Enhanced in vitro chondrogenesis of primary mesenchymal stem cells by combined gene transfer

Tissue Engineering - Part A

Volumn 15, Issue 5, 2009, Pages 1127-1139

  Steinert, Andre F ^a,b   Palmer, Glyn D ^a   Pilapil, Carmencita ^a   Nöth, Ulrich ^b   Evans, Christopher H ^a   Ghivizzani, Steven C ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGLOMERATION; AGGREGATES; BIOACTIVITY; BONE; CARTILAGE; CELL CULTURE; CELLS; FLOWCHARTING; GENES; LIGAMENTS; PEPTIDES;

ADENOVIRAL VECTORS; AGGREGATE CULTURE; ARTICULAR CARTILAGES; BONE MARROW; BONE MORPHOGENETIC PROTEIN-2; CARTILAGE REPAIR; CELL-BASED; CELL-BASED THERAPY; CHONDROGENESIS; CHONDROGENIC; CHONDROGENIC DIFFERENTIATION; CO-EXPRESSION; DEFINED SERUM-FREE MEDIUM; GLYCOSAMINOGLYCAN; IN-VITRO; IN-VIVO; INSULIN-LIKE GROWTH FACTOR; LOW DOSE; MARKER GENES; MESENCHYMAL STEM CELL; MULTIPLE GENES; PROTEOGLYCANS; REGENERATION CAPACITY; TRANS-GENES; TRANSFORMING GROWTH FACTORS; TRANSGENE; TYPE II;

GENE TRANSFER;

ADENOVIRUS VECTOR; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN TYPE 2; GENE PRODUCT; GLYCOSAMINOGLYCAN; PROTEOGLYCAN; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL AGGREGATION; CELL CULTURE; CELL DIFFERENTIATION; CHONDROGENESIS; CONTROLLED STUDY; DNA MODIFICATION; DNA SYNTHESIS; GENE EXPRESSION; GENE TRANSFER; GLYCOSAMINOGLYCAN METABOLISM; IN VITRO STUDY; MARKER GENE; MESENCHYMAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRUS PARTICLE;

EID: 66249107073     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2007.0252     Document Type: Article

References (53)

