The effect of two- and three-dimensional cell culture on the chondrogenic potential of human adipose-derived mesenchymal stem cells after subcutaneous transplantation with an injectable hydrogel

Cell Transplantation

Volumn 20, Issue 10, 2011, Pages 1575-1588

  Merceron, Christophe ^a   Portron, Sophie ^a   Masson, Martial ^a   Lesoeur, Julie ^a   Fellah, Borhane Hakim ^a,b,c   Gauthier, Olivier ^a,b   Geffroy, Olivier ^a,b   Weiss, Pierre ^a   Guicheux, Jérôme ^a   Vinatier, Claire ^a,c  

^a UNIVERSITÉ DE NANTES   (France)

^b LUNAM UNIVERSITÉ   (France)

^c GRAFTYS   (France)

Author keywords

Cartilage; Chondrogenic differentiation; Human adipose derived stem cells (hATSCs); Hydrogel; Tissue engineering

Indexed keywords

PROTEIN;

ARTICLE; DROSOPHILA; PRIORITY JOURNAL;

MUS MUSCULUS;

EID: 84856073417     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368910X557191     Document Type: Article

References (56)

1. Aigner, T.; Stove, J. Collagens-major component of the physiological cartilage matrix, major target of cartilage degeneration, major tool in cartilage repair. Adv. Drug Deliv. Rev. 55:1569-1593; 2003.
2. Awad, H. A.; Wickham, M. Q.; Leddy, H. A.; Gimble, J. M.; Guilak, F. Chondrogenic differentiation of adiposederived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials 25:3211-3222; 2004.
3. Bai, X.; Sadat, S.; Gehmert, S.; Alt, E.; Song, Y. H. VEGF receptor Flk-1 plays an important role in c-kit expression in adipose tissue derived stem cells. FEBS Lett. 581:4681-4684; 2007.
4. Barry, F.; Boynton, R. E.; Liu, B.; Murphy, J. M. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: Differentiation-dependent gene expression of matrix components. Exp. Cell Res. 268:189-200; 2001.
5. Bennett, K. P.; Bergeron, C.; Acar, E.; Klees, R. F.; Vandenberg, S. L.; Yener, B.; Plopper, G. E. Proteomics reveals multiple routes to the osteogenic phenotype in mesenchymal stem cells. BMC Genomics 8:380-390; 2007.
6. Benoit, D. S.; Schwartz, M. P.; Durney, A. R.; Anseth, K. S. Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat. Mater. 7:816-823; 2008.
7. Bonaventure, J.; Kadhom, N.; Cohen-Solal, L.; Ng, K. H.; Bourguignon, J.; Lasselin, C.; Freisinger, P. Reexpression of cartilage-specific genes by dedifferentiated human articular chondrocytes cultured in alginate beads. Exp. Cell Res. 212:97-104; 1994.
8. Bourges, X.; Weiss, P.; Coudreuse, A.; Daculsi, G.; Legeay, G. General properties of silated hydroxyethylcellulose for potential biomedical applications. Biopolymers 63:232-238; 2002.
9. Bourges, X.; Weiss, P.; Daculsi, G.; Legeay, G. Synthesis and general properties of silated-hydroxypropyl methylcellulose in prospect of biomedical use. Adv. Colloid Interface Sci. 99:215-228; 2002.
10. Bouwmeester, S. J.; Beckers, J. M.; Kuijer, R.; van der Linden, A. J.; Bulstra, S. K. Long-term results of rib perichondrial grafts for repair of cartilage defects in the human knee. Int. Orthop. 21:313-317; 1997.
11. 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. 331:889-895; 1994.
12. Bunnell, B. A.; Estes, B. T.; Guilak, F.; Gimble, J. M. Differentiation of adipose stem cells. Methods Mol. Biol. 456:155-171; 2008.
13. Cancedda, R.; Dozin, B.; Giannoni, P.; Quarto, R. Tissue engineering and cell therapy of cartilage and bone. Matrix Biol. 22:81-91; 2003.
14. Chung, C.; Burdick, J. A. Engineering cartilage tissue. Adv. Drug Deliv. Rev. 60:243-262; 2008.
15. Dawson, E.; Mapili, G.; Erickson, K.; Taqvi, S.; Roy, K. Biomaterials for stem cell differentiation. Adv. Drug Deliv. Rev. 60:215-228; 2008.
16. Discher, D. E.; Mooney, D. J.; Zandstra, P. W. Growth factors, matrices, and forces combine and control stem cells. Science 324:1673-1677; 2009.
17. 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 8:315-317; 2006.
18. Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126:677-689; 2006.
