Human mesenchymal stem cells overexpressing therapeutic genes: From basic science to clinical applications for articular cartilage repair

Bio-Medical Materials and Engineering

Volumn 22, Issue 4, 2012, Pages 197-208

  Cucchiarini, Magali ^a   Venkatesan, Jagadeesh K ^a   Ekici, Myriam ^a   Schmitt, Gertrud ^a   Madry, Henning ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Articular cartilage repair; chondrogenic differentiation; gene transfer; mesenchymal stem cells

Indexed keywords

ARTICULAR CARTILAGE REPAIR; ARTICULAR CARTILAGES; BASIC SCIENCE; CHONDROGENIC DIFFERENTIATION; CLINICAL APPLICATION; GENETICALLY MODIFIED; HEALING PROCESS; HUMAN MESENCHYMAL STEM CELLS; LIMITED CAPACITY; MESENCHYMAL STEM CELL; NATIVE STRUCTURES; ORTHOPAEDIC SURGERY; PROGENITOR CELL; SELF REPAIR; THERAPEUTIC GENES; TRANSFER PROTOCOL;

CELL CULTURE; GENE TRANSFER; GENES; REPAIR; STEM CELLS; TISSUE;

CARTILAGE;

ANIMAL; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL DIFFERENTIATION; CHONDROGENESIS; CYTOLOGY; GENE TRANSFER; GROWTH, DEVELOPMENT AND AGING; HUMAN; INJURY; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; REVIEW;

ANIMALS; CARTILAGE, ARTICULAR; CELL DIFFERENTIATION; CHONDROCYTES; CHONDROGENESIS; GENE TRANSFER TECHNIQUES; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS;

EID: 84863933698     PISSN: 09592989     EISSN: None     Source Type: Journal    
DOI: 10.3233/BME-2012-0709     Document Type: Article

References (149)

1. J.A. Buckwalter and H.J. Mankin, Articular cartilage repair and transplantation, Arthritis Rheum. 41 (1998), 1331-1342. (Pubitemid 28373112)
2. A.J. Friedenstein, R.K. Chailakhja and K.S. Lalykina. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells, Cell. Tissue Kinet. 3 (1970), 393-403.
3. J.N. Beresford, Osteogenic stem cells and the stromal system of bone and marrow, Clin. Orthop. Relat. Res. 240 (1989), 270-280. (Pubitemid 19072149)
4. A.I. Caplan, Mesenchymal stem cells, J. Orthop. Res. 9 (1991), 641-650.
5. S.E. Haynesworth, J. Goshima, V.M. Goldberg and A.I. Caplan, Characterization of cells with osteogenic potential from human marrow, Bone 13 (1992), 81-88.
6. D.J. Prockop, Marrow stromal cells as stem cells for nonhematopoietic tissues, Science 276 (1997), 71-74. (Pubitemid 27161245)
7. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, J.D. Mosca, M.A. Moorman, D.W. Simonetti, S. Craig and D.R. Marshak, Multilineage potential of adult human mesenchymal stem cells, Science 284 (1999), 143-147. (Pubitemid 29282067)
8. F.P. Barry and J.M. Murphy, Mesenchymal stem cells: clinical applications and biological characterization, Int. J. Biochem. Cell Biol. 36 (2004), 568-584. (Pubitemid 38324589)
9. C. De Bari, F. Dell'Accio, P. Tylzanowski and F.P. Luyten, Multipotent mesenchymal stem cells from adult human synovial membrane, Arthritis Rheum. 44 (2001), 1928-1942. (Pubitemid 32758241)
10. R.J. Jankowski, B.M. Deasy and J. Huard, Muscle-derived stem cells, Gene Ther. 9 (2002), 642-647. (Pubitemid 34575318)
11. L.P. da Silva Meirelles, P.C. Chagastelles and N.B. Nardi, Mesenchymal stem cells reside in virtually all post-natal organs and tissues, J. Cell. Sci. 119 (2006), 2204-2213. (Pubitemid 43960310)
12. D.L. Troyer and M.L. Weiss, Wharton's jelly-derived cells are a primitive stromal cell population, Stem Cells 26 (2008), 591-599.
13. E.M. Horwitz, K. Le Blanc, M. Dominici, I. Mueller, I. Slaper-Cortenbach, F.C. Marini, R.J. Deans, D.S. Krause and A. Keating, Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement, Cytotherapy 7 (2005), 393-395. (Pubitemid 41671625)
14. M. Dominici, K. Le Blanc, I. Mueller, I. Slaper-Cortenbach, F. Marini, D. Krause, R. Deans, A. Keating, D. Prockop and E. Horwitz, Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement, Cytotherapy 8 (2006), 315-317. (Pubitemid 44269669)
15. C.M. Kolf, E. Cho and R.S. Tuan, Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation, Arthritis Res. Ther. 9 (2007), 204-213.
16. E.L. Fong, C.K. Chan and S.B. Goodman, Stem cell homing in musculoskeletal injury, Biomaterials 32 (2011), 395-409.
17. A.I. Caplan and J.E. Dennis, Mesenchymal stem cells as trophic mediators, J. Cell. Biochem. 98 (2006), 1076-1084. (Pubitemid 44128350)
18. S. Aggarwal andM.F. Pittenger, Human mesenchymal stem cells modulate allogeneic immune cell responses, Blood 105 (2005), 1815-1822. (Pubitemid 40223708)
19. A. Uccelli, V. Pistoia and L. Moretta,Mesenchymal stem cells: a new strategy for immunosuppression?, Trends Immunol. 28 (2007), 219-226. (Pubitemid 46667240)
20. N.G. Singer and A.I. Caplan, Mesenchymal stem cells: mechanisms of inflammation, Annu. Rev. Pathol. 6 (2011), 457-478.
