Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype

Nature Protocols

Volumn 5, Issue 7, 2010, Pages 1294-1311

  Estes, Bradley T ^a   Diekman, Brian O ^a   Gimble, Jeffrey M ^b   Guilak, Farshid ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; COLLAGEN TYPE 10A1; COLLAGEN TYPE 1A1; COLLAGEN TYPE 2A1; MEMBRANE PROTEIN; PROTEIN AGC1; RNA 18S; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; BONE MORPHOGENETIC PROTEIN 6; TRANSFORMING GROWTH FACTOR BETA3;

ADIPOSE TISSUE CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL EXPANSION; CELL ISOLATION; CELL LINEAGE; CHONDROGENESIS; CLINICAL PROTOCOL; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL; MOLECULAR BIOLOGY; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN AGGREGATION; QUANTITATIVE ANALYSIS; TISSUE ENGINEERING; ADIPOSE TISSUE; ADULT; ADULT STEM CELL; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL PROLIFERATION; CULTURE TECHNIQUE; CYTOLOGY; MULTIPOTENT STEM CELL; PHYSIOLOGY; PROCEDURES;

ADIPOSE TISSUE; ADULT; ADULT STEM CELLS; BONE MORPHOGENETIC PROTEIN 6; CARTILAGE, ARTICULAR; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; HUMANS; MULTIPOTENT STEM CELLS; PHENOTYPE; TISSUE ENGINEERING; TRANSFORMING GROWTH FACTOR BETA3;

EID: 77954286452     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2010.81     Document Type: Article

References (67)

