Monolayer cell expansion conditions affect the chondrogenic potential of adipose-derived stem cells

Biotechnology and Bioengineering

Volumn 99, Issue 4, 2008, Pages 986-995

  Estes, Bradley T ^a   Diekman, Brian O ^a   Guilak, Farshid ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Adipose stem cells; Adult stem cells; Chondrogenesis; Differentiation; Mesenchymal stem cells; Progenitor cells

Indexed keywords

BIOPOLYMERS; DIFFERENTIATION (CALCULUS); ENZYMES; MONOLAYERS; SUSPENSIONS (FLUIDS); TISSUE CULTURE;

ADIPOSE STEM CELLS; FETAL BOVINE SERUM; MESENCHYMAL STEM CELLS; MONOLAYER CULTURE; PROGENITOR CELLS;

CELL GROWTH;

AGAROSE; GROWTH FACTOR;

ADIPOSE TISSUE CELL; ADULT; ARTICLE; CELL DENSITY; CELL DIFFERENTIATION; CELL EXPANSION; CELL GROWTH; CELL ISOLATION; CELL STRUCTURE; CELL VIABILITY; CHONDROGENESIS; FEMALE; GEL; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOTHESIS; ISOTOPE LABELING; LIPOSUCTION; PHENOTYPE; STEM CELL; SYNTHESIS; TISSUE CULTURE; ADIPOCYTE; CARTILAGE CELL; CELL CULTURE; CELL PROLIFERATION; CELL SURVIVAL; CULTURE TECHNIQUE; CYTOLOGY; METHODOLOGY; MIDDLE AGED; PHYSIOLOGY;

BOVINAE;

ADIPOCYTES; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; FEMALE; HUMANS; MIDDLE AGED; STEM CELLS;

EID: 39549109318     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.21662     Document Type: Article

References (48)