21. K.W. Liechty, T.C.MacKenzie, A.F. Shaaban, A. Radu, A.M. Moseley, R. Deans, D.R. Marshak and A.W. Flake, Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep, Nat. Med. 6 (2000), 1282-1286.
22. A. Augello and C. De Bari, The regulation of differentiation in mesenchymal stem cells, Hum. Gene Ther. 21 (2010), 1226-1238.
23. B. Johnstone, T.M. Hering, A.I. Caplan, V.M. Goldberg and J.U. Yoo, In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells, Exp. Cell. Res. 238 (1998), 265-272. (Pubitemid 28366150)
24. A.M. Mackay, S.C. Beck, J.M. Murphy, F.P. Barry, C.O. Chichester and M.F. Pittenger, Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow, Tissue Eng. 4 (1998), 415-428. (Pubitemid 28553528)
25. J.U. Yoo, T.S. Barthel, K. Nishimura, L. Solchaga, A.I. Caplan, V.M. Goldberg and B. Johnstone, The chondrogenic potential of human bone-marrow-derived mesenchymal progenitor cells, J. Bone Joint Surg. Am. 80 (1998), 1745-1757. (Pubitemid 29013807)
26. S. Wakitani, T. Saito and A.I. Caplan, Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine, Muscle Nerve 18 (1995), 1417-1426.
27. H.A. Awad, D.L. Butler, G.P. Boivin, F.N. Smith, P. Malaviya, B. Huibregtse and A.I. Caplan, Autologous mesenchymal stem cell-mediated repair of tendon, Tissue Eng. 5 (1999), 267-277. (Pubitemid 29296109)
28. C. De Bari, F. Dell'Accio, F. Vandenabeele, J.R. Vermeesch, J.M. Raymackers and F.P. Luyten, Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane, J. Cell. Biol. 160 (2003), 909-918. (Pubitemid 36350845)
29. I.B. Black and D. Woodbury, Adult rat and human bone marrow stromal stem cells differentiate into neurons, Blood Cells Mol. Dis. 27 (2001), 632-636. (Pubitemid 32757058)
30. J.A. Buckwalter, V.C. Mow and A. Ratcliffe, Restoration of injured or degenerated articular cartilage, J. Am. Acad. Orthop. Surg. 2 (1994), 192-201.
31. A.I. Caplan, M. Elyaderani, Y. Mochizuki, S. Wakitani and V.M. Goldberg, Principles of cartilage repair and regeneration, Clin. Orthop. Relat. Res. 342 (1997), 254-269. (Pubitemid 27400825)
32. X. Chevalier, Intraarticular treatments for osteoarthritis: new perspectives, Curr. Drug Targets 11 (2010), 546-560.
33. P.D. Benya, S.R. Padilla andM.E. Nimni, The progeny of rabbit articular chondrocytes synthesize collagen types I and III and type I trimer, but not type II. Verifications by cyanogen bromide peptide analysis, Biochemistry 16 (1977), 865-872. (Pubitemid 8054868)
34. K. von der Mark, V. Gauss, H. von der Mark and P. Muller, Relationship between cell shape and type of collagen synthesised as chondrocytes lose their cartilage phenotype in culture, Nature 267 (1977), 531-532. (Pubitemid 8098481)
35. E.M. Horwitz, D.J. Prockop, L.A. Fitzpatrick, W.W. Koo, P.L. Gordon, M. Neel, M. Sussman, P. Orchard, J.C. Marx, R.E. Pyeritz and M.K. Brenner, Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta, Nat. Med. 5 (1999), 309-313. (Pubitemid 29124367)
36. E.M. Horwitz, D.J. Prockop, P.L. Gordon, W.W. Koo, L.A. Fitzpatrick, M.D. Neel, M.E. McCarville, P.J. Orchard, R.E. Pyeritz and M.K. Brenner, Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta, Blood 97 (2001), 1227-1231. (Pubitemid 32183743)
37. R. Quarto, M. Mastrogiacomo, R. Cancedda, S.M. Kutepov, V. Mukhachev, A. Lavroukov, E. Kon and M. Marcacci, Repair of large bone defects with the use of autologous bone marrow stromal cells, N. Engl. J. Med. 344 (2001), 385-386. (Pubitemid 32107654)
38. E.M. Horwitz, P.L. Gordon, W.K. Koo, J.C. Marx, M.D. Neel, R.Y. McNall, L. Muul and T. Hofmann, Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone, Proc. Natl. Acad. Sci. USA 99 (2002), 8932-8937. (Pubitemid 34693661)
39. S. Wakitani, K. Imoto, T. Yamamoto, M. Saito, N. Murata and M. Yoneda, Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees, Osteoarthritis Cartilage 10 (2002), 199-206. (Pubitemid 34189569)
40. H. Kitoh, T. Kitakoji, H. Tsuchiya, H. Mitsuyama, H. Nakamura, M. Katoh and N. Ishiguro, Transplantation of marrowderived mesenchymal stem cells and platelet-rich plasma during distraction osteogenesis-a preliminary result of three cases, Bone 35 (2004), 892-898. (Pubitemid 39349220)
41. K. Kawate, H. Yajima, H. Ohgushi, N. Kotobuki, K. Sugimoto, T. Ohmura, Y. Kobata, K. Shigematsu, K. Kawamura, K. Tamai and Y. Takakura, Tissue-engineered approach for the treatment of steroid-induced osteonecrosis of the femoral head: transplantation of autologous mesenchymal stem cells cultured with beta-tricalcium phosphate ceramics and free vascularized fibula, Artif. Organs 30 (2006), 960-962. (Pubitemid 44915585)
42. T. Morishita, K. Honoki, H. Ohgushi, N. Kotobuki, A. Matsushima and Y. Takakura, Tissue engineering approach to the treatment of bone tumors: three cases of cultured bone grafts derived from patients' mesenchymal stem cells, Artif. Organs 30 (2006), 115-118.
