Regeneration potential and mechanism of bone marrow mesenchymal stem cell transplantation for treating intervertebral disc degeneration

Journal of Orthopaedic Science

Volumn 15, Issue 6, 2010, Pages 707-719

  Wang, Yun Tao ^a   Wu, Xiao Tao ^a   Wang, Feng ^a  

^a SOUTHEAST UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECAN; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN TYPE 1; COLLAGEN TYPE 2; CYCLIN DEPENDENT KINASE INHIBITOR 2A; ENDOTHELIAL GROWTH FACTOR; FAS ANTIGEN; FAS LIGAND; GROWTH FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OSTEOGENIC PROTEIN 1; PLATELET DERIVED GROWTH FACTOR; PROTEIN P21; PROTEIN P53; PROTEOGLYCAN; RETINOBLASTOMA PROTEIN; SMAD8 PROTEIN; SOMATOMEDIN C; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BRACHYURY; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ALLOGENEIC BONE MARROW DERIVED MESENCHYMAL STEM CELL TRANSPLANTATION; APOPTOSIS; AUTOLOGOUS BONE MARROW DERIVED MESENCHYMAL STEM CELL TRANSPLANTATION; BONE MARROW DERIVED MESENCHYMAL STEM CELL TRANSPLANTATION; CELL AGING; CELL CONTACT; CELL DIFFERENTIATION; CELL FUSION; CELL PROLIFERATION; CELL REGENERATION; CELL SENESCENCE; CELL VIABILITY; COCULTURE; EXTRACELLULAR MATRIX; GENE EXPRESSION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; INTERVERTEBRAL DISK DEGENERATION; LOW BACK PAIN; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROENVIRONMENT; NONHUMAN; NUCLEUS PULPOSUS; PROTEIN EXPRESSION; REVIEW;

EID: 78651081178     PISSN: 09492658     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00776-010-1536-3     Document Type: Review

References (111)

1. S.R. Pye D.M. Reid R. Smith J.E. Adams K. Nelson A.J. Silman, et al. 2004 Radiographic features of lumbar disc degeneration and self-reported back pain J Rheumatol 31 753 758 15088303
2. J.A. Hoyland C.L. Le Maitre A.J. Freemont 2008 Investigation of the role of IL-1 and TNF in matrix degradation in the intervertebral disc Rheumatology 47 809 814 1:CAS:528:DC%2BD1cXmtlent7w%3D 18397957 10.1093/rheumatology/ken056 (Pubitemid 351796365)
3. J.A. Miller C. Schmatz A.B. Schultz 1988 Lumbar disc degeneration: correlation with age, sex, and spine level in 600 autopsy specimens Spine 13 173 178 1:STN:280:DyaL1czgsFGguw%3D%3D 3406837 10.1097/00007632-198802000-00008
4. C.L. Le Maitre A.J. Freemont J.A. Hoyland 2004 Localization of degradative enzymes and their inhibitors in the degenerate human intervertebral disc J Pathol 204 47 54 15307137 10.1002/path.1608 1:CAS:528: DC%2BD2cXot1alsLY%3D (Pubitemid 39214481)
5. C.L. Le Maitre A.J. Freemont J.A. Hoyland 2007 Accelerated cellular senescence in degenerate intervertebral discs: a possible role in the pathogenesis of intervertebral disc degeneration Arthritis Res Ther 9 R45 17498290 10.1186/ar2198 1:CAS:528:DC%2BD2sXmsVOqt74%3D (Pubitemid 46852087)
6. S.M. Richardson R. Knowles J. Tyler A. Mobasheri J.A. Hoyland 2008 Expression of glucose transporters GLUT-1, GLUT-3, GLUT-9 and HIF-1α in normal and degenerate human intervertebral disc Histochem Cell Biol 129 503 511 1:CAS:528:DC%2BD1cXjsVClsbg%3D 18172662 10.1007/s00418-007-0372-9
7. C.Q. Zhao L.M. Wang L.S. Jiang L.Y. Dai 2007 The cell biology of intervertebral disc aging and degeneration Ageing Res Rev 6 247 261 17870673 10.1016/j.arr.2007.08.001 (Pubitemid 47405307)
