In vitro chondrogenesis of bone marrow-derived mesenchymal stem cells in a photopolymerizing hydrogel

Tissue Engineering

Volumn 9, Issue 4, 2003, Pages 679-688

  Williams, Christopher G ^a,b   Kim, Tae Kyun ^a,b   Taboas, Anya ^a   Malik, Athar ^a   Manson, Paul ^b   Elisseeff, Jennifer ^a  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECAN; COLLAGEN; COLLAGEN TYPE 2; GLYCOSAMINOGLYCAN; LINK PROTEIN; MACROGOL; RNA; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ARTICLE; BIOCHEMISTRY; BONE MARROW; CARTILAGE; CARTILAGE MATRIX; CELL CULTURE; CELL PROLIFERATION; CHONDROGENESIS; CONTROLLED STUDY; CULTURE MEDIUM; DRY WEIGHT; EXTRACELLULAR MATRIX; GENE EXPRESSION; GOAT; HISTOLOGY; HYDROGEL; IMMUNOHISTOCHEMISTRY; MESENCHYME CELL; MONOLAYER CULTURE; NONHUMAN; PHENOTYPE; PHOTOREACTIVITY; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; STEM CELL; TISSUE CULTURE; TISSUE ENGINEERING; UPREGULATION;

ANIMALS; BONE MARROW CELLS; CHONDROCYTES; CHONDROGENESIS; COLLAGEN; DNA; EXTRACELLULAR MATRIX PROTEINS; GLYCOSAMINOGLYCANS; GOATS; HYDROGELS; MESODERM; POLYETHYLENE GLYCOLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELLS; TISSUE ENGINEERING;

EID: 0041358606     PISSN: 10763279     EISSN: None     Source Type: Journal    
DOI: 10.1089/107632703768247377     Document Type: Article

References (45)