43. S. Tilley, B.J. Bolland, K. Partridge, A.M. New, J.M. Latham, D.G. Dunlop and R.O. Oreffo, Taking tissue-engineering principles into theater: augmentation of impacted allograft with human bone marrow stromal cells, Regen. Med. 1 (2006), 685-692.
44. S. Bajada, P.E. Harrison, B.A. Ashton, V.N. Cassar-Pullicino, N. Ashammakhi and J.B. Richardson, Successful treatment of refractory tibial nonunion using calcium sulphate and bone marrow stromal cell implantation, J. Bone Joint Surg. Br. 89 (2007), 1382-1386. (Pubitemid 350157325)
45. H. Filho Cerruti, I. Kerkis, A. Kerkis, N.H. Tatsui, A. da Costa Neves, D.F. Bueno and M.C. da Silva, Allogenous bone grafts improved by bone marrow stem cells and platelet growth factors: clinical case reports, Artif. Organs 31 (2007), 268-273. (Pubitemid 46587676)
46. R. Kuroda, K. Ishida, T. Matsumoto, T. Akisue, H. Fujioka, K. Mizuno, H. Ohgushi, S. Wakitani and M. Kurosaka, Treatment of a full-thickness articular cartilage defect in the femoral condyle of an athlete with autologous bone-marrow stromal cells, Osteoarthritis Cartilage 15 (2007), 226-231. (Pubitemid 46132105)
47. S. Wakitani, M. Nawata, K. Tensho, T. Okabe, H. Machida and H. Ohgushi, Repair of articular cartilage defects in the patello-femoral joint with autologous bone marrow mesenchymal cell transplantation: three case reports involving nine defects in five knees, J. Tissue Eng. Regen. Med. 1 (2007), 74-79.
48. C.J. Centeno, D. Busse, J. Kisiday, C. Keohan, M. Freeman and D. Karli, Increased knee cartilage volume in degenerative joint disease using percutaneously implanted, autologous mesenchymal stem cells, Pain Physician 11 (2008), 343-353. (Pubitemid 351959424)
49. C.J. Centeno, D. Busse, J. Kisiday, C. Keohan, M. Freeman and D. Karli, Regeneration of meniscus cartilage in a knee treated with percutaneously implanted autologous mesenchymal stem cells, Med. Hypotheses 71 (2008), 900-908.
50. Y. Gan, K. Dai, P. Zhang, T. Tang, Z. Zhu and J. Lu, The clinical use of enriched bone marrow stem cells combined with porous beta-tricalcium phosphate in posterior spinal fusion, Biomaterials 29 (2008), 3973-3982.
51. A.A. Kulakov, D.V. Goldshtein, A.S. Grigoryan, A.A. Rzhaninova, I.S. Alekseeva, I.V. Arutyunyan and A.V. Volkov, Clinical study of the efficiency of combined cell transplant on the basis of multipotent mesenchymal stromal adipose tissue cells in patients with pronounced deficit of the maxillary and mandibulary bone tissue, Bull. Exp. Biol. Med. 146 (2008), 522-525.
52. I. Muller, M. Vaegler, C. Holzwarth, N. Tzaribatchev, S.M. Pfister, B. Schutt, P. Reize, J. Greil, R. Handgretinger and M. Rudert, Secretion of angiogenic proteins by human multipotent mesenchymal stromal cells and their clinical potential in the treatment of avascular osteonecrosis, Leukemia 22 (2008), 2054-2061.
53. C. Hendrich, E. Franz, G. Waertel, R. Krebs and M. Jager, Safety of autologous bone marrow aspiration concentrate transplantation: initial experiences in 101 patients, Orthop. Rev. (Pavia) 1 (2009), e32-e36.
54. M. Jager, E.M. Jelinek, K.M. Wess, A. Scharfstadt, M. Jacobson, S.V. Kevy and R. Krauspe, Bone marrow concentrate: a novel strategy for bone defect treatment, Curr. Stem Cell Res. Ther. 4 (2009), 34-43.
55. K. Lee and S.B. Goodman, Cell therapy for secondary osteonecrosis of the femoral condyles using the Cellect DBM System: a preliminary report, J. Arthroplasty 24 (2009), 43-48.
56. S.M. Rush, G.A. Hamilton and L.M. Ackerson, Mesenchymal stem cell allograft in revision foot and ankle surgery: a clinical and radiographic analysis, J. Foot Ankle Surg. 48 (2009), 163-169.
57. A.M. Haleem, A.A. Singergy, D. Sabry, H.M. Atta, L.A. Rashed, C.R. Chu, M.T. El Shewy, A. Azzam and M.T. Abdel Aziz, The clinical use of human culture-expanded autologous bone marrow mesenchymal stem cells transplanted on platelet-rich fibrin glue in the treatment of articular cartilage defects: a pilot study and preliminary results, Cartilage 1 (2010), 253-261.