8. K.W. Kim H.N. Chung K.Y. Ha J.S. Lee Y.Y. Kim 2009 Senescence mechanisms of nucleus pulposus chondrocytes in human intervertebral discs Spine J 9 658 666 19540815 10.1016/j.spinee.2009.04.018
9. S. Sobajima G. Vadala A. Shimer J.S. Kim L.G. Gilbertson J.D. Kang 2008 Feasibility of a stem cell therapy for intervertebral disc degeneration Spine J 8 888 896 18082460 10.1016/j.spinee.2007.09.011
10. T. Yasuma S. Koh T. Okamura Y. Yamauchi 1990 Histological changes in aging lumbar intervertebral discs: their role in protrusions and prolapses J Bone Joint Surg Am 72 220 229 1:STN:280:DyaK3c7lsVWntA%3D%3D 2303508
11. R.E. Thompson M.J. Pearcy K.J. Downing B.A. Manthey I.H. Parkinson N.L. Fazzalari 2000 Disc lesions and the mechanics of the intervertebral joint complex Spine 25 3026 3035 1:STN:280:DC%2BD3M7gsFKlsw%3D%3D 11145814 10.1097/00007632-200012010-00010
12. H.E. Gruber J.A. Ingram H.J. Norton E.N. Hanley 2007 Senescence in cells of the aging and degenerating intervertebral disc: immunolocalization of senescence-associated beta-galactosidase in human and sand rat discs Spine 32 321 327 17268263 10.1097/01.brs.0000253960.57051.de (Pubitemid 46197471)
13. S. Kaneyama K. Nishida T. Takada T. Suzuki T. Shimomura K. Maeno, et al. 2008 Fas ligand expression on human nucleus pulposus cells decreases with disc degeneration processes J Orthop Sci 13 130 135 1:CAS:528:DC%2BD1cXksVKkur4%3D 18392917 10.1007/s00776-007-1204-4 (Pubitemid 351502767)
14. B. Peng J. Hao S. Hou W. Wu D. Jiang X. Fu, et al. 2006 Possible pathogenesis of painful intervertebral disc degeneration Spine 31 560 566 16508552 10.1097/01.brs.0000201324.45537.46
15. S.M. Richardson R.V. Walker S. Parker N.P. Rhodes J.A. Hunt A.J. Freemont, et al. 2006 Intervertebral disc cell-mediated mesenchymal stem cell differentiation Stem Cells 24 707 716 1:CAS:528:DC%2BD28XhtFKitbfE 16223853 10.1634/stemcells.2005-0205 (Pubitemid 44464775)
16. S.T. Yoon N.M. Patel 2006 Molecular therapy of the intervertebral disc Eur Spine J 15 S379 S388 16835736 10.1007/s00586-006-0155-3 (Pubitemid 44371017)
17. Y. Zhang D. Markova H.J. Im W. Hu E.J. Thonar T.C. He, et al. 2009 Primary bovine intervertebral disc cells transduced with adenovirus overexpressing 12 BMPs and Sox9 maintain appropriate phenotype Am J Phys Med Rehabil 88 455 463 19454853 10.1097/PHM.0b013e3181a5f0aa
18. K. Masuda 2008 Biological repair of the degenerated intervertebral disc by the injection of growth factors Eur Spine J 17 441 451 19005698 10.1007/s00586-008-0749-z
19. K. Masuda H.S. An 2006 Prevention of disc degeneration with growth factors Eur Spine J 15 S422 S432 16865380 10.1007/s00586-006-0149-1 (Pubitemid 44376241)
20. D. Sakai J. Mochida T. Iwashina T. Watanabe T. Nakai K. Ando, et al. 2005 Differentiation of mesenchymal stem cells transplanted to a rabbit degenerative disc model: potential and limitations for stem cell therapy in disc regeneration Spine 30 2379 2387 16261113 10.1097/01.brs.0000184365.28481.e3 (Pubitemid 41567599)
21. S.U. Kuh Y. Zhu J. Li K.J. Tsai Q. Fei W.C. Hutton, et al. 2009 A comparison of three cell types as potential candidates for intervertebral disc therapy: annulus fibrosus cells, chondrocytes, and bone marrow derived cells Joint Bone Spine 76 70 74 1:CAS:528:DC%2BC3cXht1CltbbI 18955010 10.1016/j.jbspin.2008.02.021
22. M. Gorensek C. Jaksimovic N. Kregar-Velikonja M. Gorensek M. Knezevic M. Jeras, et al. 2004 Nucleus pulposus repair with cultured autologous elastic cartilage derived chondrocytes Cell Mol Biol Lett 9 363 373 15213815
