Regenerating cartilages by engineered ASCs: Prolonged TGF-β3/BMP-6 expression improved articular cartilage formation and restored zonal structure

Molecular Therapy

Volumn 22, Issue 1, 2014, Pages 186-195

  Lu, Chia Hsin ^a   Yeh, Tsung Szu ^a,b   Yeh, Chia Lin ^a   Fang, Yu Hua Dean ^c   Sung, Li Yu ^a   Lin, Shih Yeh ^a   Yen, Tzu Chen ^c,d   Chang, Yu Han ^c,d   Hu, Yu Chen ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^d CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 6; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA3;

ADIPOSE DERIVED STEM CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; BACULOVIRUS; BONE DEVELOPMENT; BONE REGENERATION; BONE REMODELING; BONE STRUCTURE; CARTILAGE; CELL DENSITY; CELL DIFFERENTIATION; CELL ENGINEERING; CELL STRUCTURE; CELL VIABILITY; CHONDROGENESIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; GENETIC ENGINEERING; GENETIC RECOMBINATION; KNEE; MALE; MARKER GENE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PROTEIN EXPRESSION; RABBIT; RUNX2 GENE; SOX 9 GENE; TRANSGENE; UPREGULATION;

ORYCTOLAGUS CUNICULUS;

ADIPOSE TISSUE; ANIMALS; BIOMECHANICAL PHENOMENA; BONE MORPHOGENETIC PROTEIN 6; CARTILAGE; CHONDROGENESIS; GENE EXPRESSION; GENE ORDER; GENETIC VECTORS; GUIDED TISSUE REGENERATION; MALE; RABBITS; STEM CELLS; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TRANSDUCTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA3;

EID: 84891829635     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.165     Document Type: Article

References (49)