1. Steinert, A.F., Ghivizzani, S.C., Rethwilm, A., Tuan, R.S., Evans, C.H., and Noth, U. Major biological obstacles for persistent cell-based regeneration of articular cartilage. Arthritis Res Ther. 9, 213, 2007.
2. Nesic, D., Whiteside, R., Brittberg, M., Wendt, D., Martin, I., and Mainil-Varlet, P. Cartilage tissue engineering for degenerative joint disease. Adv Drug Deliv Rev. 58, 300, 2006.
3. Kuo, C.K., Li, W.J., Mauck, R.L., and Tuan, R.S. Cartilage tissue engineering: its potential and uses. Curr Opin Rheumatol. 18, 64, 2006.
4. Mikos, A.G., Herring, S.W., Ochareon, P., Elisseeff, J., Lu, H.H., Kandel, R., Schoen, F.J., Toner, M., Mooney, D., Atala, A., Dyke, M.E., Kaplan, D., and Vunjak-Novakovic, G. Engineering complex tissues. Tissue Eng. 12, 3307, 2006.
5. 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.
6. Caplan, A.I., and Bruder, S.P. Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med. 7, 259, 2001.
7. Noth, U., Osyczka, A.M., Tuli, R., Hickok, N.J., Danielson, K.G., and Tuan, R.S. Multilineage mesenchymal differentiation potential of human trabecular bone-derived cells. J Orthop Res. 20, 1060, 2002.
8. Zuk, P.A., Zhu, M., Mizuno, H., Huang, J., Futrell, J.W., Katz, A.J., Benhaim, P., Lorenz, H.P., and Hedrick, M.H. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 7, 211, 2001.
9. Chen, F.H., Rousche, K.T., and Tuan, R.S. Technology Insight: adult stem cells in cartilage regeneration and tissue engineering. Nat Clin Pract Rheumatol. 2, 373, 2006.
10. Goldring, M.B., Tsuchimochi, K., and Ijiri, K. The control of chondrogenesis. J Cell Biochem. 97, 33, 2006.
11. Steinert, A., Weber, M., Dimmler, A., Julius, C., Schutze, N., Noth, U., Cramer, H., Eulert, J., Zimmermann, U., and Hendrich, C. Chondrogenic differentiation of mesenchymal progenitor cells encapsulated in ultrahigh-viscosity alginate. J Orthop Res. 21, 1090, 2003.
12. 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.
13. Nixon, A.J., Brower-Toland, B.D., Bent, S.J., Saxer, R.A., Wilke, M.J., Robbins, P.D., and Evans, C.H. Insulinlike growth factor-I gene therapy applications for cartilage repair. Clin Orthop Relat Res. 379, S201, 2000.
14. Worster, A.A., Brower-Toland, B.D., Fortier, L.A., Bent, S.J., Williams, J., and Nixon, A.J. Chondrocytic differentiation of mesenchymal stem cells sequentially exposed to transforming growth factor-beta1 in monolayer and insulin-like growth factor-I in a three-dimensional matrix. J Orthop Res. 19, 738, 2001.
15. 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.
16. Hanada, K., Solchaga, L.A., Caplan, A.I., Hering, T.M., Goldberg, V.M., Yoo, J.U., and Johnstone, B. BMP-2 induction and TGF-beta 1 modulation of rat periosteal cell chondrogenesis. J Cell Biochem. 81, 284, 2001.
17. Barry, F., Boynton, R.E., Liu, B., and Murphy, J.M. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation- dependent gene expression of matrix components. Exp Cell Res. 268, 189, 2001.
18. Noth, U., Rackwitz, L., Heymer, A., Weber, M., Baumann, B., Steinert, A., Schutze, N., Jakob, F., and Eulert, J. Chondrogenic differentiation of human mesenchymal stem cells in collagen type I hydrogels. J Biomed Mater Res A. 83, 626, 2007.
19. 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.
20. Hunziker, E.B. Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects. Osteoarthritis Cartilage. 10, 432, 2002.
21. Trippel, S.B., Ghivizzani, S.C., and Nixon, A.J. Gene-based approaches for the repair of articular cartilage. Gene Ther. 11, 351, 2004.
22. Evans, C.H., Robbins, P.D., Ghivizzani, S.C., Wasko, M.C., Tomaino, M.M., Kang, R., Muzzonigro, T.A., Vogt, M., Elder, E.M., Whiteside, T.L., Watkins, S.C., and Herndon, J.H. Gene transfer to human joints: progress toward a gene therapy of arthritis. Proc Natl Acad Sci U S A. 102, 8698, 2005.
23. Gelse, K., and Schneider, H. Ex vivo gene therapy approaches to cartilage repair. Adv Drug Deliv Rev. 58, 259, 2006.
24. Cucchiarini, M., and Madry, H. Gene therapy for cartilage defects. J Gene Med. 7, 1495, 2005.
25. Steinert, A.F., Nöth, U., and Tuan, R.S. Concepts in gene therapy for cartilage repair. Injury. 39S1, 97, 2008.
26. Palmer, G.D., Steinert, A.F., Pascher, A., Gouze, E., Gouze, J.N., Pilapil, C., Betz, O., Johnstone, B., Evans, C.H., and Ghivizzani, S.C. Gene-induced chondrogenesis of primary mesenchymal stem cells in vitro. Mol Therapy. 12, 219, 2005.
27. Steinert, A.F., Palmer, G.D., Capito, R., Hofstaetter, J.G., Pilapil, C., Ghivizzani, S.C., Spector, M., and Evans, C.H. Genetically enhanced engineering of meniscus tissue using ex vivo delivery of transforming growth factor-beta1 complementary deoxyribonucleic acid. Tissue Eng. 13, 2227, 2007.
28. Longobardi, L., O'Rear, L., Aakula, S., Johnstone, B., Shimer, K., Chytil, A., Horton, W.A., Moses, H.L., and Spagnoli, A. Effect of IGF-I in the chondrogenesis of bone marrow mesenchymal stem cells in the presence or absence of TGF-beta signaling. J Bone Miner Res. 21, 626, 2006.
29. Fukumoto, T., Sperling, J.W., Sanyal, A., Fitzsimmons, J.S., Reinholz, G.G., Conover, C.A., and O'Driscoll, S.W. Combined effects of insulin-like growth factor-1 and transforming growth factor-beta1 on periosteal mesenchymal cells during chondrogenesis in vitro. Osteoarthritis Cartilage. 11, 55, 2003.
30. Hardy, S., Kitamura, M., Harris-Stansil, T., Dai, Y., and Phipps, M.L. Construction of adenovirus vectors through Cre-lox recombination. J Virol. 71, 1842, 1997.
