of porcine adipose tissue-derived mesenchymal stem cells. J Orthop Surg Res 2015; 10: 35.
94. Lee DH, Sonn C, Han SB, Oh Y, Lee KM, Lee SH., Synovial fluid CD34- CD44+ CD90+ mesenchymal stem cell levels are associated with the severity of primary knee osteoarthritis. Osteoarthritis Cartilage 2012; 20: 106.
95. Murphy JM, Dixon K, Beck S, Fabian D, Feldman A, Barry F., Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis. Arthritis Rheum 2002; 46: 704.
96. Chua KH, Safwani WKZW, Hamid AA, Shuhup SK, Haflah NHM, Yahaya NHM., Retropatellar fat pad-derived stem cells from older osteoarthritic patients have lesser differentiation capacity and expression of stemness genes. Cytotherapy 2014; 16: 599.
97. Centeno CJ, Schultz JR, Cheever M, Robinson B, Freeman M, Marasco W., Safety and complications reporting on the re-implantation of culture-expanded mesenchymal stem cells using autologous platelet lysate technique. Curr stem Cell Res Ther 2010; 5: 81.
98. Toghraie F, Chenari N, Gholipour M, 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.
99. Fatemehsadat Toghraie D, Chenari N, Ghaderi A., Scaffold-free adipose-derived stem cells (ASCs) improve experimentally induced osteoarthritis in rabbits. Arch Iran Med 2012; 15: 495.
100. Desando G, Cavallo C, Sartoni F, Martini L, Parrilli A, Veronesi F, Fini M, Giardino R, Facchini A, Grigolo B., Intra-articular delivery of adipose derived stromal cells attenuates osteoarthritis progression in an experimental rabbit model. Arthritis Res Ther 2013; 15: R22.
101. ter Huurne M, Schelbergen R, Blattes R, Blom A, de Munter W, Grevers LC, Jeanson J, Noël D, Casteilla L, Jorgensen C., Antiinflammatory and chondroprotective effects of intraarticular injection of adipose-derived stem cells in experimental osteoarthritis. Arthritis Rheum 2012; 64: 3604.
102. Ude CC, Sulaiman SB, Min-Hwei N, Hui-Cheng C, Ahmad J, Yahaya NM, Saim AB, Idrus RB., Cartilage regeneration by chondrogenic induced adult stem cells in osteoarthritic sheep model. PloS One 2014; 9: e98770.
103. 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 Rep 2011; 5: 296.
104. Koh YG, Jo SB, Kwon OR, Suh DS, Lee SW, Park SH, Choi YJ., Mesenchymal stem cell injections improve symptoms of knee osteoarthritis. Arthroscopy 2013; 29: 748.
105. Koh YG, Choi YJ., Infrapatellar fat pad-derived mesenchymal stem cell therapy for knee osteoarthritis. Knee 2012; 19: 902.
106. Koh YG, Choi YJ, Kwon SK, Kim YS, Yeo JE., Clinical results and second-look arthroscopic findings after treatment with adipose-derived stem cells for knee osteoarthritis. Knee Surg Sports Traumatol Arthrosc 2015; 23: 1308.
107. Jo CH, Lee YG, Shin WH, Kim H, Chai JW, Jeong EC, Kim JE, Shim H, Shin JS, Shin IS, Ra JC, Oh S, Yoon KS., Intra-articular injection of mesenchymal stem cells for the treatment of osteoarthritis of the knee: A proof-of-concept clinical trial. Stem Cells 2014; 32: 1254.