1. Mow, V.C., Radcliffe, A., and Poole, A.R. Review: Cartilage and diarthrodial joints as paradigms for hierarchical materials and structures. Biomaterials 13, 67, 1992.
2. Guo, J.F., Jourdian, G.W., and MacCallum, D.K. Culture and growth characteristics of chondrocytes encapsulated in alginate beads. Connect. Tissue Res. 19, 277, 1989.
3. Vacanti, C.A., Langer, R., Schloo, B., and Vacanti, J.P. Synthetic polymers seeded with chondrocytes provide a template for new cartilage formation. Plast. Reconstr. Surg. 88, 753, 1991.
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. Freed, L., and Vunjak-Novakovic, G. Tissue engineering of cartilage. In: Bronzind, J., ed. The Biomedical Engineering Handbook. Boca Raton, FL: CRC Press, 1995, pp. 1778-1796.
6. Elisseeff, J., Anseth, K., Sims, D., McIntosh, W., Randolph, M., Yaremchuk, M., and Langer, R. Transdermal photopolymerization of poly(ethylene oxide)-based injectable hydrogels for tissue-engineered cartilage. Plast. Reconstr. Surg. 104, 1014, 1999.
7. Bryant, S.J., Nuttleman, C.R., and Anseth, K.S. The effects of crosslinking density on cartilage formation in photocrosslinkable hydrogels. Biomed. Sci. Instrum. 35, 309, 1999.
8. Yang, W.D., Chen, S.J., Mao, T.Q., Chen, F.L., Lei, D.L., Tao, K., Tang, L.H., and Xiao, M.G. A study of injectable tissue-engineered autologous cartilage. Chin. J. Dent. Res. 3, 10, 2000.
9. Kim, H.A., Suh, D.I., and Song, Y.W. Relationship between chondrocyte apoptosis and matrix depletion in human articular cartilage. J. Rheumatol. 28, 2038, 2001.
10. Bonaventure, J., Kadhom, N., Cohen-Solal, L., Ng, K.H., Bourguignon, J., Lasselin, C., and Freisinger, P. Reexpression of cartilage-specific genes by dedifferentiated human articular chondrocytes cultured in alginate beads. Exp. Cell Res. 212, 97, 1994.
11. Saadeh, P.B., Brent, B., Mehrara, B.J., Steinbrech, D.S., Ting, V., Gittes, G.K., and Longaker, M.T. Human cartilage engineering: Chondrocyte extraction, proliferation, and: characterization for construct development. Ann. Plast. Surg. 42, 509, 1999.
12. Stewart, M.C., Saunders, K.M., Burton-Wurster, N., and Mcleod, J.N. Phenotypic stability of articular chondrocytes in vitro: The effects of culture models, bone morphogenetic protein 2, and serum supplementation. J. Bone Miner. Res. 15, 166, 2000.
13. Kim, T.K., Park, J.S., Lee, M.C., Seong, S.C., and Kim, H.J. Alternative splicing of type II procollagen gene in the dedifferentiation of rat epiphyseal chondrocytes serially cultured in monolayer. Connect. Tissue Res. 43, 56, 2002.
14. Colter, D.C., Sekiya, I., and Prockop, D.J. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc. Natl. Acad. Sci. U.S.A. 98, 7841, 2001.
15. Shake, J.G., Gruber, P.J., Baumgartner, W.A., Senechal, G., Meyers, J., Redmond, J.M., Pittenger, M.F., and Martin, B.J. Mesenchymal stem cell implantation in a swine myocardial infarct model: Engraftment and functional effects. Ann. Thorac. Surg. 73, 1919, 2002.
16. Jiang, Y., Jahagirdar, B.N., Reinhardt, R.L., Schwartz, R.E., Keene, C.D., Ortiz-Gonzalez, X.R., Reyes, M., Lenvik, T., Lund, T., Blackstad, M., Du, J., Aldrich, S., Lisberg, A., Low, W.C., Largaespada, D.A., and Verfaillie, C.M. Pluripotency of mesenchymal stem cells derived from adult marrow Nature 418, 41, 2002.
17. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S., and Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143, 1999.
18. Calvert, J.W., Marra, K.G., Cook, L., Kumta, P.N., DiMilla, P.A., and Weiss, L.E. Characterization of osteoblast-like behavior of cultured bone marrow stromal cells on various polymer surfaces. J. Biomed. Mater. Res. 52, 279, 2000.
19. Johnstone, B., Hering, T.M., Caplan, A.I., Goldberg, V.M., and Yoo, J.U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp. Cell Res. 238, 265, 1998.
20. 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.
21. Martin, I., Shastri, V.P., Padera, R.F., Yang, J., Mackay, A.J., Langer, R., Vunjak-Novakovic, G., and Freed, L.E. Selective differentiation of mammalian bone marrow stromal cells cultured on three-dimensional polymer foams. J. Biomed. Mater. Res. 55, 229, 2001.