1. Afizah H, Yang Z, Hui JH, Ouyang HW, Lee EH. 2007. A comparison between the chondrogenic potential of human bone marrow stem cells (BMSCs) and adipose-derived stem cells (ADSCs) taken from the same donors. Tissue Eng 13(4):659-666.
2. Aust L, Devlin B, Foster SJ, Halvorsen YD, Hicok K, du Laney T, Sen A, Willingmyre GD, Gimble JM. 2004. Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy 6(1):7-14.
3. Awad HA, Halvorsen YD, Gimble JM, Guilak F. 2003. Effects of transforming growth factor beta1 and dexamethasone on the growth and chondrogenic differentiation of adipose-derived stromal cells. Tissue Eng 9(6):1301-1312.
4. Awad HA, Wickham MQ, Leddy HA, Gimble JM, Guilak F. 2004. Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials 25(16):3211-3222.
5. Bianchi G, Banfi A, Mastrogiacomo M, Notaro R, Luzzatto L, Cancedda R, Quarto R. 2003. Ex vivo enrichment of mesenchymal cell progenitors by fibroblast growth factor 2. Exp Cell Res 287(1):98-105.
6. Chiou M, Xu Y, Longaker MT. 2006. Mitogenic and chondrogenic effects of fibroblast growth factor-2 in adipose-derived mesenchymal cells. Biochem Biophys Res Commun 343(2):644-652.
7. Coleman RM, Case ND, Guldberg RE. 2007. Hydrogel effects on bone marrow stromal cell response to chondrogenic growth factors. Biomaterials 28(12):2077-2086.
8. Colter DC, Class R, DiGirolamo CM, Prockop DJ. 2000. Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. Proc Natl Acad Sci USA 97(7):3213-3218.
9. Colter DC, Sekiya I, Prockop DJ. 2001. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc Natl Acad Sci USA 98(14):7841-7845.
10. Darling EM, Athanasiou KA. 2005a. Rapid phenotypic changes in passaged articular chondrocyte subpopulations. J Orthop Res 23(2):425-432.
11. Darling EM, Athanasiou KA. 2005b. Retaining zonal chondrocyte phenotypeby means of novel growth environments. Tissue Eng 11(3-4):395-403.
12. De Ugarte DA, Morizono K, Elbarbary A, Alfonso Z, Zuk PA, Zhu M, Dragoo JL, Ashjian P, Thomas B, Benhaim P, Chen I, Fraser J, Hedrick MH. 2003. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 174(3):101-109.
13. Dragoo JL, Choi JY, Lieberman JR, Huang J, Zuk PA, Zhang J, Hedrick MH, Benhaim P. 2003. Bone induction by BMP-2 transduced stem cells derived from human fat. J Orthop Res 21(4):622-629.
14. Erickson GR, Gimble JM, Franklin DM, Rice HE, Awad H, Guilak F. 2002. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun 290(2):763-769.
15. Estes BT, Wu AW, Guilak F. 2006a. Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenetic protein 6. Arthritis Rheum 54(4):1222-1232.
16. Estes BT, Wu AW, Storms RW, Guilak F. 2006b. Extended passaging, but not aldehyde dehydrogenase activity, increases the chondrogenic potential of human adipose-derived adult stem cells. J Cell Physiol 209(3):987-995.
17. Fan VH, Tamama K, Au A, Littrell R, Richardson LB, Wright JW, Wells A, Griffith LG. 2007. Tethered epidermal growth factor provides a survival advantage to mesenchymal stem cells. Stem Cells 25(5):1241-1251.
18. Gimble J, Guilak F. 2003a. Adipose-derived adult stem cells: Isolation, characterization, and differentiation potential. Cytotherapy 5(5):362-369.
19. Gimble JM, Guilak F. 2003b. Differentiation potential of adipose derived adult stem (ADAS) cells. Curr Top Dev Biol 58:137-160.
20. Guilak F, Lott KE, Awad HA, Cao Q, Hicok KC, Fermor B, Gimble JM. 2006. Clonal analysis of the differentiation potential of human adipose-derived adult stem cells. J Cell Physiol 206(1):229-237.
21. Halvorsen YC, Wilkison WO, Gimble JM. 2000. Adipose-derived stromal cells-their utility and potential in bone formation. Int J Obes Relat Metab Disord 24(Suppl 4):S41-S44.
22. Halvorsen YD, Bond A, Sen A, Franklin DM, Lea-Currie YR, Sujkowski D, Ellis PN, Wilkison WO, Gimble JM. 2001a. Thiazolidinediones and glucocorticoids synergistically induce differentiation of human adipose tissue stromal cells: Biochemical, cellular, and molecular analysis. Metabolism 50(4):407-413.
23. Halvorsen YD, Franklin D, Bond AL, Hitt DC, Auchter C, Boskey AL, Paschalis EP, Wilkison WO, Gimble JM. 2001b. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng 7(6):729-741.
24. Hennig T, Lorenz H, Thiel A, Goetzke K, Dickhut A, Geiger F, Richter W. 2007. Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGFbeta receptor and BMP profile and is overcome by BMP-6. J Cell Physiol 211(3):682-691.
