Overexpression of human IGF-I via direct rAAV-mediated gene transfer improves the early repair of articular cartilage defects in vivo

Gene Therapy

Volumn 21, Issue 9, 2014, Pages 811-819

  Cucchiarini, M ^a   Madry, H ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; PARATHYROID HORMONE; RECOMBINANT SOMATOMEDIN C; TRANSCRIPTION FACTOR RUNX2; SOMATOMEDIN C;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ARTICULAR CARTILAGE; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA CONTENT; EXPERIMENTAL RABBIT; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; GENE TRANSFER; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; VIRAL GENE DELIVERY SYSTEM; ADMINISTRATION AND DOSAGE; ANIMAL; CARTILAGE CELL; CONGENITAL MALFORMATION; DEPENDOPARVOVIRUS; FEMALE; GENE THERAPY; GENE VECTOR; GENETICS; HEK293 CELL LINE; HUMAN; KNEE INJURIES; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; RABBIT; VIROLOGY; WOUND HEALING;

ADENO-ASSOCIATED VIRUS; ORYCTOLAGUS CUNICULUS;

ANIMALS; BETA CATENIN; CARTILAGE, ARTICULAR; CHONDROCYTES; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DEPENDOVIRUS; FEMALE; GENETIC THERAPY; GENETIC VECTORS; HEK293 CELLS; HUMANS; INSULIN-LIKE GROWTH FACTOR I; KNEE INJURIES; MESENCHYMAL STROMAL CELLS; RABBITS; WOUND HEALING;

EID: 84925382903     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2014.58     Document Type: Article

References (50)