1. Vinatier, C, Mrugala, D, Jorgensen, C, Guicheux, J and Noël, D (2009). Cartilage engineering: A crucial combination of cells, biomaterials and biofactors. Trends Biotechnol 27: 307-314
2. Santo, VE, Gomes, ME, Mano, JF and Reis, RL (2013). Controlled release strategies for bone, cartilage, and osteochondral engineering-part I: Recapitulation of native tissue healing and variables for the design of delivery systems. Tissue Eng Part B Rev 19: 308-326
3. Cui, L, Wu, Y, Cen, L, Zhou, H, Yin, S, Liu, G et al. (2009). Repair of articular cartilage defect in non-weight bearing areas using adipose derived stem cells loaded polyglycolic acid mesh. Biomaterials 30: 2683-2693
4. Huey, DJ, Hu, JC and Athanasiou, KA (2012). Unlike bone, cartilage regeneration remains elusive. Science 338: 917-921
5. Vater, C, Kasten, P and Stiehler, M (2011). Culture media for the differentiation of mesenchymal stromal cells. Acta Biomater 7: 463-477
6. Pelttari, K, Winter, A, Steck, E, Goetzke, K, Hennig, T, Ochs, BG et al. (2006). 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
7. Mueller, MB and Tuan, RS (2008). Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum 58: 1377-1388
8. Puetzer, JL, Petitte, JN and Loboa, EG (2010). Comparative review of growth factors for induction of three-dimensional in vitro chondrogenesis in human mesenchymal stem cells isolated from bone marrow and adipose tissue. Tissue Eng Part B Rev 16: 435-444
9. Santo, VE, Gomes, ME, Mano, JF and Reis, RL (2013). Controlled release strategies for bone, cartilage, and osteochondral engineering-part II: Challenges on the evolution from single to multiple bioactive factor delivery. Tissue Eng Part B Rev. 19:327-352
10. Freyria, AM and Mallein-Gerin, F (2012). Chondrocytes or adult stem cells for cartilage repair: The indisputable role of growth factors. Injury 43: 259-265
11. Afizah, H, Yang, Z, Hui, JH, Ouyang, HW and Lee, EH (2007). A comparison between the chondrogenic potential of human bone marrow stem cells (BMSCs) and adiposederived stem cells (ADSCs) taken from the same donors. Tissue Eng 13: 659-666
12. Hennig, T, Lorenz, H, Thiel, A, Goetzke, K, Dickhut, A, Geiger, F et al. (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: 682-691
13. Cao, L, Yang, F, Liu, G, Yu, D, Li, H, Fan, Q et al. (2011). The promotion of cartilage defect repair using adenovirus mediated Sox9 gene transfer of rabbit bone marrow mesenchymal stem cells. Biomaterials 32: 3910-3920
14. Yang, HN, Park, JS, Woo, DG, Jeon, SY, Do, HJ, Lim, HY et al. (2011). Chondrogenesis of mesenchymal stem cells and dedifferentiated chondrocytes by transfection with SOX Trio genes. Biomaterials 32: 7695-7704
15. Gelse, K and Schneider, H (2006). Ex vivo gene therapy approaches to cartilage repair. Adv Drug Deliv Rev 58: 259-284
16. Airenne, KJ, Hu, YC, Kost, TA, Smith, RH, Kotin, RM, Ono, C et al. (2013). Baculovirus: An insect-derived vector for diverse gene transfer applications. Mol Ther 21: 739-749
17. Chen, CY, Lin, CY, Chen, GY and Hu, YC (2011). Baculovirus as a gene delivery vector: Recent understandings of molecular alterations in transduced cells and latest applications. Biotechnol Adv 29: 618-631
18. Lin, CY, Lu, CH, Luo, WY, Chang, YH, Sung, LY, Chiu, HY et al. (2010). Baculovirus as a gene delivery vector for cartilage and bone tissue engineering. Curr Gene Ther 10: 242-254
19. Chen, HC, Sung, LY, Lo, WH, Chuang, CK, Wang, YH, Lin, JL et al. (2008). Combination of baculovirus-expressed BMP-2 and rotating-shaft bioreactor culture synergistically enhances cartilage formation. Gene Ther 15: 309-317
20. Chen, HC, Chang, YH, Chuang, CK, Lin, CY, Sung, LY, Wang, YH et al. (2009). The repair of osteochondral defects using baculovirus-mediated gene transfer with dedifferentiated chondrocytes in bioreactor culture. Biomaterials 30: 674-681
21. Lu, CH, Lin, KJ, Chiu, HY, Chen, CY, Yen, TC, Hwang, SM et al. (2012). Improved chondrogenesis and engineered cartilage formation from TGF-ß3-expressing adiposederived stem cells cultured in the rotating-shaft bioreactor. Tissue Eng Part A 18: 2114-2124
22. Lo, WH, Hwang, SM, Chuang, CK, Chen, CY and Hu, YC (2009). Development of a hybrid baculoviral vector for sustained transgene expression. Mol Ther 17: 658-666
23. Lin, CY, Chang, YH, Kao, CY, Lu, CH, Sung, LY, Yen, TC et al. (2012). Augmented healing of critical-size calvarial defects by baculovirus-engineered MSCs that persistently express growth factors. Biomaterials 33: 3682-3692
24. Lin, CY, Lin, KJ, Kao, CY, Chen, MC, Lo, WH, Yen, TC et al. (2011). The role of adiposederived stem cells engineered with the persistently expressing hybrid baculovirus in the healing of massive bone defects. Biomaterials 32: 6505-6514