1. Hootman, J.M., Brault, M.W., Helmick, C.G., Theis, K.A. & Armour, B.S. Prevalence and most common causes of disability among adults\United States, 2005. Morb. Mortal. Wkly Rep. 58, 421-426 (2009).
2. Praemer, A., Furner, S. & Rice, D.P. Musculoskeletal Conditions in the United States. (American Academy of Orthopaedic Surgeons, Rosemont, IL, 1999).
3. Goldring, M.B. Update on the biology of the chondrocyte and new approaches to treating cartilage diseases. Best Pract. Res. Clin. Rheumatol. 20, 1003-1025 (2006).
4. Jackson, D.W., Simon, T.M. & Aberman, H.M. Symptomatic articular cartilage degeneration: the impact in the new millennium. Clin. Orthop. Relat. Res (Suppl 391): S14-S25 (2001).
5. Rotter, N., Haisch, A. & Bucheler, M. Cartilage and bone tissue engineering for reconstructive head and neck surgery. Eur. Arch. Otorhinolaryngol. 262, 539-545 (2005). (Pubitemid 41159114)
6. Langer, R. & Vacanti, J.P. Tissue engineering. Science 260, 920-926 (1993).
7. Aichroth, P.M., Patel, D.V. & Moyes, S.T. A prospective review of arthroscopic debridement for degenerative joint disease of the knee. Int. Orthop. 15, 351-355 (1991).
8. Aubin, P.P., Cheah, H.K., Davis, A.M. & Gross, A.E. Long-term followup of fresh femoral osteochondral allografts for posttraumatic knee defects. Clin. Orthop. Relat. Res (Suppl 391): S318-S327 (2001).
9. Baumgaertner, M.R., Cannon, W.D. Jr., Vittori, J.M., Schmidt, E.S. & Maurer, R.C. Arthroscopic debridement of the arthritic knee. Clin. Orthop. Relat. Res. 253, 197-202 (1990).
10. Denoncourt, P.M., Patel, D. & Dimakopoulos, P. Arthroscopy update #1. Treatment of osteochondrosis dissecans of the knee by arthroscopic curettage, follow-up study. Orthop. Rev. 15, 652-657 (1986).
11. Emmerson, B.C. et al. Fresh osteochondral allografting in the treatment of osteochondritis dissecans of the femoral condyle. Am. J. Sports. Med. 35, 907-914 (2007).
12. Friedman, M.J., Berasi, C.C. & Fox, J.M. Preliminary results with abrasion arthroplasty in the osteoarthritic knee. Clin. Orthop. Relat. Res. 182, 200-205 (1984).
13. Ghazavi, M.T., Pritzker, K.P., Davis, A.M. & Gross, A.E. Fresh osteochondral allografts for post-traumatic osteochondral defects of the knee. J. Bone Joint Surg. Br. 79, 1008-1013 (1997).
14. Johnson, L.L. Arthroscopic abrasion arthroplasty: a review. Clin. Orthop. Relat. Res Suppl 391: S306-S317 (2001).
15. Kish, G., Modis, L. & Hangody, L. Osteochondral mosaicplasty for the treatment of focal chondral and osteochondral lesions of the knee and talus in the athlete. Rationale, indications, techniques, and results. Clin. Sports Med. 18, 45-66, vi (1999).
16. Steadman, J.R. et al. Outcomes of microfracture for traumatic chondral defects of the knee: average 11-year follow-up. Arthroscopy 19, 477-484 (2003).
17. Steadman, J.R., Rodkey, W.G. & Rodrigo, J.J. Microfracture: surgical technique and rehabilitation to treat chondral defects. Clin. Orthop. Relat. Res. (Suppl 391): S362-S369 (2001).
18. Nehrer, S., Spector, M. & Minas, T. Histologic analysis of tissue after failed cartilage repair procedures. Clin. Orthop. Relat. Res. 365, 149-162 (1999).
19. Shapiro, F., Koide, S. & Glimcher, M.J. Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J. Bone Joint Surg. Am. 75, 532-553 (1993).
20. Tew, S.R., Kwan, A.P., Hann, A., Thomson, B.M. & Archer, C.W. The reactions of articular cartilage to experimental wounding: role of apoptosis. Arthritis Rheum. 43, 215-225 (2000).
21. Breinan, H.A. et al. Effect of cultured autologous chondrocytes on repair of chondral defects in a canine model. J. Bone Joint Surg. Am. 79, 1439-1451 (1997).
22. Brittberg, M. et al. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N. Engl. J. Med. 331, 889-895 (1994).
23. Knutsen, G. et al. Autologous chondrocyte implantation compared with microfracture in the knee. A randomized trial. J. Bone Joint Surg. Am. 86-a, 455-464 (2004).
24. Lee, C.R., Grodzinsky, A.J., Hsu, H.P., Martin, S.D. & Spector, M. Effects of harvest and selected cartilage repair procedures on the physical and biochemical properties of articular cartilage in the canine knee. J. Orthop. Res. 18, 790-799 (2000).
25. Thirion, S. & Berenbaum, F. Culture and phenotyping of chondrocytes in primary culture. Methods Mol. Med. 100, 1-14 (2004).
26. Stokes, D.G. et al. Assessment of the gene expression profle of differentiated and dedifferentiated human fetal chondrocytes by microarray analysis. Arthritis Rheum. 46, 404-419 (2002).
27. Ohara, K., Nakamura, K. & Ohta, E. Chest wall deformities and thoracic scoliosis after costal cartilage graft harvesting. Plast. Reconstr. Surg. 99, 1030-1036 (1997).
28. Chang, S.C., Tobias, G., Roy, A.K., Vacanti, C.A. & Bonassar, L.J. Tissue engineering of autologous cartilage for craniofacial reconstruction by injection molding. Plast. Reconstr. Surg. 112, 793-799; discussion 800-801 (2003).
29. Caplan, A.I. & Bruder, S.P. Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol. Med. 7, 259-264 (2001).
30. Owen, M. & Friedenstein, A.J. Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found. Symp. 136, 42-60 (1988).
31. Pittenger, M.F. et al. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147 (1999).
32. Aust, L. et al. Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy 6, 7-14 (2004).
33. Gimble, J.M. & Guilak, F. Differentiation potential of adipose derived adult stem (ADAS) cells. Curr. Top. Dev. Biol. 58, 137-160 (2003).
34. Awad, H.A., Halvorsen, Y.D., Gimble, J.M. & Guilak, F. Effects of transforming growth factor beta1 and dexamethasone on the growth and chondrogenic differentiation of adipose-derived stromal cells. Tissue Eng. 9, 1301-1312 (2003).