58. T. Yoshikawa, Y. Ueda, K. Miyazaki, M. Koizumi and Y. Takakura, Disc regeneration therapy using marrow mesenchymal cell transplantation: a report of two case studies, Spine 35 (1976), E475-E480.
59. F. Davatchi, B.S. Abdollahi, M. Mohyeddin, F. Shahram and B. Nikbin, Mesenchymal stem cell therapy for knee osteoarthritis. Preliminary report of four patients, Int. J. Rheum. Dis. 14 (2011), 211-215.
60. M. Jager, M. Herten, U. Fochtmann, J. Fischer, P. Hernigou, C. Zilkens, C. Hendrich and R. Krauspe, Bridging the gap: bone marrow aspiration concentrate reduces autologous bone grafting in osseous defects, J. Orthop. Res. 29 (2011), 173-180.
61. C. Kasemkijwattana, S. Hongeng, S. Kesprayura, V. Rungsinaporn, K. Chaipinyo and K. Chansiri, Autologous bone marrow mesenchymal stem cells implantation for cartilage defects: two cases report, J. Med. Assoc. Thai. 94 (2011), 395-400.
62. L. Orozco, R. Soler, C. Morera, M. Alberca, A. Sanchez and J. Garcia-Sancho, Intervertebral disc repair by autologous mesenchymal bone marrow cells: a pilot study, Transplantation 92(7) (2011), 822-828.
63. J. Pak, Regeneration of human bones in hip osteonecrosis and human cartilage in knee osteoarthritis with autologous adipose-tissue-derived stem cells: a case series, J. Med. Case Reports 5 (2011), 296-303.
64. S. Wakitani, T. Okabe, S. Horibe, T. Mitsuoka, M. Saito, T. Koyama, M. Nawata, K. Tensho, H. Kato, K. Uematsu, R. Kuroda, M. Kurosaka, S. Yoshiya, K. Hattori and H. Ohgushi, Safety of autologous bone marrow-derived mesenchymal stem cell transplantation for cartilage repair in 41 patients with 45 joints followed for up to 11 years and 5 months, J. Tissue Eng. Regen. Med. 5 (2011), 146-150.
65. G.F. Muschler, H. Nitto, C.A. Boehm and K.A. Easley, Age-and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors, J. Orthop. Res. 19 (2001), 117-125. (Pubitemid 32288644)
66. S.C. Mendes, J.M. Tibbe, M. Veenhof, K. Bakker, S. Both, P.P. Platenburg, F.C. Oner, J.D. de Bruijn and C.A. van Blitterswijk, Bone tissue-engineered implants using human bone marrow stromal cells: effect of culture conditions and donor age, Tissue Eng. 8 (2002), 911-920. (Pubitemid 35397237)
67. J.M. Murphy, K. Dixon, S. Beck, D. Fabian, A. Feldman and F. Barry, Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis, Arthritis Rheum. 46 (2002), 704-713. (Pubitemid 34218142)
68. K. Stenderup, J. Justesen, C. Clausen and M. Kassem, Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells, Bone 33 (2003), 919-926. (Pubitemid 37543568)
69. A.I. Caplan, Adult mesenchymal stem cells for tissue engineering versus regenerative medicine, J. Cell. Physiol. 213 (2007), 341-347. (Pubitemid 47509711)
70. P. Coipeau, P. Rosset, A. Langonne, J. Gaillard, B. Delorme, A. Rico, J. Domenech, P. Charbord and L. Sensebe, Impaired differentiation potential of human trabecular bone mesenchymal stromal cells from elderly patients, Cytotherapy 11 (2009), 584-594.
71. D.J. Prockop, Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms, Mol. Ther. 17 (2009), 939-946.
72. S. Roberts, P. Genever, A. McCaskie and C.D. Bari, Prospects of stem cell therapy in osteoarthritis, Regen. Med. 6 (2011), 351-366.
73. R.S. Tuan, Stemming cartilage degeneration: adult mesenchymal stem cells as a cell source for articular cartilage tissue engineering, Arthritis Rheum. 54 (2006), 3075-3078. (Pubitemid 44622075)
74. W. Richter, Cell-based cartilage repair: illusion or solution for osteoarthritis, Curr. Opin. Rheumatol. 19 (2007), 451-456. (Pubitemid 47344237)
75. A.F. Steinert, S.C. Ghivizzani, A. Rethwilm, R.S. Tuan, C.H. Evans and U. Noth,Major biological obstacles for persistent cell-based regeneration of articular cartilage, Arthritis Res. Ther. 9 (2007), 213-227.
76. M.B. Mueller and R.S. Tuan, Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells, Arthritis Rheum. 58 (2008), 1377-1388. (Pubitemid 351705927)
77. U. Noth, A.F. Steinert and R.S. Tuan, Technology insight: adult mesenchymal stem cells for osteoarthritis therapy, Nat. Clin. Pract. Rheumatol. 4 (2008), 371-380. (Pubitemid 351974009)
78. K. Pelttari, E. Steck and W. Richter, The use of mesenchymal stem cells for chondrogenesis, Injury 39(Suppl. 1) (2008), S58-S65.
79. C.M. Coleman, C. Curtin, F.P. Barry, C. O'Flatharta and J.M. Murphy, Mesenchymal stem cells and osteoarthritis: remedy or accomplice?, Hum. Gene Ther. 21 (2010), 1239-1250.
80. A.P. Hollander, S.C. Dickinson and W. Kafienah, Stem cells and cartilage development: complexities of a simple tissue, Stem Cells 28 (2010), 1992-1996.