31. Palmer, G.D., Gouze, E., Gouze, J.N., Betz, O.B., Evans, C.H., and Ghivizzani, S.C. Gene transfer to articular chondrocytes with recombinant adenovirus. Methods Mol Biol. 215, 235, 2003.
32. Farndale, R.W., Sayers, C.A., and Barrett, A.J. A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures. Connect Tissue Res. 9, 247, 1982.
33. Chomczynski, P., and Sacchi, N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenolchloroform extraction. Anal Biochem. 162, 156, 1987.
34. Park, J., Gelse, K., Frank, S., von der Mark, K., Aigner, T., and Schneider, H. Transgene-activated mesenchymal cells for articular cartilage repair: a comparison of primary bone marrow-, perichondrium/periosteum-and fat-derived cells. J Gene Med. 8, 112, 2006.
35. Kawamura, K., Chu, C.R., Sobajima, S., Robbins, P.D., Fu, F.H., Izzo, N.J., and Niyibizi, C. Adenoviral-mediated transfer of TGF-beta1 but not IGF-1 induces chondrogenic differentiation of human mesenchymal stem cells in pellet cultures. Exp Hematol. 33, 865, 2005.
36. Gelse, K., von der Mark, K., Aigner, T., Park, J., and Schneider, H. Articular cartilage repair by gene therapy using growth factor-producing mesenchymal cells. Arthritis Rheum. 48, 430, 2003.
37. Madry, H., Kaul, G., Cucchiarini, M., Stein, U., Zurakowski, D., Remberger, K., Menger M.D., Kohn, D., and Trippel S.B. Enhanced repair of articular cartilage defects in vivo by transplanted chondrocytes overexpressing insulin-like growth factor I (IGF-I). Gene Ther. 15, 1171, 2005.
38. Pagnotto, M.R., Wang, Z., Karpie, J.C., Ferretti, M., Xiao, X., Chu, C.R. Adeno-associated viral gene transfer of transforming growth factor-beta1 to human mesenchymal stem cells improves cartilage repair. Gene Ther. 14, 804, 2007.
39. Mizuta, H., Sanyal, A., Fukumoto, T., Fitzsimmons, J.S., Matsui, N., Bolander, M.E., Oursler, M.J., and O'Driscoll, S.W. The spatiotemporal expression of TGF-beta1 and its receptors during periosteal chondrogenesis in vitro. J Orthop Res. 20, 562, 2002.
40. Nixon, A.J., Saxer, R.A., and Brower-Toland, B.D. Exogenous insulin-like growth factor-I stimulates an autoinductive IGF-I autocrine/paracrine response in chondrocytes. J Orthop Res. 19, 26, 2001.
41. Smith, P., Shuler, F.D., Georgescu, H.I., Ghivizzani, S.C., Johnstone, B., Niyibizi, C., Robbins, P.D., and Evans, C.H. Genetic enhancement of matrix synthesis by articular chondrocytes: comparison of different growth factor genes in the presence and absence of interleukin-1. Arthritis Rheum. 43, 1156, 2000.
42. Yaeger, P.C., Masi, T.L., de Ortiz, J.L., Binette, F., Tubo, R., and McPherson, J.M. Synergistic action of transforming growth factor-beta and insulin-like growth factor-I induces expression of type II collagen and aggrecan genes in adult human articular chondrocytes. Exp Cell Res. 237, 318, 1997.
43. van Osch, G.J., van den Berg, W.B., Hunziker, E.B., and Hauselmann, H.J. Differential effects of IGF-1 and TGF beta-2 on the assembly of proteoglycans in pericellular and territorial matrix by cultured bovine articular chondrocytes. Osteoarthritis Cartilage. 6, 187, 1998.
44. Indrawattana, N., Chen, G., Tadokoro, M., Shann, L.H., Ohgushi, H., Tateishi, T., Tanaka, J., and Bunyaratvej, A. Growth factor combination for chondrogenic induction from human mesenchymal stem cell. Biochem Biophys Res Commun. 320, 914, 2004.
45. Loeser, R.F., Pacione, C.A., and Chubinskaya, S. The combination of insulin-like growth factor 1 and osteogenic protein 1 promotes increased survival of and matrix synthesis by normal and osteoarthritic human articular chondrocytes. Arthritis Rheum. 48, 2188, 2003.
46. DeLise, A.M., Fischer, L., and Tuan, R.S. Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage. 8, 309, 2000.
47. Mwale, F., Stachura, D., Roughley, P., and Antoniou, J. Limitations of using aggrecan and type X collagen as markers of chondrogenesis in mesenchymal stem cell differentiation. J Orthop Res. 24, 1791, 2006.
48. Zachos, T., Diggs, A., Weisbrode, S., Bartlett, J., Bertone, A. Mesenchymal stem cell-mediated gene delivery of bone morphogenetic protein-2 in an articular fracture model. Mol Ther. 15, 1543, 2007.
49. Evans, C.H., Palmer, G.D., Pascher, A., Porter, R., Kwong, F.N., Gouze, E., Gouze, J.N., Liu, F., Steinert, A., Betz, O., Betz, V., Vrahas, M., and Ghivizzani, S.C. Facilitated endogenous repair: making tissue engineering simple, practical, and economical. Tissue Eng. 13, 1987, 2007.
50. Hunter, C.J., Imler, S.M., Malaviya, P., Nerem, R.M., and Levenston, M.E. Mechanical compression alters gene expression and extracellular matrix synthesis by chondrocytes cultured in collagen I gels. Biomaterials. 23, 1249, 2002.
51. Rees, S.G., Flannery, C.R., Little, C.B., Hughes, C.E., Caterson, B., and Dent, C.M. Catabolism of aggrecan, decorin and biglycan in tendon. Biochem J. 350, 181, 2000.
52. Gruber, R., Mayer, C., Bobacz, K., Krauth, M.T., Graninger, W., Luyten, F.P., and Erlacher, L. Effects of cartilage-derived morphogenetic proteins and osteogenic protein-1 on osteochondrogenic differentiation of periosteum-derived cells. Endocrinology. 142, 2087, 2001.
53. van Susante, J.L.C., Pieper, J., Buma, P., van Kuppevelt, T.H., van Beuningen, H., van Der Kraan, P.M., Veerkamp, J.H., van den Berg, W.B., and Veth, R.P.H. Linkage of chondroitin-sulfate to type I collagen scaffolds stimulates the bioactivity of seeded chondrocytes in vitro. Biomaterials. 22, 2359, 2001.