25. Sung, LY, Chen, CL, Lin, SY, Hwang, SM, Lu, CH, Li, KC et al. (2013). Enhanced and prolonged baculovirus-mediated expression by incorporating recombinase system and in cis elements: A comparative study. Nucleic Acids Res 41: E139
26. Diekman, BO, Rowland, CR, Lennon, DP, Caplan, AI and Guilak, F (2010). Chondrogenesis of adult stem cells from adipose tissue and bone marrow: Induction by growth factors and cartilage-derived matrix. Tissue Eng Part A 16: 523-533
27. Sekiya, I, Larson, BL, Vuoristo, JT, Reger, RL and Prockop, DJ (2005). Comparison of effect of BMP-2, -4, and -6 on in vitro cartilage formation of human adult stem cells from bone marrow stroma. Cell Tissue Res 320: 269-276
28. Fan, H, Tao, H, Wu, Y, Hu, Y, Yan, Y and Luo, Z (2010). TGF-ß3 immobilized PLGAgelatin/ chondroitin sulfate/hyaluronic acid hybrid scaffold for cartilage regeneration. J Biomed Mater Res A 95: 982-992
29. Mauck, RL, Yuan, X and Tuan, RS (2006). Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteoarthr Cartil 14: 179-189
30. Khan, IM, Gilbert, SJ, Singhrao, SK, Duance, VC and Archer, CW (2008). Cartilage integration: Evaluation of the reasons for failure of integration during cartilage repair. A review. Eur Cell Mater 16: 26-39
31. Lewis, PB, McCarty, LP 3rd, Kang, RW and Cole, BJ (2006). Basic science and treatment options for articular cartilage injuries. J Orthop Sports Phys Ther 36: 717-727
32. Sophia Fox, AJ, Bedi, A and Rodeo, SA (2009). The basic science of articular cartilage: Structure, composition, and function. Sports Health 1: 461-468
33. Gannon, AR, Nagel, T and Kelly, DJ (2012). The role of the superficial region in determining the dynamic properties of articular cartilage. Osteoarthr Cartil 20: 1417-1425
34. Mahmoudifar, N and Doran, PM (2012). Chondrogenesis and cartilage tissue engineering: The longer road to technology development. Trends Biotechnol 30: 166-176
35. Keeney, M, Lai, JH and Yang, F (2011). Recent progress in cartilage tissue engineering. Curr Opin Biotechnol 22: 734-740
36. Chen, ZY, Riu, E, He, CY, Xu, H and Kay, MA (2008). Silencing of episomal transgene expression in liver by plasmid bacterial backbone DNA is independent of CpG methylation. Mol Ther 16: 548-556
37. Gracey Maniar, LE, Maniar, JM, Chen, ZY, Lu, J, Fire, AZ and Kay, MA (2013). Minicircle DNA vectors achieve sustained expression reflected by active chromatin and transcriptional level. Mol Ther 21: 131-138
38. Dietz, WM, Skinner, NE, Hamilton, SE, Jund, MD, Heitfeld, SM, Litterman, AJ et al. (2013). Minicircle DNA is Superior to Plasmid DNA in Eliciting Antigen-specific CD8(+) T-cell Responses. Mol Ther 21: 1526-1535
39. Lu, J, Zhang, F and Kay, MA (2013). A mini-intronic plasmid (MIP): A novel robust transgene expression vector in vivo and in vitro. Mol Ther 21: 954-963
40. Chen, GY, Shiah, HC, Su, HJ, Chen, CY, Chuang, YJ, Lo, WH et al. (2009). Baculovirus transduction of mesenchymal stem cells triggers the toll-like receptor 3 pathway. J Virol 83: 10548-10556
41. Ho, YC, Lee, HP, Hwang, SM, Lo, WH, Chen, HC, Chung, CK et al. (2006). Baculovirus transduction of human mesenchymal stem cell-derived progenitor cells: Variation of transgene expression with cellular differentiation states. Gene Ther 13: 1471-1479
42. Chuang, CK, Wong, TH, Hwang, SM, Chang, YH, Chen, GY, Chiu, YC et al. (2009). Baculovirus transduction of mesenchymal stem cells: In vitro responses and in vivo immune responses after cell transplantation. Mol Ther 17: 889-896
43. Chen, CY, Wu, HH, Chen, CP, Chern, SR, Hwang, SM, Huang, SF et al. (2011). Biosafety assessment of human mesenchymal stem cells engineered by hybrid baculovirus vectors. Mol Pharm 8: 1505-1514
44. Lin, CY, Lin, KJ, Li, KC, Sung, LY, Hsueh, S, Lu, CH et al. (2012). Immune responses during healing of massive segmental femoral bone defects mediated by hybrid baculovirus-engineered ASCs. Biomaterials 33: 7422-7434
45. Raymond, CS and Soriano, P (2007). High-efficiency FLP and PhiC31 site-specific recombination in mammalian cells. PLoS ONE 2: E162
46. O'Reilly, D, Miller, L and Luckow, V (1992). Baculovirus Expression Vectors: A Laboratory Manual. W.H. Freeman and Co: New York
47. Chu, CR, Szczodry, M and Bruno, S (2010). Animal models for cartilage regeneration and repair. Tissue Eng Part B Rev 16: 105-115
48. Chang, CH, Kuo, TF, Lin, CC, Chou, CH, Chen, KH, Lin, FH et al. (2006). Tissue engineering-based cartilage repair with allogenous chondrocytes and gelatinchondroitin- hyaluronan tri-copolymer scaffold: A porcine model assessed at 18, 24, and 36 weeks. Biomaterials 27: 1876-1888
49. Ebihara, G, Sato, M, Yamato, M, Mitani, G, Kutsuna, T, Nagai, T et al. (2012). Cartilage repair in transplanted scaffold-free chondrocyte sheets using a minipig model. Biomaterials 33: 3846-3851