81. C.H. Evans, S.C. Ghivizzani, P. Smith, F.D. Shuler, Z. Mi and P.D. Robbins, Using gene therapy to protect and restore cartilage, Clin. Orthop. Relat. Res. 379(Suppl.) (2000), S214-S219.
82. M. Cucchiarini and H. Madry, Gene therapy for cartilage defects, J. Gene Med. 7 (2005), 1495-1509. (Pubitemid 43025510)
83. C.J. Xian and B.K. Foster, Repair of injured articular and growth plate cartilage using mesenchymal stem cells and chondrogenic gene therapy, Curr. Stem Cell. Res. Ther. 1 (2006), 213-229.
84. M. Cucchiarini and H. Madry, Genetic modification of mesenchymal stem cells for cartilage repair, Biomed. Mater. Eng. 20 (2010), 135-143.
85. H. Madry and M. Cucchiarini, Clinical potential and challenges of using genetically modified cells for articular cartilage repair, Croat. Med. J. 52 (2011), 245-261.
86. C.H. Evans, S.C. Ghivizzani and P.D. Robbins, Orthopedic gene therapy in 2008, Mol. Ther. 17 (2009), 231-244.
87. J.A. Allay, J.E. Dennis, S.E. Haynesworth,M.K.Majumdar, D.W. Clapp, L.D. Shultz, A.I. Caplan and S.L. Gerson, LacZ and interleukin-3 expression in vivo after retroviral transduction of marrow-derived human osteogenic mesenchymal progenitors, Hum. Gene Ther. 8 (1997), 1417-1427. (Pubitemid 27393997)
88. J.M. Mason, D.A. Grande, M. Barcia, R. Grant, R.G. Pergolizzi and A.S. Breitbart, Expression of human bone morphogenic protein 7 in primary rabbit periosteal cells: potential utility in gene therapy for osteochondral repair, Gene Ther. 5 (1998), 1098-1104. (Pubitemid 28401312)
89. J.M. Mason, A.S. Breitbart, M. Barcia, D. Porti, R.G. Pergolizzi and D.A. Grande, Cartilage and bone regeneration using gene-enhanced tissue engineering, Clin. Orthop. Relat. Res. 379(Suppl.) (2000), S171-S178.
90. J.D. Mosca, J.K. Hendricks, D. Buyaner, J. Davis-Sproul, L.C. Chuang, M.K. Majumdar, R. Chopra, F. Barry, M. Murphy, M.A. Thiede, U. Junker, R.J. Rigg, S.P. Forestell, E. Bohnlein, R. Storb and B.M. Sandmaier, Mesenchymal stem cells as vehicles for gene delivery, Clin. Orthop. Relat. Res. 379(Suppl.) (2000), S71-S90.
91. A.J. Nixon, B.D. Brower-Toland, S.J. Bent, R.A. Saxer, M.J. Wilke, P.D. Robbins and C.H. Evans, Insulin-like growth factor-I gene therapy applications for cartilage repair, Clin. Orthop. Relat. Res. 379(Suppl.) (2000), S201-S213.
92. R.S. Goomer, L.J. Deftos, R. Terkeltaub, T. Maris, M.C. Lee, F.L. Harwood and D. Amiel, High-efficiency non-viral transfection of primary chondrocytes and perichondrial cells for ex-vivo gene therapy to repair articular cartilage defects, Osteoarthritis Cartilage 9 (2001), 248-256. (Pubitemid 32390207)
93. G. Turgeman, D.D. Pittman, R. Muller, B.G. Kurkalli, S. Zhou, G. Pelled, A. Peyser, Y. Zilberman, I.K. Moutsatsos and D. Gazit, Engineered human mesenchymal stem cells: a novel platform for skeletal cell mediated gene therapy, J. Gene Med. 3 (2001), 240-251. (Pubitemid 33684772)
94. N. Kobayashi, T. Koshino, M. Uesugi, N. Yokoo, K.Q. Xin, K. Okuda, H. Mizukami, K. Ozawa and T. Saito, Gene marking in adeno-associated virus vector infected periosteum derived cells for cartilage repair, J. Rheumatol. 29 (2002), 2176-2180.