1. Guo X, Zheng Q, Yang S, Shao Z, Yuan Q, Pan Z et al. Repair of full-thickness articular cartilage defects by cultured mesenchymal stem cells transfected with the transforming growth factor beta1 gene. Biomed Mater 2006; 1: 206-215.
2. Ivkovic A, Pascher A, Hudetz D, Maticic D, Jelic M, Dickinson L et al. Articular cartilage repair by genetically modified bone marrow aspirate in sheep. Gene Therapy 2010; 17: 779-789.
3. Pagnotto MR, Wang Z, Karpie JC, Ferretti M, Xiao X, Chu CR. Adeno-Associated viral gene transfer of transforming growth factor-beta1 to human mesenchymal stem cells improves cartilage repair. Gene Therapy 2007; 14: 804-813.
4. Evans CH, Liu FJ, Glatt V, Hoyland JA, Kirker-Head C, Walsh A et al. Use of genetically modified muscle and fat grafts to repair defects in bone and cartilage. Eur Cell Mater 2009; 18: 96-111.
5. Hidaka C, Goodrich LR, Chen CT, Warren RF, Crystal RG, Nixon AJ. Acceleration of cartilage repair by genetically modified chondrocytes over expressing bone morphogenetic protein-7. J Orthop Res 2003; 21: 573-583.
6. Kuroda R, Usas A, Kubo S, Corsi K, Peng H, Rose T et al. Cartilage repair using bone morphogenetic protein 4 and muscle-derived stem cells. Arthritis Rheum 2006; 54: 433-442.
7. Mason JM, Breitbart AS, Barcia M, Porti D, Pergolizzi RG, Grande DA. Cartilage and bone regeneration using gene-enhanced tissue engineering. Clin Orthop Relat Res 2000; 379 (Suppl): S171-S178.
8. Menendez MI, Clark DJ, Carlton M, Flanigan DC, Jia G, Sammet S et al. Direct delayed human adenoviral BMP-2 or BMP-6 gene therapy for bone and cartilage regeneration in a pony osteochondral model. Osteoarthritis Cartilage 2011; 19: 1066-1075.
9. Vogt S, Wexel G, Tischer T, Schillinger E, Ueblacker P, Wagner B et al. The influence of the stable expression of BMP2 in fibrin clots on the remodelling and repair of osteochondral defects. Biomaterials 2009; 30: 2385-2392.
10. Cucchiarini M, Madry H, Ma C, Thurn T, Zurakowski D, Menger MD et al. Improved tissue repair in articular cartilage defects in vivo by rAAV-mediated overexpression of human fibroblast growth factor 2. Mol Ther 2005; 12: 229-238.
11. Kaul G, Cucchiarini M, Arntzen D, Zurakowski D, Menger MD, Kohn D et al. Local stimulation of articular cartilage repair by transplantation of encapsulated chondrocytes overexpressing human fibroblast growth factor 2 (FGF-2) in vivo. J Gene Med 2006; 8: 100-111.
12. Zhu S, Zhang B, Man C, Ma Y, Liu X, Hu J. Combined effects of connective tissue growth factor-modified bone marrow-derived mesenchymal stem cells and NaOH-treated PLGA scaffolds on repair of articular cartilage defect in rabbits. Cell Transplant 2013; 23: 715-727.
13. Cao L, Yang F, Liu G, Yu D, Li H, Fan Q et al. The promotion of cartilage defect repair using adenovirus mediated Sox9 gene transfer of rabbit bone marrow mesenchymal stem cells. Biomaterials 2011; 32: 3910-3920.
14. Cucchiarini M, Orth P, Madry H. Direct rAAV SOX9 administration for durable articular cartilage repair with delayed terminal differentiation and hypertrophy in vivo. J Mol Med (Berl) 2013; 91: 625-636.
15. Lee JM, Im GI. SOX trio-co-transduced adipose stem cells in fibrin gel to enhance cartilage repair and delay the progression of osteoarthritis in the rat. Biomaterials 2012; 33: 2016-2024.
16. Liu TM, Guo XM, Tan HS, Hui JH, Lim B, Lee EH. Zinc-finger protein 145, acting as an upstream regulator of SOX9, improves the differentiation potential of human mesenchymal stem cells for cartilage regeneration and repair. Arthritis Rheum 2011; 63: 2711-2720.
17. Katayama R, Wakitani S, Tsumaki N, Morita Y, Matsushita I, Gejo R et al. Repair of articular cartilage defects in rabbits using CDMP1 gene-transfected autologous mesenchymal cells derived from bone marrow. Rheumatology 2004; 43: 980-985.
18. Klinger P, Surmann-Schmitt C, Brem M, Swoboda B, Distler JH, Carl HD et al. Chondromodulin 1 stabilizes the chondrocyte phenotype and inhibits endochondral ossification of porcine cartilage repair tissue. Arthritis Rheum 2011; 63: 2721-2731.
19. Fortier LA, Mohammed HO, Lust G, Nixon AJ. Insulin-like growth factor-I enhances cell-based repair of articular cartilage. J Bone Joint Surg Br 2002; 84: 276-288.
20. Holland TA, Bodde EW, Cuijpers VM, Baggett LS, Tabata Y, Mikos AG et al. Degradable hydrogel scaffolds for in vivo delivery of single and dual growth factors in cartilage repair. Osteoarthritis Cartilage 2007; 15: 187-197.
21. Kim K, Lam J, Lu S, Spicer PP, Lueckgen A, Tabata Y et al. Osteochondral tissue regeneration using a bilayered composite hydrogel with modulating dual growth factor release kinetics in a rabbit model. J Control Rel 2013; 168: 166-178.
22. Nixon AJ, Fortier LA, Williams J, Mohammed H. Enhanced repair of extensive articular defects by insulin-like growth factor-I-laden fibrin composites. J Orthop Res 1999; 17: 475-487.
23. Goodrich LR, Hidaka C, Robbins PD, Evans CH, Nixon AJ. Genetic modification of chondrocytes with insulin-like growth factor-1 enhances cartilage healing in an equine model. J Bone Joint Surg Br 2007; 89: 672-685.
24. Leng P, Ding CR, Zhang HN, Wang YZ. Reconstruct large osteochondral defects of the knee with hIGF-1 gene enhanced mosaicplasty. Knee 2012; 19: 804-811.
25. Madry H, Kaul G, Cucchiarini M, Stein U, Zurakowski D, Remberger K et al. Enhanced repair of articular cartilage defects in vivo by transplanted chondrocytes overexpressing insulin-like growth factor I (IGF-I). Gene Therapy 2005; 12: 1171-1179.
26. Madry H, Kaul G, Zurakowski D, Vunjak-Novakovic G, Cucchiarini M. Cartilage constructs engineered from chondrocytes overexpressing IGF-I improve the repair of osteochondral defects in a rabbit model. Eur Cell Mater 2013; 25: 229-247.