25. Huang JI, Zuk PA, Jones NF, Zhu M, Lorenz HP, Hedrick MH, Benhaim P. 2004. Chondrogenic potential of multipotential cells from human adipose tissue. Plast Reconstr Surg 113(2):585-594.
26. 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. 2002. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418(6893):41-49.
27. Lee RH, Kim B, Choi I, Kim H, Choi HS, Suh K, Bae YC, Jung JS. 2004. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem 14(4-6):311-324.
28. Lefebvre V, Huang W, Harley VR, Goodfellow PN, de Crombrugghe B. 1997. SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol Cell Biol 17(4):2336-2346.
29. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(- Delta Delta C(T)) Method. Methods 25(4):402-408.
30. Mallein-Gerin F, Garrone R, van der Rest M. 1991. Proteoglycan and collagen synthesis are correlated with actin organization in dedifferentiating chondrocytes. Eur J Cell Biol 56(2):364-373.
31. Mastrogiacomo M, Cancedda R, Quarto R. 2001. Effect of different growth factors on the chondrogenic potential of human bone marrow stromal cells. Osteoarthritis Cartilage 9(Suppl A):S36-S40.
32. Mehlhorn AT, Niemeyer P, Kaiser S, Finkenzeller G, Stark GB, Sudkamp NP, Schmal H. 2006. Differential expression pattern of extracellular matrix molecules during chondrogenesis of mesenchymal stem cells from bone marrow and adipose tissue. Tissue Eng 12(10):2853-2862.
33. Mizuno H, Zuk PA, Zhu M, Lorenz HP, Benhaim P, Hedrick MH. 2002. Myogenic differentiation by human processed lipoaspirate cells. Plast Reconstr Surg 109(1):199-209; discussion 210-211.
34. Quarto N, Longaker MT. 2006. FGF-2 inhibits osteogenesis in mouse adipose tissue-derived stromal cells and sustains their proliferative and osteogenic potential state. Tissue Eng 12(6):1405-1418.
35. Reyes M, Lund T, Lenvik T, Aguiar D, Koodie L, Verfaillie CM. 2001. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 98(9):2615-2625.
36. Reyes M, Dudek A, Jahagirdar B, Koodie L, Marker PH, Verfaillie CM. 2002. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 109(3):337-346.
37. Safford KM, Hicok KC, Safford SD, Halvorsen YD, Wilkison WO, Gimble JM, Rice HE. 2002. Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem Biophys Res Commun 294(2): 371-379.
38. Schwartz RE, Reyes M, Koodie L, Jiang Y, Blackstad M, Lund T, Lenvik T, Johnson S, Hu WS, Verfaillie CM. 2002. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J Clin Invest 109(10):1291-1302.
39. Sekiya I, Larson BL, Smith JR, Pochampally R, Cui JG, Prockop DJ. 2002. Expansion of human adult stem cells from bone marrow stroma: Conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 20(6):530-541.
40. Tsutsumi S, Shimazu A, Miyazaki K, Pan H, Koike C, Yoshida E, Takagishi K, Kato Y. 2001. Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Commun 288(2):413-419.
41. Valcourt U, Gouttenoire J, Aubert-Foucher E, Herbage D, Mallein-Gerin F. 2003. Alternative splicing of type II procollagen pre-mRNA in chondrocytes is oppositely regulated by BMP-2 and TGF-beta1. FEBS Lett 545(2-3):115-119.
42. Wall ME, Bernacki SH, Loboa EG. 2007. Effects of serial passaging on the adipogenic and osteogenic differentiation potential of adipose-derived human mesenchymal stem cells. Tissue Eng 13(6):1291-1298.
43. Wang DW, Fermor B, Gimble JM, Awad HA, Guilak F. 2005. Influence of oxygen on the proliferation and metabolism of adipose derived adult stem cells. J Cell Physiol 204(1):184-191.
44. Wickham MQ, Erickson GR, Gimble JM, Vail TP, Guilak F. 2003. Multipotent stromal cells derived from the infrapatellar fat pad of the knee. Clin Orthop Relat Res 412:196-212.
45. Winter A, Breit S, Parsch D, Benz K, Steck E, Hauner H, Weber RM, Ewerbeck V, Richter W. 2003. Cartilage-like gene expression in differentiated human stem cell spheroids: A comparison of bone marrow-derived and adipose tissue-derived stromal cells. Arthritis Rheum 48(2):418-429.
46. Yanada S, Ochi M, Kojima K, Sharman P, Yasunaga Y, Hiyama E. 2006. Possibility of selection of chondrogenic progenitor cells by telomere length in FGF-2-expanded mesenchymal stromal cells. Cell Prolif 39(6): 575-584.
47. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. 2001. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng 7(2):211-228.
48. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. 2002. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13(12):4279-4295.