95. K. Gelse, K. von der Mark, T. Aigner, J. Park and H. Schneider, Articular cartilage repair by gene therapy using growth factor-producing mesenchymal cells, Arthritis Rheum. 48 (2003), 430-441. (Pubitemid 36278012)
96. D.A. Grande, J. Mason, E. Light and D. Dines, Stem cells as platforms for delivery of genes to enhance cartilage repair, J. Bone Joint Surg. Am. 85A(Suppl. 2) (2003), 111-116. (Pubitemid 36535053)
97. T. Milbrandt, L. Berthoux, V. Christenson, C. Baumbusch, D. Rekosh, G. Balian and D. Diduch, Tracing transduced cells in osteochondral defects, J. Pediatr. Orthop. 23 (2003), 430-436. (Pubitemid 36760195)
98. J.M. Murphy, D.J. Fink, E.B. Hunziker and F.P. Barry, Stem cell therapy in a caprine model of osteoarthritis, Arthritis Rheum. 48 (2003), 3464-3474. (Pubitemid 37531912)
99. T. Ikeda, S. Kamekura, A. Mabuchi, I. Kou, S. Seki, T. Takato, K. Nakamura, H. Kawaguchi, S. Ikegawa and U.I. Chung, The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signals sufficient for induction of permanent cartilage, Arthritis Rheum. 50 (2004), 3561-3573. (Pubitemid 39488681)
100. H. Ito, J.J. Goater, P. Tiyapatanaputi, P.T. Rubery, R.J. O'Keefe and E.M. Schwarz, Light-activated gene transduction of recombinant adeno-associated virus in human mesenchymal stem cells, Gene Ther. 11 (2004), 34-41. (Pubitemid 38111386)
101. R. Katayama, S. Wakitani, N. Tsumaki, Y. Morita, I. Matsushita, R. Gejo and T. Kimura, Repair of articular artilage defects in rabbits using CDMP1 gene-transfected autologous mesenchymal cells derived from bone marrow, Rheumatology (Oxford) 43 (2004), 980-985. (Pubitemid 39144444)
102. A. Pascher, G.D. Palmer, A. Steinert, T. Oligino, E. Gouze, J.N. Gouze, O. Betz, M. Spector, P.D. Robbins, C.H. Evans and S.C. Ghivizzani, Gene delivery to cartilage defects using coagulated bone marrow aspirate, Gene Ther. 11 (2004), 133-141. (Pubitemid 38159685)
103. J. Hoelters, M. Ciccarella, M. Drechsel, C. Geissler, H. Gulkan, W. Bocker, M. Schieker, M. Jochum and P. Neth, Nonviral genetic modification mediates effective transgene expression and functional RNA interference in human mesenchymal stem cells, J. Gene Med. 7 (2005), 718-728. (Pubitemid 40872858)
104. G.D. Palmer, A. Steinert, A. Pascher, E. Gouze, J.N. Gouze, O. Betz, B. Johnstone, C.H. Evans and S.C. Ghivizzani, Gene-induced chondrogenesis of primary mesenchymal stem cells in vitro, Mol. Ther. 12 (2005), 219-228. (Pubitemid 41025091)
105. X. Guo, Q. Zheng, S. Yang, Z. Shao, Q. Yuan, Z. Pan, S. Tang, K. Liu and D. Quan, Repair of full-thickness articular cartilage defects by cultured mesenchymal stem cells transfected with the transforming growth factor beta1 gene, Biomed. Mater. 1 (2006), 206-215. (Pubitemid 46217612)
106. R. Kuroda, A. Usas, S. Kubo, K. Corsi, H. Peng, T. Rose, J. Cummins, F.H. Fu and J. Huard, Cartilage repair using bone morphogenetic protein 4 and muscle-derived stem cells, Arthritis Rheum. 54 (2006), 433-442. (Pubitemid 43228617)
107. J. Park, K. Gelse, S. Frank, K. von der Mark, T. Aigner and H. Schneider, Transgene-activated mesenchymal cells for articular cartilage repair: a comparison of primary bone marrow-, perichondrium/periosteum-and fat-derived cells, J. Gene Med. 8 (2006), 112-125. (Pubitemid 43169387)
108. X. Shao, J.C. Goh, D.W. Hutmacher, E.H. Lee and G. Zigang, Repair of large articular osteochondral defects using hybrid scaffolds and bone marrow-derived mesenchymal stem cells in a rabbit model, Tissue Eng. 12 (2006), 1539-1551. (Pubitemid 44174788)
109. A. Van Damme, L. Thorrez, L. Ma, H. Vandenburgh, J. Eyckmans, F. Dell'Accio, C. De Bari, F. Luyten, D. Lillicrap, D. Collen, T. VandenDriessche and M.K. Chuah, Efficient lentiviral transduction and improved engraftment of human bone marrow mesenchymal cells, Stem Cells 24 (2006), 896-907. (Pubitemid 44464723)
110. G. Zhou, W. Liu, L. Cui, X. Wang, T. Liu and Y. Cao, Repair of porcine articular osteochondral defects in nonweightbearing areas with autologous bone marrow stromal cells, Tissue Eng. 12 (2006), 3209-3221. (Pubitemid 44846425)
111. M.R. Pagnotto, Z. Wang, J.C. Karpie, M. Ferretti, X. Xiao and C.R. Chu, Adeno-associated viral gene transfer of transforming growth factor-beta1 to human mesenchymal stem cells improves cartilage repair, Gene Ther. 8 (2007), 804-813. (Pubitemid 46706060)
112. K. Gelse, C. Muhle, O. Franke, J. Park, M. Jehle, K. Durst, M. Goken, F. Hennig, K. von der Mark and H. Schneider, Cell-based resurfacing of large cartilage defects: long-term evaluation of grafts from autologous transgene-activated periosteal cells in a porcine model of osteoarthritis, Arthritis Rheum. 58 (2008), 475-488. (Pubitemid 351294882)
113. K. Gelse, C. Muhle, K. Knaup, B. Swoboda, M. Wiesener, F. Hennig, A. Olk and H. Schneider, Chondrogenic differentiation of growth factor-stimulated precursor cells in cartilage repair tissue is associated with increased HIF-1alpha activity, Osteoarthritis Cartilage 16 (2008), 1457-1465.
114. T. Matsumoto, S. Kubo, L.B. Meszaros, K.A. Corsi, G.M. Cooper, G. Li, A. Usas, A. Osawa, F.H. Fu and J. Huard, The influence of sex on the chondrogenic potential of muscle-derived stem cells: implications for cartilage regeneration and repair, Arthritis Rheum. 58 (2008), 3809-3819.
115. X. Zhang, Z. Zheng, P. Liu, Y. Ma, L. Lin, N. Lang, X. Fu, J. Zhang, K. Ma, P. Chen, C. Zhou and Y. Ao, The synergistic effects of microfracture, perforated decalcified cortical bone matrix and adenovirus-bone morphogenetic protein-4 in cartilage defect repair, Biomaterials 29 (2008), 4616-4629.