23. K. Nishimura J. Mochida 1998 Percutaneous reinsertion of the nucleus pulposus: an experimental study Spine 23 1531 1539 1:STN:280: DyaK1czkslagsw%3D%3D 9682309 10.1097/00007632-199807150-00006 (Pubitemid 28459957)
24. T. Nomura J. Mochida M. Okuma K. Nishimura K. Sakabe 2001 Nucleus pulposus allograft retards intervertebral disc degeneration Clin Orthop 389 94 101 11501830 10.1097/00003086-200108000-00015
25. T. Iwashina J. Mochida D. Sakai Y. Yamamoto T. Miyazaki K. Ando, et al. 2006 Feasibility of using a human nucleus pulposus cell line as a cell source in cell transplantation therapy for intervertebral disc degeneration Spine 31 1177 1186 16688029 10.1097/01.brs.0000217687.36874.c4
26. D. Sakai J. Mochida Y. Yamamoto E. Toh T. Iwashina T. Miyazaki, et al. 2004 Immortalization of human nucleus pulposus cells by a recombinant SV40 adenovirus vector: establishment of a novel cell line for the study of human nucleus pulposus cells Spine 29 1515 1523 15247572 10.1097/01.BRS.0000131419. 25265.23 (Pubitemid 38943834)
27. H. Sheikh K. Zakharian R.P. De La Torre C. Facek A. Vasquez G.R. Chaudhry, et al. 2009 In vivo intervertebral disc regeneration using stem cell-derived chondroprogenitors J Neurosurg Spine 10 265 272 19320588 10.3171/2008.12.SPINE0835
28. H.J. Meisel V. Siodla T. Ganey Y. Minkus W.C. Hutton O.J. Alasevic 2007 Clinical experience in cell-based therapeutics: disc chondrocyte transplantation A treatment for degenerated or damaged intervertebral disc Biomol Eng 24 5 21 1:CAS:528:DC%2BD2sXhs1Cmur8%3D 16963315 10.1016/j.bioeng.2006.07.002 (Pubitemid 46216157)
29. H.J. Meisel T. Ganey W.C. Hutton J. Libera Y. Minkus O. Alasevic 2006 Clinical experience in cell-based therapeutics: intervention and outcome Eur Spine J 15 S397 405 16850291 10.1007/s00586-006-0169-x (Pubitemid 44371019)
30. C. Hohaus T.M. Ganey Y. Minkus H.J. Meisel 2008 Cell transplantation in lumbar spine disc degeneration disease Eur Spine J 17 492 503 19005697 10.1007/s00586-008-0750-6
31. D.G. Anderson M.V. Risbud I.M. Shapiro A.R. Vaccaro T.J. Albert 2005 Cell-based therapy for disc repair Spine J 5 297S 303S 16291126 10.1016/j.spinee.2005.02.019 (Pubitemid 41700074)
32. A. Bartholomew C. Sturgeon M. Siatskas K. Ferrer K. Mclntosh S. Patil, et al. 2002 Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo Exp Hematol 30 42 48 11823036 10.1016/S0301-472X(01)00769-X (Pubitemid 34059216)
33. D. Sakai J. Mochida Y. Yamamoto T. Nomura M. Okuma K. Nishimura, et al. 2003 Transplantation of mesenchymal stem cells embedded in Atelocollagen gel to the intervertebral disc: a potential therapeutic model for disc degeneration Biomaterials 24 3531 3541 1:CAS:528:DC%2BD3sXktlOgtL0%3D 12809782 10.1016/S0142-9612(03)00222-9 (Pubitemid 36703127)
34. E.M. Horwitz D.J. Prockop L.A. Fitzpatrick W.W.K. Koo P.L. Gordon M. Neel, et al. 1999 Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta Nat Med 5 309 313 1:CAS:528:DyaK1MXhsVSltLk%3D 10086387 10.1038/6529 (Pubitemid 29124367)
35. K. Le Blanc C. Tammik K. Rosendahl E. Zetterberg O. Ringden 2003 HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells Exp Hematol 31 890 896 14550804 10.1016/S0301-472X(03) 00110-3 1:CAS:528:DC%2BD3sXnvVOlsrk%3D (Pubitemid 37211373)
