GFOGER-modified MMP-sensitive polyethylene glycol hydrogels induce chondrogenic differentiation of human mesenchymal stem cells

Tissue Engineering - Part A

Volumn 20, Issue 7-8, 2014, Pages 1165-1174

  Mhanna, Rami ^a   Öztürk, Ece ^a   Vallmajo Martin, Queralt ^a   Millan, Christopher ^a   Müller, Michael ^a   Zenobi Wong, Marcy ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMIMETICS; COLLAGEN; CYTOLOGY; GENE EXPRESSION; HYDROGELS; MORPHOLOGY; PEPTIDES; POLYETHYLENE GLYCOLS; STEM CELLS;

CELLULAR MICROENVIRONMENT; CHONDROGENIC DIFFERENTIATION; EXTRACELLULAR MATRIX PROTEIN; FIBRONECTIN ADHESION PEPTIDES; HUMAN BONE MARROW MESENCHYMAL STEM CELLS; HUMAN MESENCHYMAL STEM CELLS; POLYETHYLENE GLYCOL (PEG); RECEPTOR-LIGAND BINDING;

GELS;

ALCIAN BLUE; ARGINYLGLYCYLASPARTIC ACID; COLLAGEN; COLLAGEN TYPE 2; INTEGRIN; MACROGOL; MATRIX METALLOPROTEINASE; PEPTIDE DERIVATIVE; SCLEROPROTEIN; AGGRECAN; ARGINYL-GLYCYL-ASPARTIC ACID; DNA; GLYCOSAMINOGLYCAN; HYDROGEL; MACROGOL DERIVATIVE; OLIGOPEPTIDE; PEPTIDE; PEPTIDE FRAGMENT;

AMINO ACID SEQUENCE; ARTICLE; BIODEGRADABILITY; CELL DIFFERENTIATION; CELL ENCAPSULATION; CELL FATE; CELL INTERACTION; CELL PROLIFERATION; CELL SPREADING; CELL STRUCTURE; CHONDROGENESIS; CONTROLLED STUDY; CYTOSKELETON; GENE EXPRESSION; HUMAN; HUMAN CELL; HYDROGEL; LIGAND BINDING; MESENCHYMAL STEM CELL; MICHAEL ADDITION; MICROENVIRONMENT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; CELL CULTURE; CELL SHAPE; CHEMISTRY; COMPRESSIVE STRENGTH; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; MOLECULAR GENETICS; PHARMACOLOGY; STAINING;

AGGRECANS; AMINO ACID SEQUENCE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SHAPE; CELLS, CULTURED; CHONDROGENESIS; COLLAGEN; COLLAGEN TYPE II; COMPRESSIVE STRENGTH; DNA; GENE EXPRESSION REGULATION; GLYCOSAMINOGLYCANS; HUMANS; HYDROGELS; MATRIX METALLOPROTEINASES; MESENCHYMAL STROMAL CELLS; MOLECULAR SEQUENCE DATA; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; PEPTIDES; POLYETHYLENE GLYCOLS; STAINING AND LABELING;

EID: 84898415623     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0519     Document Type: Article

References (56)