116. S. Elsler, S. Schetting, D. Kohn, M. Cucchiarini and H. Madry, Comparison and optimization of novel nonviral vectors for gene transfer in human bone marrow-derived mesenchymal stem cells, Trans. ORS 34 (2009), 1243.
117. S. Kubo, G.M. Cooper, T. Matsumoto, J.A. Phillippi, K.A. Corsi, A. Usas, G. Li, F.H. Fu and J. Huard, Blocking vascular endothelial growth factor with soluble Flt-1 improves the chondrogenic potential of mouse skeletal muscle-derived stem cells, Arthritis Rheum. 60 (2009), 155-165.
118. T. Matsumoto, G.M. Cooper, B. Gharaibeh, L.B. Meszaros, G. Li, A. Usas, F.H. Fu and J. Huard, Cartilage repair in a rat model of osteoarthritis through intraarticular transplantation of muscle-derived stem cells expressing bone morphogenetic protein 4 and soluble Flt-1, Arthritis Rheum. 60 (2009), 1390-1405.
119. B. Hu, J.L. Ren, J.R. Zhang, Q. Ma, Y.P. Liu and T.Q. Mao, Enhanced treatment of articular cartilage defect of the knee by intra-articular injection of Bcl-xL-engineered mesenchymal stem cells in rabbit model, J. Tissue Eng. Regen. Med. 4 (2010), 105-114.
120. A. Ivkovic, A. Pascher, D. Hudetz, D. Maticic, M. Jelic, S. Dickinson, M. Loparic, M. Haspl, R. Windhager and M. Pecina, Articular cartilage repair by genetically modified bone marrow aspirate in sheep, Gene Ther. 17 (2010), 779-789.
121. L. Cao, F. Yang, G. Liu, D. Yu, H. Li, Q. Fan, Y. Gan, T. Tang and K. Dai, The promotion of cartilage defect repair using adenovirus mediated SOX9 gene transfer of rabbit bone marrow mesenchymal stem cells, Biomaterials 32 (2011), 3910-3920.
122. M. Cucchiarini, M. Ekici, S. Schetting, D. Kohn and H. Madry, 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 17 (2011), 1921-1933.
123. P. Klinger, C. Surmann-Schmitt, M. Brem, B. Swoboda, J.H. Distler, H.D. Carl, K. von der Mark, F.F. Hennig and K. Gelse, Chondromodulin 1 stabilizes the chondrocyte phenotype and inhibits endochondral ossification of porcine cartilage repair tissue, Arthritis Rheum. 63 (2011), 2721-2731.
124. T.M. Liu, X.M. Guo, H.S. Tan, J.H. Hui, B. Lim and E.H. Lee, 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. 63 (2011), 2711-2720.
125. K. Kawamura, C.R. Chu, S. Sobajima, P.D. Robbins, F.H. Fu, N.J. Izzo and C. Niyibizi, Adenoviral-mediated transfer of TGF-beta1 but not IGF-1 induces chondrogenic differentiation of human mesenchymal stem cells in pellet cultures, Exp. Hematol. 33 (2005), 865-872. (Pubitemid 40982652)
126. X. Jin, Y. Sun, K. Zhang, J.Wang, T. Shi, X. Ju and S. Lou, Ectopic neocartilage formation from predifferentiated human adipose derived stem cells induced by adenoviral-mediated transfer of hTGF beta2, Biomaterials 28 (2007), 2994-3003. (Pubitemid 46560869)
127. J. Hao, Y. Yao, R.R. Varshney, L. Wang, C. Prakash, H. Li and D.A. Wang, Gene transfer and living release of transforming growth factor-beta3 for cartilage tissue engineering applications, Tissue Eng. Part C 14 (2008), 273-280.
128. X.B. Jin, Y.S. Sun, K. Zhang, J. Wang, T.P. Shi, X.D. Ju and S.Q. Lou, Tissue engineered cartilage from hTGF beta2 transduced human adipose derived stem cells seeded in PLGA/alginate compound in vitro and in vivo, J. Biomed. Mater. Res. A. 86 (2008), 1077-1087.
129. A.F. Steinert, G.D. Palmer, C. Pilapil, U. Noth, C.H. Evans and S.C. Ghivizzani, Enhanced in vitro chondrogenesis of primary mesenchymal stem cells by combined gene transfer, Tissue Eng. Part A 15 (2009), 1127-1139.
130. H.H. Lee, A.M. Haleem, V. Yao, J. Li, X. Xiao and C.R. Chu, Release of bioactive adeno-associated virus from fibrin scaffolds: effects of fibrin glue concentrations, Tissue Eng. Part A 17 (2011), 1969-1978.
131. A.F. Steinert, B. Proffen, M. Kunz, C. Hendrich, S.C. Ghivizzani, U. Noth, A. Rethwilm, J. Eulert and C.H. Evans, Hypertrophy is induced during the in vitro chondrogenic differentiation of human mesenchymal stem cells by bone morphogenetic protein-2 and bone morphogenetic protein-4 gene transfer, Arthritis Res. Ther. 11 (2009), R148-R162.
132. H. Tsuchiya, H. Kitoh, F. Sugiura and N. Ishiguro, Chondrogenesis enhanced by overexpression of SOX9 gene in mouse bone marrow-derived mesenchymal stem cells, Biochem. Biophys. Res. Commun. 301 (2003), 338-343. (Pubitemid 36279243)
133. L. Kupcsik, M.J. Stoddart, Z. Li, L.M. Benneker and M. Alini, Improving chondrogenesis: potential and limitations of SOX9 gene transfer and mechanical stimulation for cartilage tissue engineering, Tissue Eng. Part A 16 (2010), 1845-1855.