22. Lanza, R.P., Langer, R., and Vacanti, J. Principles of Tissue Engineering, 2nd Ed. San Diego, CA: Academic Press, 2000.
23. Gao, J., Dennis, J.E., Solchaga, L.A., Awadallah, A.S., Goldberg, V.M., and Caplan, A.I. Tissue-engineered fabrication of an osteochondral composite graft using rat bone marrow-derived mesenchymal stem cells. Tissue Eng. 7, 363, 2001.
24. Rosen, V., Nove, J., Song, J.J., Thies, R.S., Cox, K., and Wozney, J.M. Responsiveness of clonal limb bud cell lines to bone morphogenetic protein 2 reveals a sequential relationship between cartilage and bone cell phenotypes, J. Bone Miner. Res. 9, 1759, 1994.
25. Majumdar, M.K., Wang, E., and Morris, E.A. BMP-2 and BMP-9 promotes chondrogenic differentiation of human multipotential mesenchymal cells and overcomes the inhibitory effect of IL-1. J. Cell. Physiol. 189, 275, 2001.
26. Sekiya, I., Colter, D.C., and Prockop, D.J. BMP-6 enhances chondrogenesis in a subpopulation of human marrow stromal cells. Biochem. Biophys. Res. Commun. 284, 411, 2001.
27. Alliston, T., and Derynck, R. Transforming growth factor-β in skeletal development and maintenance. In: Canalis, E., ed. Skeletal Growth Factors. Philadelphia, PA: Lippincott Williams & Wilkins, 2000, pp. 233-249.
28. Caterson, E.J., Li, W.J., Nesti, L.J., Albert, T., Danielson, K., and Tuan,_R.S. Polymer/alginate amalgam for cartilage-tissue engineering. Ann. N.Y. Acad. Sci. 961, 134, 2002.
29. 1 released from a biodegradable hydrogel. J. Control. Release 64, 133, 2000.
30. Caterson, E.J., Nesti, L.J., Li, W.J., Danielson, K.G., Albert, T.J., Vaccaro, A.R., and Tuan, R.S. Three-dimensional cartilage formation by bone marrow-derived cells seeded in polylactide/alginate amalgam. J. Biomed. Mater. Res. 57, 394, 2001.
31. Jen, A., Wake, M., and Mikos, A.G. Review: Hydrogels for cell immobilization. Biotechnol. Bioeng. 50, 357, 1996.
32. Peter, S.J., Miller, M.J., Yasko, A.W., Yaszemski, M.J., and Mikos, A.G. Polymer concepts in tissue engineering. J. Biomed. Mater. Res. 43, 422, 1998.
33. Hoffman, A.S. Hydrogels for biomedical applications. Adv. Drug Deliv. Rev. 54, 3, 2002.
34. Hennink, W.E., and van Nostrum, C.F. Novel crosslinking methods to design hydrogels. Adv. Drug Deliv. Rev. 54, 13, 2002.
35. Anseth, K.S., Metters, A.T., Brynt, S.J., Martens, P.J., Elisseeff, J.H., and Bowman, C.N. In situ forming degradable networks and their application in tissue engineering and drug delivery. J. Control. Release 78, 199, 2002.
36. Elisseeff, J., McIntosh, W., Anseth, K., Riley, S., Ragan, P., and Langer, R. Photoencapsulation of chondrocytes in poly(ethylene oxide)-based semi-interpenetrating networks. J. Biomed. Mater. Res. 51, 164, 2000.
37. Poshusta, A.K., and Anseth, K.S. Photopolymerized biomaterials for application in the temporomandibular joint. Cells Tissues Organs 169, 272, 2001.
38. Bryant, S.J., and Anseth, K.S. The effects of scaffold thickness on tissue engineered cartilage in photocrosslinked poly(ethylene oxide) hydrogels. Biomaterials 22, 619, 2001.
39. Bryant, S.J., and Anseth, K.S. Hydrogel properties influence ECM production by chondrocytes photoencapsulated in poly(ethylene glycol) hydrogels. J. Biomed. Mater. Res. 59, 63, 2002.
40. Kim, Y., Sah, R., Doong, J., and Grodzinsky, A.J. Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal. Biochem. 174, 168, 1988.
41. Farndale, R., Buttle, D., and Barrett, A. Improved quantitation and discrimination of sulphated glycosaminoglycans by the use of dimethylmethylene blue. Biochim. Biophys. Acta 883, 173, 1986.
42. Woessner, J.F. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch. Biochem. Biophys. 93, 440, 1961.
43. Benya, P.D., and Shaffer, J.D. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30, 215, 1982.
44. Diduch, D.R., Jordan, L.C., Mierisch, C.M., and Balian, G. Marrow stromal cells embedded in alginate for repair of osteochondral defects. Arthroscopy 16, 571, 2000.
45. Kavalkovich, K., Murphy, M., and Barry, F.P. Comparative chondrogenic activity of mesenchymal stem cells and articular chondrocytes. Presented at the 4th International Cartilage Repair Society Symposium, Toronto, Canada, June 15-18, 2002.