1. Becerra, J., Andrades, J.A., Guerado, E., Zamora-Navas, P., Lo'pez-Puertas, J.M., Reddi, and A.H. Articular cartilage: Structure and regeneration. Tissue Eng Part B Rev 16, 617, 2010
2. Grande, D.A., Southerland, S.S., Manji, R., Pate, D.W., Schwartz, R.E., and Lucas, P.A. Repair of articular cartilage defects using mesenchymal stem cells. Tissue Eng 1, 345, 1995
3. Chiang, H., and Jiang, C.C. Repair of articular cartilage defects: Review and perspectives. J Formos Med Assoc 108, 87, 2009
4. Brittberg, M., Lindahl, A., Nilsson, A., Ohlsson, C., Isaksson, O., and Peterson, L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 331, 889, 1994
5. Strauss, E.J., Fonseca, L.E., Shah, M.R., and Yorum, T. Management of focal cartilage defects in the knee-Is ACI the answer?. Bull NYU Hosp Jt Dis 69, 63, 2011
6. Johnstone, B., Hering, T.M., Caplan, A.I., Goldberg, V.M., andYoo, J.U. In vitro chondrogenesis of bonemarrow-derived mesenchymal progenitor cells. Exp Cell Res 238, 265, 1998
7. Sakaguchi, Y., Sekiya, I., Yagishita, K., and Muneta, T. Comparison of human stem cells derived from various mesenchymal tissues: Superiority of synovium as a cell source. Arthritis Rheum 52, 2521, 2005
8. Mackay, A.M., Beck, S.C., Murphy, J.M., Barry, F.P., Chichester, C.O., and Pittenger, M.F. Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 4, 415, 1998
9. De Bari, C., Dell'Accio, F., Tylzanowski, P., and Luyten, F.P. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 44, 1928, 2001
10. Erickson, G.R., Gimble, J.M., Franklin, D.M., Rice, H.E., Awad, H., and Guilak, F. Chondrogenic Potential of Adipose Tissue-Derived Stromal Cells in Vitro and in Vivo. Biochem Biophys Res Commun 290, 763, 2002
11. Awad, H.A., Quinn Wickham, M., Leddy, H.A., Gimble, J.M., and Guilak, F. Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials 25, 3211, 2004
12. Ma, H.-L., Hung, S.-C., Lin, S.-Y., Chen, Y.-L., and Lo, W.-H. Chondrogenesis of human mesenchymal stem cells encapsulated in alginate beads. J Biomed Mater Res Part A 64A, 273, 2003
13. Mauck, R.L., Yuan, X., and Tuan, R.S. Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-Term agarose culture. Osteoarthritis Cartilage 14, 179, 2006
14. Wang, Y., Kim, U.-J., Blasioli, D.J., Kim, H.-J., and Kaplan, D.L. In vitro cartilage tissue engineering with 3D porous aqueous-derived silk scaffolds and mesenchymal stem cells. Biomaterials 26, 7082, 2005
15. Cho, J.H., Kim, S.-H., Park, K.D., Jung, M.C., Yang, W.I., Han, S.W., et al. Chondrogenic differentiation of human mesenchymal stem cells using a thermosensitive poly(Nisopropylacrylamide) and water-soluble chitosan copolymer. Biomaterials 25, 5743, 2004
16. Hwang, N.S., Varghese, S., Zhang, Z., and Elisseeff, J. Chondrogenic differentiation of human embryonic stem cell-derived cells in arginine-glycine-Aspartate-modified hydrogels. Tissue Eng 12, 2695, 2006
17. Zhou, G., Liu, W., Cui, L., Wang, X., Liu, T., and Cao, Y. Repair of porcine articular osteochondral defects in nonweightbearing areas with autologous bone marrow stromal cells. Tissue Eng 12, 3209, 2006
18. Lutolf, M.P., and Hubbell, J.A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotech 23, 47, 2005
19. Varghese, S., Hwang, N.S., Canver, A.C., Theprungsirikul, P., Lin, D.W., and Elisseeff, J. Chondroitin sulfate based niches for chondrogenic differentiation of mesenchymal stem cells. Matrix Biol 27, 12, 2008
20. Williams, C.G., Kim, T.K., Taboas, A., Malik, A., Manson, P., and Elisseeff, J. In vitro chondrogenesis of bone marrow-derived mesenchymal stem cells in a photopolymerizing hydrogel. Tissue Eng 9, 679, 2003
21. McCall, J.D., Luoma, J.E., and Anseth, K.S. Covalently tethered transforming growth factor beta in PEG hydrogels promotes chondrogenic differentiation of encapsulated human mesenchymal stem cells. Drug Deliv Transl Res 2, 305, 2012
22. Lin, C.-C., and Anseth, K.S. Controlling affinity binding with peptide-functionalized poly(ethylene glycol) hydrogels. Adv Funct Mater 19, 2325, 2009
23. Zhu, J. Bioactive modification of poly(ethylene glycol) hydrogels for tissue engineering. Biomaterials 31, 4639, 2010
24. Lutolf, M.P., Lauer-Fields, J.L., Schmoekel, H.G., Metters, A.T., Weber, F.E., Fields, G.B., et al. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: Engineering cell-invasion characteristics. Proc Natl Acad Sci U S A 100, 5413, 2003
25. Park, Y., Lutolf, M.P., Hubbell, J.A., Hunziker, E.B., and Wong, M. Bovine primary chondrocyte culture in synthetic matrix metalloproteinase- sensitive poly(ethylene glycol)-based hydrogels as a scaffold for cartilage repair. Tissue Eng 10, 515, 2004
26. Hwang, N.S., Varghese, S., and Elisseeff, J. Controlled differentiation of stem cells. Adv Drug Deliv Rev 60, 199, 2008
27. Wilson, A., and Trumpp, A. Bone-marrow haematopoieticstem-cell niches. Nat Rev Immunol 6, 93, 2006
28. Benoit, D.S.W., Schwartz, M.P., Durney, A.R., and Anseth, K.S. Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat Mater 7, 816, 2008