19. Erickson, G. R.; Gimble, J. M.; Franklin, D. M.; Rice, H. E.; Awad, H.; Guilak, F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem. Biophys. Res. Commun. 290:763-769; 2002.
20. Estes, B. T.; Diekman, B. O.; Gimble, J. M.; Guilak, F. Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype. Nat. Protoc. 5:1294-1311; 2010.
21. Fatimi, F.; Tassin, J. F.; Quillard, S.; Axelos, M. A.; Weiss, P. The rheological properties of silated hydroxypropylmethylcellulose tissue engineering matrices. Biomaterials 29:533-543.
22. Gilbert, J. E. Current treatment options for the restoration of articular cartilage. Am. J. Knee Surg. 11:42-46; 1998.
23. Gimble, J. M.; Katz, A. J.; Bunnell, B. A. Adiposederived stem cells for regenerative medicine. Circ. Res. 100:1249-1260; 2007.
24. Hardingham, T. E.; Fosang, A. J.; Dudhia, J. The structure, function and turnover of aggrecan, the large aggregating proteoglycan from cartilage. Eur. J. Clin. Chem. Clin. Biochem. 32:249-257; 1994.
25. Hunziker, E. B. Articular cartilage repair: Basic science and clinical progress. A review of the current status and prospects. Osteoarthritis Cartilage 10:432-463; 2002.
26. Jin, X. B.; Sun, Y. S.; Zhang, K.; Wang, J.; Ju, X. D.; Lou, S. Q. Neocartilage formation from predifferentiated human adipose derived stem cells in vivo. Acta Pharmacol. Sin. 28:663-671; 2007.
27. Jin, X. B.; Sun, Y. S.; Zhang, K.; Wang, J.; Shi, T. P.; Ju, X. D.; Lou, S. Q. Tissue engineered cartilage from hTGF beta2 transduced human adipose derived stem cells seeded in PLGA/alginate compound in vitro and in vivo. J. Biomed. Mater. Res. A 86:1077-1087; 2008.
28. 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.
29. Jung, M.; Kaszap, B.; Redohl, A.; Steck, E.; Breusch, S.; Richter, W.; Gotterbarm, T. Enhanced early tissue regeneration after matrix-assisted autologous mesenchymal stem cell transplantation in full thickness chondral defects in a minipig model. Cell Transplant. 18:923-932; 2009.
30. Koulalis, D.; Schultz, W.; Heyden, M.; Konig, F. Autologous osteochondral grafts in the treatment of cartilage defects of the knee joint. Knee Surg. Sports Traumatol. Arthrosc. 12:329-334; 2004.
31. Lee, Y. A.; Kang, S. S.; Baek, S. H.; Jung, J. C.; Jin, E. J.; Tak, E. N.; Sonn, J. K. Redifferentiation of dedifferentiated chondrocytes on chitosan membranes and involvement of PKCalpha and P38 MAP kinase. Mol. Cells 24:9-15; 2007.
32. Markway, B. D.; Tan, G. K.; Brooke, G.; Hudson, J. E.; Cooper-White, J. J.; Doran, M. R. Enhanced chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in low oxygen environment micropellet cultures. Cell Transplant. 19:29-42; 2010.
33. Martin, I.; Shastri, V. P.; Padera, R. F.; Yang, J.; Mackay, A. J.; Langer, R.; Vunjak-Novakovic, G.; Freed, L. E. Selective differentiation of mammalian bone marrow stromal cells cultured on three-dimensional polymer foams. J. Biomed. Mater. Res. 55:229-235; 2001.
34. Martin-Hernandez, C.; Cebamanos-Celma, J.; MolinaRos, A.; Ballester-Jimenez, J. J.; Ballester-Soleda, J. Regenerated cartilage produced by autogenous periosteal grafts: A histologic and mechanical study in rabbits under the influence of continuous passive motion. Arthroscopy 26:76-83; 2010.
35. Merceron, C.; Vinatier, C.; Clouet, J.; Colliec-Jouault, S.; Weiss, P.; Guicheux, J. Adipose-derived mesenchymal stem cells and biomaterials for cartilage tissue engineering. Joint Bone Spine 75:672-674; 2008.
36. Merceron, C.; Vinatier, C.; Portron, S.; Masson, M.; Amiaud, J.; Guigand, L.; Cherel, Y.; Weiss, P.; Guicheux, J. Differential effects of hypoxia on osteochondrogenic potential of human adipose-derived stem cells. Am. J. Physiol. Cell Physiol. 298:355-364; 2010.
37. Mueller, M. B.; Tuan, R. S. Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum. 58:1377-1388; 2008.