36. V.Y. Leung D. Chan K.M. Cheung 2006 Regeneration of intervertebral disc by mesenchymal stem cells: potentials, limitations, and future direction Eur Spine J 15 S406 S413 16845553 10.1007/s00586-006-0183-z (Pubitemid 44371020)
37. R.J.W. Hoogendoorn Z.F. Lu R.J. Kroeze R.A. Bank P.I. Wuisman M.N. Helder 2008 Adipose stem cells for intervertebral disc regeneration: current status and concepts for the future J Cell Mol Med 12 2205 2216 1:CAS:528: DC%2BD1MXht1WhtLs%3D 18298653 10.1111/j.1582-4934.2008.00291.x
38. J.J. Jim N. Noponen-Hietala K.M. Cheung J. Ott J. Karppinen A. Sahraravand, et al. 2005 The TRP2 allele of COL9A2 is an age-dependent risk factor for the development and severity of intervertebral disc degeneration Spine 30 2735 2742 16371896 10.1097/01.brs.0000190828.85331.ef (Pubitemid 43011033)
39. N. Noponen-Hietala I. Virtanen R. Karttunen S. Schwenke E. Jakkula H. Li, et al. 2005 Genetic variations in IL6 associate with intervertebral disc disease characterized by sciatica Pain 114 186 194 1:CAS:528: DC%2BD2MXhslCitL8%3D 15733644 10.1016/j.pain.2004.12.015 (Pubitemid 40279100)
40. K. Semba K. Araki Z. Li K. Matsumoto M. Suzuki N. Nakagata, et al. 2006 A novel murine gene, sickle tail, linked to the Danforth's short tail locus, is required for normal development of the intervertebral disc Genetics 172 445 456 1:CAS:528:DC%2BD28XhvV2jsbs%3D 16204209 10.1534/genetics.105.048934 (Pubitemid 43345505)
41. S. Sethe A. Scutt A. Stolzing 2006 Aging of mesenchymal stem cells Ageing Res Rev 5 91 116 1:CAS:528:DC%2BD28Xis1yisLw%3D 16310414 10.1016/j.arr.2005.10. 001 (Pubitemid 43139669)
42. I. Bellantuono A. Aldahmash M. Kassem 2009 Aging of marrow stromal (skeletal) stem cells and their contribution to age-related bone loss Biochim Biophys Acta 1792 364 370 1:CAS:528:DC%2BD1MXksVaqsbg%3D 19419706
43. J.M. Ryan F.P. Barry J.M. Murphy B.P. Mahon 2005 Mesenchymal stem cells avoid allogeneic rejection J Inflamm (Lond) 2 8 10.1186/1476-9255-2-8 1:CAS:528:DC%2BD2MXntFGht7c%3D (Pubitemid 41364607)
44. P. Gaetani M.L. Torre M. Klinger M. Faustini F. Crovato M. Bucco, et al. 2008 Adipose-derived stem cell therapy for Intervertebral disc regeneration: an in vitro reconstructed tissue in alginate capsules Tissue Eng Part A 14 1415 1423 1:CAS:528:DC%2BD1cXpsFKrtbs%3D 18593270 10.1089/ten.tea.2007.0330
45. T. Ganey W.C. Hutton T. Moseley M. Hedrick H. Meisel 2009 Intervertebral disc repair using adipose tissue-derived stem and regenerative cells: experiments in a canine model Spine 34 2297 2304 19934809 10.1097/BRS. 0b013e3181a54157
46. G. Vadalà S. Sobajima J.Y. Lee J. Huard V. Denaro J. Kang, et al. 2008 In vitro interaction between muscle-derived stem cells and nucleus pulposus cells Spine J 8 804 809 18023623 10.1016/j.spinee.2007.07.394
47. W. Murrell E. Sanford L. Anderberg B. Cavanagh A. Mackay-Sim 2009 Olfactory stem cells can be induced to express chondrogenic phenotype in a rat intervertebral disc injury model Spine J 9 585 594 19345615 10.1016/j.spinee. 2009.02.011
48. C.L. Gilchrist J. Chen W.J. Richardson R.F. Loeser L.A. Setton 2007 Functional integrin subunits regulating cell-matrix interactions in the intervertebral disc J Orthop Res 25 829 840 1:CAS:528:DC%2BD2sXmvFSrs7g%3D 17318895 10.1002/jor.20343 (Pubitemid 46831892)