29. Salinas, C.N., and Anseth, K.S. The influence of the RGD peptide motif and its contextual presentation in PEG gels on human mesenchymal stem cell viability. J Tissue Eng Regen Med 2, 296, 2008
30. Lin, Y.-C., Brayfield, C.A., Gerlach, J.C., Peter Rubin, J., and Marra, K.G. Peptide modification of polyethersulfone surfaces to improve adipose-derived stem cell adhesion. Acta Biomater 5, 1416, 2009
31. Liu, S.Q., Tian, Q., Wang, L., Hedrick, J.L., Hui, J.H.P., Yang, Y.Y., et al. Injectable biodegradable poly(ethylene glycol)/RGD peptide hybrid hydrogels for in vitro chondrogenesis of human mesenchymal stem cells. Macromol Rapid Commun 31, 1148, 2010
32. Salinas, C.N., and Anseth, K.S. The enhancement of chondrogenic differentiation of human mesenchymal stem cells by enzymatically regulated RGD functionalities. Biomaterials 29, 2370, 2008
33. Connelly, J.T., Garci'a, A.J., and Levenston, M.E. Inhibition of in vitro chondrogenesis in RGD-modified three-dimensional alginate gels. Biomaterials 28, 1071, 2007
34. Loeser, R.F. Integrins and cell signaling in chondrocytes. Biorheology 39, 119, 2002
35. Knight, C.G., Morton, L.F., Peachey, A.R., Tuckwell, D.S., Farndale, R.W., and Barnes, M.J. The Collagen-binding A-domains of Integrins a1b1 and a2b1recognize the same specific amino acid sequence, GFOGER, in native (Triplehelical) collagens. J Biol Chem 275, 35, 2000
36. Gigout, A., Jolicoeur, M., Nelea, M., Raynal, N., Farndale, R., and Buschmann, M.D. Chondrocyte aggregation in suspension culture is GFOGER-GPP- And b1 integrindependent. J Biol Chem 283, 31522, 2008
37. Chiu, L.-H., Chen, S.-C., Wu, K.-C., Yang, C.-B., Fang, C.-L., Lai, W.-F.T., et al. Differential effect of ECM molecules on re-expression of cartilaginous markers in near quiescent human chondrocytes. J Cell Physiol 226, 1981, 2011
38. Wojtowicz, A.M., Shekaran, A., Oest, M.E., Dupont, K.M., Templeman, K.L., Hutmacher, D.W., et al. Coating of biomaterial scaffolds with the collagen-mimetic peptide GFOGER for bone defect repair. Biomaterials 31, 2574, 2010
39. Raynor, J.E., Petrie, T.A., Garci'a, A.J., and Collard, D.M. Controlling cell adhesion to titanium: Functionalization of poly[oligo(ethylene glycol)methacrylate] brushes with celladhesive peptides. Adv Mater 19, 1724, 2007
40. Reyes, C.D., Petrie, T.A., Burns, K.L., Schwartz, Z., and Garci'a, A.J. Biomolecular surface coating to enhance orthopaedic tissue healing and integration. Biomaterials 28, 3228, 2007
41. Connelly, J., Petrie, T., Garci'a, A., and Levenston, M. Fibronectin-And collagen-mimetic ligands regulate bone marrow stromal cell chondrogenesis in three-dimensional hydrogels. Eur Cell Mater 22, 168, 2011
42. Liu, S.Q., Tian, Q., Hedrick, J.L., Po Hui, J.H., Rachel Ee, P.L., and Yang, Y.Y. Biomimetic hydrogels for chondrogenic differentiation of human mesenchymal stem cells to neocartilage. Biomaterials 31, 7298, 2010
43. Tsutsumi, S., Shimazu, A., Miyazaki, K., Pan, H., Koike, C., Yoshida, E., et al. Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Commun 288, 413, 2001
44. Studer, D., Lischer, S., Jochum, W., Ehrbar, M., Zenobi-Wong, M., and Maniura-Weber, K. Ribosomal protein L13a as a reference gene for human bone marrow-derived mesenchymal stromal cells during expansion, Adipo-, Chondro-, and Osteogenesis. Tissue Eng Part C Methods 18, 761, 2012
45. Livak, K.J., and Schmittgen, T.D. Analysis of relative gene expression data using real-Time quantitative PCR and the 2 - DDCT method. Methods 25, 402, 2001
46. Estes, B.T., Diekman, B.O., Gimble, J.M., and Guilak, F. Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype. Nat Protocols 5, 1294, 2010
47. Jongpaiboonkit, L., King, W.J., and Murphy, W.L. Screening for 3D environments that support human mesenchymal stem cell viability using hydrogel arrays. Tissue Eng Part A 15, 343, 2009
48. Nuttelman, C.R., Tripodi, M.C., and Anseth, K.S. Synthetic hydrogel niches that promote hMSC viability. Matrix Biol 24, 208, 2005
49. Von Der Mark, K., Gauss, V., Von Der Mark, H., and Muller, P. Relationship between cell shape and type of collagen synthesised as chondrocytes lose their cartilage phenotype in culture. Nature 267, 531, 1977
50. Benya, P.D., and Shaffer, J.D. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30, 215, 1982
51. DeLise, A.M., Fischer, L., and Tuan, R.S. Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage 8, 309, 2000
52. Gao, L., McBeath, R., and Chen, C.S. Stem cell shape regulates a chondrogenic versus myogenic fate through Rac1 and N-Cadherin. Stem Cells 28, 564, 2010
53. Connelly, J.T., Garci'a, A.J., and Levenston, M.E. Interactions between integrin ligand density and cytoskeletal integrity regulate BMSC chondrogenesis. J Cell Physiol 217, 145, 2008
54. Guilak, F., Cohen, D.M., Estes, B.T., Gimble, J.M., Liedtke, W., and Chen, C.S. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5, 17, 2009
55. Ingber, D.E. Tensegrity I. Cell structure and hierarchical systems biology. J Cell Sci 116, 1157, 2003
56. Ingber, D.E. Tensegrity II. How structural networks influence cellular information processing networks. J Cell Sci 116, 1397, 2003.