27. Cucchiarini M, Ekici M, Schetting S, Kohn D, Madry H. Metabolic activities and chondrogenic differentiation of human mesenchymal stem cells following recombinant adeno-Associated virus-mediated gene transfer and overexpression of fibroblast growth factor 2. Tissue Eng Part A 2011; 17: 1921-1933.
28. Venkatesan JK, Ekici M, Madry H, Schmitt G, Kohn D, Cucchiarini M. SOX9 gene transfer via safe, stable, replication-defective recombinant adeno-Associated virus vectors as a novel, powerful tool to enhance the chondrogenic potential of human mesenchymal stem cells. Stem Cell Res Ther 2012; 3: 22-36.
29. Venkatesan JK, Rey-Rico A, Schmitt G, Wezel A, Madry H, Cucchiarini M. rAAV-mediated overexpression of TGF-beta stably restructures human osteoarthritic articular cartilage in situ. J Transl Med 2013; 11: 211-224.
30. Weimer A, Madry H, Venkatesan JK, Schmitt G, Frisch J, Wezel A et al. Benefits of rAAV-mediated IGF-I overexpression for the long-term reconstruction of human osteoarthritic cartilage by modulation of the IGF-I axis. Mol Med 2012; 18: 346-358.
31. Sellers RS, Peluso D, Morris EA. The effect of recombinant human bone morphogenetic protein-2 (rhBMP-2) on the healing of full-thickness defects of articular cartilage. J Bone Joint Surg Am 1997; 79: 1452-1463.
32. Trippel SB, Corvol MT, Dumontier MF, Rappaport R, Hung HH, Mankin HJ. Effect of somatomedin-C/insulin-like growth factor I and growth hormone on cultured growth plate and articular chondrocytes. Pediatr Res 1989; 25: 76-82.
33. Kawamura K, Chu CR, Sobajima S, Robbins PD, Fu FH, Izzo NJ et al. Adenoviralmediated transfer of TGF-beta1 but not IGF-1 induces chondrogenic differentiation of human mesenchymal stem cells in pellet cultures. Exp Hematol 2005; 33: 865-872.
34. Palmer GD, Steinert A, Pascher A, Gouze E, Gouze JN, Betz O et al. Gene-induced chondrogenesis of primary mesenchymal stem cells in vitro. Mol Ther 2005; 12: 219-228.
35. Uebersax L, Merkle HP, Meinel L. Insulin-like growth factor I releasing silk fibroin scaffolds induce chondrogenic differentiation of human mesenchymal stem cells. J Control Rel 2008; 127: 12-21.
36. Govoni KE, Lee SK, Chung YS, Behringer RR, Wergedal JE, Baylink DJ et al. Disruption of insulin-like growth factor-I expression in type IIalphaI collagenexpressing cells reduces bone length and width in mice. Physiol Genom 2007; 30: 354-362.
37. Montaseri A, Busch F, Mobasheria A, Buhrmann C, Aldinger C, Rad JS et al. IGF-1 and PDGF-bb suppress IL-1beta-induced cartilage degradation through down-regulation of NF-kappaB signaling: involvement of Src/PI-3K/AKT pathway. PLoS One 2011; 6: e28663-e28677.
38. Renard E, Porée B, Chadjichristos C, Kypriotou M, Maneix L, Bigot N et al. Sox9/Sox6 and Sp1 are involved in the insulin-like growth factor-I-mediated upregulation of human type II collagen gene expression in articular chondrocytes. J Mol Med (Berl) 2012; 90: 649-666.
39. Seifarth C, Csaki C, Shakibaei M. Anabolic actions of IGF-I and TGF-beta1 on interleukin-1beta-treated human articular chondrocytes: evaluation in two and three dimensional cultures. Histol Histopathol 2009; 24: 1245-1262.
40. Shakibaei M, Seifarth C, John T, Rahmanzadeh M, Mobasheri A. IGF-I extends the chondrogenic potential of human articular chondrocytes in vitro: molecular association between Sox9 and Erk1/2. Biochem Pharmacol 2006; 72: 1382-1395.
41. Böhme K, Conscience-Egli M, Tschan T, Winterhalter KH, Bruckner P. Induction of proliferation or hypertrophy of chondrocytes in serum-free culture: the role of insulin-like growth factor-I, insulin, or thyroxine. J Cell Biol 1992; 116: 1035-1042.
42. Hie M, Iitsuka N, Otsuka T, Tsukamoto I. Insulin-dependent diabetes mellitus decreases osteoblastogenesis associated with the inhibition of Wnt signaling through increased expression of Sost and Dkk1 and inhibition of Akt activation. Int J Mol Med 2011; 28: 455-462.
43. Jiang J, Lichtler AC, Gronowicz GA, Adams DJ, Clark SH, Rosen CJ et al. Transgenic mice with osteoblast-targeted insulin-like growth factor-I show increased bone remodeling. Bone 2006; 39: 494-504.
44. Koch H, Jadlowiec JA, Campbell PG. Insulin-like growth factor-I induces early osteoblast gene expression in human mesenchymal stem cells. Stem Cells Dev 2005; 14: 621-631.
45. Zhao G, Monier-Faugere MC, Langub MC, Geng Z, Nakayama T, Pike JW et al. Targeted overexpression of insulin-like growth factor I to osteoblasts of transgenic mice: increased trabecular bone volume without increased osteoblast proliferation. Endocrinology 2000; 141: 2674-2682.
46. Richard-Parpaillon L, Heligon C, Chesnel F, Boujard D, Philpott A. The IGF pathway regulates head formation by inhibiting Wnt signaling in Xenopus. Dev Biol 2002; 244: 407-417.
47. Morisset S, Frisbie DD, Robbins PD, Nixon AJ, McIlwraith CW. IL-1ra/IGF-1 gene therapy modulates repair of microfractured chondral defects. Clin Orthop Relat Res 2007; 462: 221-228.
48. Cucchiarini M, Terwilliger EF, Kohn D, Madry H. Remodelling of human osteoarthritic cartilage by FGF-2, alone or combined with Sox9 via rAAV gene transfer. J Cell Mol Med 2009; 13: 2476-2488.
49. Samulski RJ, Chang LS, Shenk T. A recombinant plasmid from which an infectious adeno-Associated virus genome can be excised in vitro and its use to study viral replication. J Virol 1987; 61: 3096-3101.
50. Samulski RJ, Chang LS, Shenk T. Helper-free stocks of recombinant adenoassociated viruses: normal integration does not require viral gene expression. J Virol 1989; 63: 3822-3828.