49. H.B. Henriksson M. Thornemo C. Karlsson O. Hägg K. Junevik A. Lindahl, et al. 2009 Identification of cell proliferation zones, progenitor cells and a potential stem cell niche in the intervertebral disc region: a study in four species Spine 34 2278 2287 19755937 10.1097/BRS.0b013e3181a95ad2
50. K.A. Moore I.R. Lemischka 2006 Stem cells and their niches Science 311 1880 1885 1:CAS:528:DC%2BD28XivFSmtL8%3D 16574858 10.1126/science.1110542
51. M.V. Risbud A. Guttapalli T.T. Tsai J.Y. Lee K.G. Danielson A.R. Vaccaro, et al. 2007 Evidence for skeletal progenitor cells in the degenerate human intervertebral disc Spine 32 2537 2544 17978651 10.1097/BRS.0b013e318158dea6 (Pubitemid 350059479)
52. J. Zhao N. Zhang G.D. Prestwich X.J. Wen 2008 Recruitment of endogenous stem cells for tissue repair Macromol Biosci 8 836 842 1:CAS:528: DC%2BD1cXhtFKnurzI 18528846 10.1002/mabi.200700334
53. W.H. Chen H.Y. Liu W.C. Lo S.C. Wu C.H. Chi H.Y. Chang, et al. 2009 Intervertebral disc regeneration in an ex vivo culture system using mesenchymal stem cells and platelet-rich plasma Biomaterials 30 5523 5533 1:CAS:528:DC%2BD1MXpvFCgurw%3D 19646749 10.1016/j.biomaterials.2009.07.019
54. G. Crevensten A.J. Walsh D. Ananthakrishnan P. Page G.M. Wahba J.C. Lotz, et al. 2004 Intervertebral disc cell therapy for regeneration: mesenchymal stem cell implantation in rat intervertebral discs Ann Biomed Eng 32 430 434 15095817 10.1023/B:ABME.0000017545.84833.7c
55. Y.G. Zhang X. Guo P. Xu L.L. Kang J. Li 2005 Bone mesenchymal stem cells transplanted into rabbit intervertebral discs can increase proteoglycans Clin Orthop 430 219 226 15662327
56. A. Hiyama J. Mochida T. Iwashina H. Omi T. Watanabe K. Serigano, et al. 2008 Transplantation of mesenchymal stem cells in a canine disc degeneration model J Orthop Res 26 589 600 1:CAS:528:DC%2BD1cXlsFegsrk%3D 18203202 10.1002/jor.20584
57. F. Yang V.Y. Leung K.D. Luk D. Chan K.M. Cheung 2009 Mesenchymal stem cells arrest intervertebral disc degeneration through chondrocytic differentiation and stimulation of endogenous cells Mol Ther 7 1959 1966 10.1038/mt.2009.146 1:CAS:528:DC%2BD1MXotF2qsrY%3D
58. H.B. Henriksson T. Svanvik M. Jonsson M. Hagman M. Horn A. Lindahl, et al. 2009 Transplantation of human mesenchymal stems cells into intervertebral discs in a xenogeneic porcine model Spine 34 141 148 19112334 10.1097/BRS.0b013e31818f8c20
59. A. Wei H. Tao S.A. Chung H. Brisby D.D. Ma A.D. Diwan 2009 The fate of transplanted xenogeneic bone marrow-derived stem cells in rat intervertebral discs J Orthop Res 27 374 379 18853431 10.1002/jor.20567
60. J.P. Bao X.T. Wu Y.T. Wang F.Y. Zhang 2008 In vivo MR imaging tracking of iron oxide labeled autologous bone marrow mesenchymal stem cells following degenerated disc injection J Southeast Univ Med Sci Ed 27 166 170
61. Y. Zhang H.S. An C. Tannoury E.J. Thonar M.K. Freedman D.G. Anderson 2008 Biological treatment for degenerative disc disease: implications for the field of physical medicine and rehabilitation Am J Phys Med Rehabil 87 694 702 18716481 10.1097/PHM.0b013e31817c1945
62. S.M. Haufe A.R. Mork 2006 Intradiscal injection of hematopoietic stem cells in an attempt to rejuvenate the intervertebral discs Stem Cells Dev 15 136 137 16522171 10.1089/scd.2006.15.136
63. T. Yoshikawa Y. Ueda K. Miyazaki M. Koizumi Y. Takakura 2010 Disc regeneration therapy using marrow mesenchymal cell transplantation: a report of two case studies Spine 35 E475 E480 20421856