35. Awad, H.A., Wickham, M.Q., Leddy, H.A., Gimble, J.M. & Guilak, F. Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials 25, 3211-3222 (2004).
36. Erickson, G.R. et al. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem. Biophys. Res. Commun. 290, 763-769 (2002).
37. Guilak, F. et al. Clonal analysis of the differentiation potential of human adipose-derived adult stem cells. J. Cell Physiol. 206, 229-237 (2006). (Pubitemid 41740736)
38. Halvorsen, Y.C., Wilkison, W.O. & Gimble, J.M. Adipose-derived stromal cells-their utility and potential in bone formation. Int. J. Obes. Relat. Metab. Disord. 24 (Suppl 4): S41-S44 (2000).
39. Huang, C.Y., Reuben, P.M., D'Ippolito, G., Schiller, P.C. & Cheung, H.S. Chondrogenesis of human bone marrow-derived mesenchymal stem cells in agarose culture. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 278, 428-436 (2004).
40. Safford, K.M. et al. Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem. Biophys. Res. Commun. 294, 371-379 (2002).
41. Wickham, M.Q., Erickson, G.R., Gimble, J.M., Vail, T.P. & Guilak, F. Multipotent stromal cells derived from the infrapatellar fat pad of the knee. Clin. Orthop. Relat. Res. 412, 196-212 (2003).
42. Zuk, P.A. et al. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell. 13, 4279-4295 (2002).
43. Zuk, P.A. et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 7, 211-228 (2001).
44. Wang, D.W., Fermor, B., Gimble, J.M., Awad, H.A. & Guilak, F. Infuence of oxygen on the proliferation and metabolism of adipose derived adult stem cells. J. Cell. Physiol. 204, 184-191 (2005).
45. Estes, B.T., Wu, A.W. & Guilak, F. Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenetic protein 6. Arthritis Rheum. 54, 1222-1232 (2006). (Pubitemid 43672934)
46. Oedayrajsingh-Varma, M.J. et al. Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy 8, 166-177 (2006).
47. Estes, B.T., Diekman, B.O. & Guilak, F. Monolayer cell expansion conditions affect the chondrogenic potential of adipose-derived stem cells. Biotechnol. Bioeng. 99, 986-995 (2008).
48. Hennig, T. et al. Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGFbeta receptor and BMP profle and is overcome by BMP-6. J. Cell. Physiol. 211, 682-691 (2007).
49. Johnstone, B., Hering, T.M., Caplan, A.I., Goldberg, V.M. & Yoo, J.U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp. Cell. Res. 238, 265-272 (1998).
50. Cheng, N.C., Estes, B.T., Awad, H.A. & Guilak, F. Chondrogenic differentiation of adipose-derived adult stem cells by a porous scaffold derived from native articular cartilage extracellular matrix. Tissue Eng. Part A 15, 231-241 (2009).
51. Diekman, B.O., Rowland, C.R., Caplan, A.I., Lennon, D. & Guilak, F. Chondrogenesis of adult stem cells from adipose tissue and bone marrow: Induction by growth factors and cartilage derived matrix. Tissue Eng. Part A 16, 523-533 (2010).
52. Guilak, F. & Hung, C.T. In Basic Orthopaedic Biomechanics and Mechano-Biology (eds. Mow, V.C. & Huiskes, R.) 179-207 (Lippincott Williams & Wilkins, Philadelphia, 2004).
53. Mow, V.C. & Guo, X.E. Mechano-electrochemical properties of articular cartilage: their inhomogeneities and anisotropies. Annu. Rev. Biomed. Eng. 4, 175-209 (2002).
54. Mow, V.C., Proctor, C.S. & Kelly, M.A. In Basic Biomechanics of the Musculoskeletal System (eds. Nordin, M. & Frankel, V.H.) 31-58 (Lea & Febiger, Philadelphia, London, 1989).
55. Heinegård, D. & Oldberg, A. Structure and biology of cartilage and bone matrix noncollagenous macromolecules. FASEB J 3, 2042-2051 (1989).
56. Diekman, B.O., Estes, B.T. & Guilak, F. The effects of BMP6 overexpression on adipose stem cell chondrogenesis: interactions with dexamethasone and exogenous growth factors. J. Biomed. Mater. Res. A 93, 994-1003 (2010).
57. Estes, B.T., Wu, A.W., Storms, R.W. & Guilak, F. Extended passaging, but not aldehyde dehydrogenase activity, increases the chondrogenic potential of human adipose-derived adult stem cells. J. Cell Physiol. 209, 987-995 (2006).
58. Pilgaard, L. et al. Effect of oxygen concentration, culture format and donor variability on in vitro chondrogenesis of human adipose tissue-derived stem cells. Regen. Med. 4, 539-548 (2009).
59. Vidal, M.A. et al. Comparison of chondrogenic potential in equine mesenchymal stromal cells derived from adipose tissue and bone marrow. Vet. Surg. 37, 713-724 (2008).
60. Mehlhorn, A.T. et al. Differential effects of BMP-2 and TGF-beta1 on chondrogenic differentiation of adipose derived stem cells. Cell Prolif. 40, 809-823 (2007).
61. Guilak, F. et al. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5, 17-26 (2009).
62. Moutos, F.T., Freed, L.E. & Guilak, F. A biomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. Nat. Mater. 6, 162-167 (2007).
63. Neidert, M.R., Lee, E.S., Oegema, T.R. & Tranquillo, R.T. Enhanced fbrin remodeling in vitro with TGF-beta1, insulin and plasmin for improved tissue-equivalents. Biomaterials 23, 3717-3731 (2002).
64. Stegemann, H. & Stalder, K. Determination of hydroxyproline. Clin. Chim. Acta. 18, 267-273 (1967).
65. Hollander, A.P. et al. Increased damage to type II collagen in osteoarthritic articular cartilage detected by a new immunoassay. J. Clin. Invest 93, 1722-1732 (1994).
66. Nolan, T., Hands, R.E. & Bustin, S.A. Quantifcation of mRNA using realtime RT-PCR. Nat. Protoc. 1, 1559-1582 (2006).
67. Lefebvre, V., Huang, W., Harley, V.R., Goodfellow, P.N. & de Crombrugghe, B. SOX9 is a potent activator of the chondrocyte-specifc enhancer of the pro alpha1(II) collagen gene. Mol. Cell Biol. 17, 2336-2346 (1997)