134. G.I. Im and H.J. Kim, Electroporation-mediated gene transfer of SOX trio to enhance chondrogenesis in adipose stem cells, Osteoarthritis Cartilage 19 (2011), 449-457.
135. J.H. Kim, J.S. Park, H.N. Yang, D.G.Woo, S.Y. Jeon, H.J. Do, H.Y. Lim, J.M. Kim and K.H. Park, The use of biodegradable PLGA nanoparticles to mediate SOX9 gene delivery in human mesenchymal stem cells (hMSCs) and induce chondrogenesis, Biomaterials 32 (2011), 268-278.
136. H.J. Kim and G.I. Im, Electroporation-mediated transfer of SOX trio genes (SOX-5, SOX-6, SOX-9) to enhance the chondrogenesis of mesenchymal stem cells, Stem Cells Dev. 20(12) (2011), 2103-2114.
137. J.L. Simonsen, C. Rosada, N. Serakinci, J. Justesen, K. Stenderup, S.I. Rattan, T.G. Jensen and M. Kassem, Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells, Nat. Biotechnol. 20 (2002), 592-596. (Pubitemid 34595153)
138. S.K. Kang, L. Putnam, J. Dufour, J. Ylostalo, J.S. Jung and B.A. Bunnell, Expression of telomerase extends the lifespan and enhances osteogenic differentiation of adipose tissue-derived stromal cells, Stem Cells 22 (2004), 1356-1372. (Pubitemid 39636411)
139. B.M. Abdallah, M. Haack-Sorensen, J.S. Burns, B. Elsnab, F. Jakob, P. Hokland and M. Kassem, Maintenance of differentiation potential of human bone marrow mesenchymal stem cells immortalized by human telomerase reverse transcriptase gene despite [corrected] extensive proliferation, Biochem. Biophys. Res. Commun. 326 (2005), 527-538. (Pubitemid 39642757)
140. W. Boker, Z. Yin, I. Drosse, F. Haasters, O. Rossmann, M. Wierer, C. Popov, M. Locher, W. Mutschler, D. Docheva and M. Schieker, Introducing a single-cell-derived human mesenchymal stem cell line expressing hTERT after lentiviral gene transfer, J. Cell. Mol. Med. 12 (2008), 1347-1359.
141. G. Huang, Q. Zheng, J. Sun, C. Guo, J. Yang, R. Chen, Y. Xu, G.Wang, D. Shen, Z. Pan, J. Jin and J.Wang, Stabilization of cellular properties and differentiation mutilpotential of human mesenchymal stem cells transduced with hTERT gene in a long-term culture, J. Cell. Biochem. 103 (2008), 1256-1269. (Pubitemid 351342614)
142. X. Zhang, N. Ziran, J.J. Goater, E.M. Schwarz, J.E. Puzas, R.N. Rosier, M. Zuscik, H. Drissi and R.J. O'Keefe, Primary murine limb bud mesenchymal cells in long-term culture complete chondrocyte differentiation: TGF-beta delays hypertrophy and PGE2 inhibits terminal differentiation, Bone 34 (2004), 809-817. (Pubitemid 38581126)
143. Y.J. Kim, H.J. Kim and G.I. Im, PTHrP promotes chondrogenesis and suppresses hypertrophy from both bone marrowderived and adipose tissue-derived MSCs, Biochem. Biophys. Res. Commun. 373 (2008), 104-108.
144. M. Pei, D. Chen, J. Li and L. Wei, Histone deacetylase 4 promotes TGF-beta1-induced synovium-derived stem cell chondrogenesis but inhibits chondrogenically differentiated stem cell hypertrophy, Differentiation 78 (2009), 260-268.
145. S. Yamashita, M. Andoh, H. Ueno-Kudoh, T. Sato, S. Miyaki and H. Asahara, SOX9 directly promotes Bapx1 gene expression to repress Runx2 in chondrocytes, Exp. Cell. Res. 315 (2009), 2231-2240.
146. M. Ekici, D. Kohn, H. Madry and M. Cucchiarini, Enhanced chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells following rAAV-mediated gene transfer, Trans. ORS 36 (2011), 1721.
147. T. Matsumoto, G.M. Cooper, B. Gharaibeh, L.B. Meszaros, G. Li, A. Usas, F.H. Fu and J. Huard, Blocking VEGF as a potential approach to improve cartilage healing after osteoarthritis, J. Musculoskelet. Neuronal Interact. 8 (2008), 316-317.
148. C.H. Evans, F.J. Liu, V. Glatt, J.A. Hoyland, C. Kirker-Head, A. Walsh, O. Betz, J.W. Wells, V. Betz, R.M. Porter, F.A. Saad, L.C. Gerstenfeld, T.A. Einhorn, M.B. Harris and M.S. Vrahas, Use of genetically modified muscle and fat grafts to repair defects in bone and cartilage, Eur. Cell. Mater. 18 (2009), 96-111.
149. S. Vogt, G. Wexel, T. Tischer, U. Schillinger, P. Ueblacker, B. Wagner, D. Hensler, J. Wilisch, C. Geis, D. Wubbenhorst, J. Aigner, M. Gerg, A. Kruger, G.M. Salzmann, V. Martinek, M. Anton, C. Plank, A.B. Imhoff and B. Gansbacher, The influence of the stable expression of BMP2 in fibrin clots on the remodelling and repair of osteochondral defects, Biomaterials 30 (2009), 2385-2392.