64. C.L. Le Maitre P. Baird A.J. Freemont J.A. Hoyland 2009 An in vitro study investigating the survival and phenotype of mesenchymal stem cells following injection into nucleus pulposus tissue Arthritis Res Ther 11 R20 19210770 10.1186/ar2611 1:CAS:528:DC%2BD1MXis1Kms7g%3D
65. Y. Yamamoto J. Mochida D. Sakai T. Nakai K. Nishimura H. Kawada, et al. 2004 Upregulation of the viability of nucleus pulposus cells by bone marrow-derived stromal cells: significance of direct cell-to-cell contact in coculture system Spine 29 1508 14 15247571 10.1097/01.BRS.0000131416.90906.20 (Pubitemid 38943833)
66. C. Le Visage S.W. Kim K. Tateno A.N. Sieber J.P. Kostuik K.W. Leong 2006 Interaction of human mesenchymal stem cells with disc cells: changes in extracellular matrix biosynthesis Spine 31 2036 2042 16915085 10.1097/01.brs.0000231442.05245.87
67. S.H. Yang C.C. Wu T.F. Shih Y.H. Sun F.H. Lin 2008 In vitro study on interaction between human nucleus pulposus cells and mesenchymal stem cells through paracrine stimulation Spine 33 1951 1957 18708927 10.1097/BRS. 0b013e31817e6974
68. T. Watanabe D. Sakai Y. Yamamoto T. Iwashina K. Serigano F. Tamura, et al. 2010 Human nucleus pulposus cells significantly enhanced biological properties in a coculture system with direct cell-to-cell contact with autologous mesenchymal stem cells J Orthop Res 28 623 630 1:CAS:528: DC%2BC3cXmtVCjtbg%3D 19953600
69. R.J. Deans A.B. Moseley 2000 Mesenchymal stem cells: biology and potential clinical uses Exp Hematol 28 875 884 1:CAS:528:DC%2BD3cXmtlOkur8%3D 10989188 10.1016/S0301-472X(00)00482-3
70. S.M. Richardson N. Hughes J.A. Hunt A.J. Freemont J.A. Hoyland 2008 Human mesenchymal stem cell differentiation to NP-like cells in chitosan- glycerophosphate hydrogels Biomaterials 29 85 93 1:CAS:528:DC%2BD2sXht1Wqtb%2FO 17920676 10.1016/j.biomaterials.2007.09.018 (Pubitemid 47599659)
71. K. Wuertz K. Godburn C. Neidlinger-Wilke J. Urban J.C. Latridis 2008 Behavior of mesenchymal stem cells in the chemical microenvironment of the intervertebral disc Spine 33 1843 1849 18670337 10.1097/BRS.0b013e31817b8f53
72. G. Vadalà R.K. Studer G. Sowa F. Spiezia C. Iucu V. Denaro, et al. 2008 Coculture of bone marrow mesenchymal stem cells and nucleus pulposus cells modulate gene expression profile without cell fusion Spine 33 870 876 18404106 10.1097/BRS.0b013e31816b4619 (Pubitemid 351533855)
73. J.L. Bron M.N. Helder H.J. Meisel B.J. Van-Royen T.H. Smit 2009 Repair, regenerative and supportive therapies of the annulus fibrosus: achievements and challenges Eur Spine J 18 301 313 19104850 10.1007/s00586-008-0856-x
74. A. Hiyama J. Mochida D. Sakai 2008 Stem cell applications in intervertebral disc repair Cell Mol Biol 54 24 32 1:STN:280: DC%2BD1cnptV2kug%3D%3D 18954548
75. N. Kimelman R.J. Oskouian Y. Zilberman G. Pelled Z. Gazit D. Gazit 2006 Genetically engineered adult stem cells and hybrid scaffolds as a platform for intervertebral disc regeneration Mol Ther 13 S175 S176 10.1016/j.ymthe.2006.08. 523
76. J.M. Ryan F. Barry J.M. Murphy B.P. Mahon 2007 Interferon-gamma does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells Clin Exp Immunol 149 353 363 1:CAS:528:DC%2BD2sXhtVShs73K 17521318 10.1111/j.1365-2249.2007.03422.x (Pubitemid 47063057)
77. S.E. Haynesworth M.A. Baber A.I. Caplan 1996 Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: effects of dexamethasone and IL-1 alpha J Cell Physiol 166 585 592 1:CAS:528:DyaK28XhsVegtLs%3D 8600162 10.1002/(SICI)1097-4652(199603)166:3<585::AID-JCP13>3.0.CO;2-6 (Pubitemid 26095485)