38. O'Driscoll, S. W. The healing and regeneration of articular cartilage. J. Bone Joint Surg. Am. 80:1795-1812; 1998.
39. Pelttari, K.; Winter, A.; Steck, E.; Goetzke, K.; Hennig, T.; Ochs, B. G.; Aigner, T.; Richter, W. Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum. 54:3254-3266; 2006.
40. Pochampally, R. Colony forming unit assays for MSCs. Methods Mol. Biol. 449:83-91; 2008.
41. Prante, C.; Bieback, K.; Funke, C.; Schon, S.; Kern, S.; Kuhn, J.; Gastens, M.; Kleesiek, K.; Gotting, C. The formation of extracellular matrix during chondrogenic differentiation of mesenchymal stem cells correlates with increased levels of xylosyltransferase I. Stem Cells 24: 2252-2261; 2006.
42. Scotti, C.; Tonnarelli, B.; Papadimitropoulos, A.; Scherberich, A.; Schaeren, S.; Schauerte, A.; Lopez-Rios, J.; Zeller, R.; Barbero, A.; Martin, I. Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc. Natl. Acad. Sci. USA 107:7251-7256; 2010.
43. Sekiya, I.; Vuoristo, J. T.; Larson, B. L.; Prockop, D. J. In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc. Natl. Acad. Sci. USA 99:4397-4402; 2002.
44. Steinert, A. F.; Ghivizzani, S. C.; Rethwilm, A.; Tuan, R. S.; Evans, C. H.; Noth, U. Major biological obstacles for persistent cell-based regeneration of articular cartilage. Arthritis Res. Ther. 9:213-228; 2007.
45. Terraciano, V.; Hwang, N.; Moroni, L.; Park, H. B.; Zhang, Z.; Mizrahi, J.; Seliktar, D.; Elisseeff, J. Differential response of adult and embryonic mesenchymal progenitor cells to mechanical compression in hydrogels. Stem Cells 25:2730-2738; 2007.
46. Tremolada, C.; Palmieri, G.; Ricordi, C. Adipocyte transplantation and stem cells: Plastic surgery meets regenerative medicine. Cell Transplant. 19:1217-1223; 2010.
47. Vinatier, C.; Gauthier, O.; Fatimi, A.; Merceron, C.; Masson, M.; Moreau, A.; Moreau, F.; Fellah, B.; Weiss, P.; Guicheux, J. An injectable cellulose-based hydrogel for the transfer of autologous nasal chondrocytes in articular cartilage defects. Biotechnol. Bioeng. 102:1259-1267; 2009.
48. Vinatier, C.; Gauthier, O.; Masson, M.; Malard, O.; Moreau, A.; Fellah, B. H.; Bilban, M.; Spaethe, R.; Daculsi, G.; Guicheux, J. Nasal chondrocytes and fibrin sealant for cartilage tissue engineering. J. Biomed. Mater. Res. A 89:176-185; 2009.
49. Vinatier, C.; Magne, D.; Moreau, A.; Gauthier, O.; Malard, O.; Vignes-Colombeix, C.; Daculsi, G.; Weiss, P.; Guicheux, J. Engineering cartilage with human nasal chondrocytes and a silanized hydroxypropyl methylcellulose hydrogel. J. Biomed. Mater. Res. A 80:66-74; 2007.
50. Vinatier, C.; Magne, D.; Weiss, P.; Trojani, C.; Rochet, N.; Carle, G. F.; Vignes-Colombeix, C.; Chadjichristos, C.; Galera, P.; Daculsi, G.; Guicheux, J. A silanized hydroxypropyl methylcellulose hydrogel for the three-dimensional culture of chondrocytes. Biomaterials 26:6643-6651; 2005.
51. Vinatier, C.; Mrugala, D.; Jorgensen, C.; Guicheux, J.; Noel, D. Cartilage engineering: A crucial combination of cells, biomaterials and biofactors. Trends Biotechnol. 27: 307-314; 2009.
52. 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. 18: 159-170; 2009.
53. Weiss, S.; Hennig, T.; Bock, R.; Steck, E.; Richter, W. Impact of growth factors and PTHrP on early and late chondrogenic differentiation of human mesenchymal stem cells. J. Cell. Physiol. 223:84-93; 2010.
54. Winter, A.; Breit, S.; Parsch, D.; Benz, K.; Steck, E.; Hauner, H.; Weber, R. M.; 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. 48:418-429; 2003.
55. Zuk, P. A.; Zhu, M.; Ashjian, P.; De Ugarte, D. A.; Huang, J. I.; Mizuno, H.; Alfonso, Z. C.; Fraser, J. K.; Benhaim, P.; Hedrick, M. H. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 13:4279-4295; 2002.
56. Zuk, P. A.; Zhu, M.; Mizuno, H.; Huang, J.; Futrell, J. W.; Katz, A. J.; Benhaim, P.; Lorenz, H. P.; Hedrick, M. H. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng. 7:211-228; 2001.