78. A.I. Caplan J.E. Dennis 2006 Mesenchymal stem cells as trophic mediators J Cell Biochem 98 1076 1084 1:CAS:528:DC%2BD28XnsVyjtL0%3D 16619257 10.1002/jcb.20886 (Pubitemid 44128350)
79. K. Masuda T.R. Oegema Jr H.S. An 2004 Growth factors and treatment of intervertebral disc degeneration Spine 29 2757 2769 15564925 10.1097/01.brs.0000146048.14946.af (Pubitemid 40353262)
80. H. Pratsinis D. Kletsas 2008 Growth factors in intervertebral disc homeostasis Connect Tissue Res 49 273 276 1:CAS:528:DC%2BD1cXptVKlt70%3D 18661359 10.1080/03008200802147951
81. H.E. Gruber E.C. Fisher Jr B. Desai A.A. Stasky G. Hoelscher E.N. Hanley 1997 Human intervertebral disc cells from the annulus: three-dimensional culture in agarose or alginate and responsiveness to TGF-β1 Exp Cell Res 235 13 21 1:CAS:528:DyaK2sXlvVKgsbk%3D 9281347 10.1006/excr.1997.3647 (Pubitemid 27381676)
82. J.P. Thompson T.R. Oegema Jr D.S. Bradford 1991 Stimulation of mature canine intervertebral disc by growth factors Spine 16 253 260 1:STN:280:DyaK3M3isl2lsg%3D%3D 2028297 10.1097/00007632-199103000-00001
83. R. Osada H. Ohshima H. Ishihara K. Yudoh K. Sakai H. Matsui, et al. 1996 Autocrine/paracrine mechanism of insulin-like growth factor-1 secretion, and the effect of insulin-like growth factor-1 on proteoglycan synthesis in bovine intervertebral discs J Orthop Res 14 690 699 1:CAS:528:DyaK28XmvFWitbw%3D 8893760 10.1002/jor.1100140503 (Pubitemid 26376511)
84. H.E. Gruber H.J. Norton E.N. Hanley Jr. 2000 Anti-apoptotic effects of IGF-1 and PDGF on human intervertebral disc cells in vitro Spine 25 2153 2157 1:STN:280:DC%2BD3cvpvVCgtw%3D%3D 10973395 10.1097/00007632-200009010-00002
85. H. Pratsinis D. Kletsas 2007 PDGF, bFGF and IGF-I stimulate the proliferation of intervertebral disc cells in vitro via the activation of the ERK and Akt signaling pathways Eur Spine J 16 1858 1866 17763874 10.1007/s00586-007-0408-9 (Pubitemid 350105321)
86. X. Li B.M. Leo G. Beck G. Balian D.G. Anderson 2004 Collagen and proteoglycan abnormalities in the GDF-5-deficient mice and molecular changes when treating disk cells with recombinant growth factor Spine 29 2229 2234 15480133 10.1097/01.brs.0000142427.82605.fb (Pubitemid 40362216)
87. K. Masuda K. Takegami H. An F. Kumano K. Chiba G.B. Andersson, et al. 2003 Recombinant osteogenic protein-1 upregulates extracellular matrix metabolism by rabbit annulus fibrosus and nucleus pulposus cells cultured in alginate beads J Orthop Res 21 922 930 1:CAS:528:DC%2BD3sXmt1Wktb0%3D 12919882 10.1016/S0736-0266(03)00037-8 (Pubitemid 37045572)
88. S. Tim Yoon K. Su Kim J. Li J. Soo Park T. Akamaru W.A. Elmer W.C. Hutton 2003 The effect of bone morphogenetic protein-2 on rat intervertebral disc cells in vitro Spine 28 1773 1780 1:STN:280:DC%2BD3szos1CnsA%3D%3D 12923462 10.1097/01.BRS.0000083204.44190.34 (Pubitemid 37012751)
89. L. Gilbertson S.H. Ahn P.N. Teng R.K. Studer C. Niyibizi J.D. Kang 2008 The effects of recombinant human bone morphogenetic protein-2, recombinant human bone morphogenetic protein-12, and adenoviral bone morphogenetic protein-12 on matrix synthesis in human annulus fibrosis and nucleus pulposus cells Spine J 8 449 456 18455111 10.1016/j.spinee.2006.11.006 (Pubitemid 351608960)
90. J. Mochida 2005 New strategies of disc repair; novel preclinical trials J Orthop Sci 10 112 118 15666134 10.1007/s00776-004-0864-6 (Pubitemid 40193019)
91. H.S. Yan X.T. Wu Y.T. Wang J.S. Shao Y. Cao J.P. Bao, et al. 2009 The rise and fall of the trophic and differentiated effects in cell therapy for regeneration of degenerative intervertebral discs Chin J Exp Surg 26 125 127
92. A. Wei H. Brisby S.A. Chung A.D. Diwan 2008 Bone morphogenetic protein-7 protects human intervertebral disc cells in vitro from apoptosis Spine J 8 466 474 18082466 10.1016/j.spinee.2007.04.021
93. C.Q. Zhao L.M. Wang L.S. Jiang L.Y. Dai 2006 Programmed cell death in intervertebral disc degeneration Apoptosis 11 2079 2088 17051327 10.1007/s10495-006-0290-7 (Pubitemid 44885385)
94. L.E. Broker F.A. Kruyt G. Giaccone 2005 Cell death independent of caspases: a review Clin Cancer Res 11 3155 3162 15867207 10.1158/1078-0432.CCR- 04-2223 (Pubitemid 40627860)
95. J.B. Park J.K. Lee S.J. Park K.W. Kim K.D. Riew 2005 Mitochondrial involvement in fas-mediated apoptosis of human lumbar disc cells J Bone Joint Surg Am 87 1338 1342 15930545 10.2106/JBJS.D.02527 (Pubitemid 40756637)
96. K. Ariga K. Yonenobu T. Nakase N. Hosono S. Okuda W. Meng, et al. 2003 Mechanical stress-induced apoptosis of endplate chondrocytes in organ-cultured mouse intervertebral discs: an ex vivo study Spine 28 1528 1533 12865839 10.1097/00007632-200307150-00010 (Pubitemid 36877085)
97. S.K. Tschoeke M. Hellmuth A. Hostmann Y. Robinson W. Ertel A. Oberholzer, et al. 2008 Apoptosis of human intervertebral discs after trauma compares to degenerated discs involving both receptor-mediated and mitochondrial-dependent pathways J Orthop Res 26 999 1006 1:CAS:528:DC%2BD1cXosFGrurg%3D 18302283 10.1002/jor.20601
98. J.B. Park I.C. Park S.J. Park H.O. Jin J.K. Lee K.D. Riew 2006 Antiapoptotic effects of caspase inhibitors on rat intervertebral disc cells J Bone Joint Surg Am 88 771 779 16595467 10.2106/JBJS.E.00762
99. H. Tapp R. Deepe J.A. Ingram E.G. Yarmola M.R. Bubb E.N. Hanley Jr, et al. 2009 Exogenous thymosin beta(4) prevents apoptosis in human intervertebral annulus cells in vitro Biotech Histochem 84 287 294 1:CAS:528: DC%2BC3cXisVSksw%3D%3D 20055734 10.3109/10520290903116884
100. Y. Kang W.M. Liao P.Y. Sheng L.J. Zhang X.W. Yuan L. Lei, et al. 2007 Construction and identification of human bone morphogenetic protein-7 recombinant adeno-associated virus type 2 vector and its expression in bone mesenchymal stem cells Zhonghua Wai Ke Za Zhi 45 1279 1283 18067746
101. M.V. Risbud A. Guttapalli D.G. Stokes D. Hawkins K.G. Danielson T.P. Schaer, et al. 2006 Nucleus pulposus cells express HIF-1 alpha under normoxic culture conditions: a metabolic adaptation to the intervertebral disc microenvironment J Cell Biochem 98 152 159 1:CAS:528:DC%2BD28Xjslaqs7g%3D 16408279 10.1002/jcb.20765
102. Y. Zeng K.G. Danielson T.J. Albert I.M. Shapiro M.V. Risbud 2007 HIF-1 alpha is a regulator of galectin-3 expression in the intervertebral disc J Bone Miner Res 22 1851 1861 1:CAS:528:DC%2BD2sXhsVyjtrnM 17592963 10.1359/jbmr.070620 (Pubitemid 351229301)
103. H.E. Gruber J.A. Ingram D.E. Davis E.N. Hanley Jr. 2009 Increased cell senescence is associated with decreased cell proliferation in vivo in the degenerating human annulus Spine J 9 210 215 18440281 10.1016/j.spinee.2008.01. 012
104. S. Roberts E.H. Evans D. Kletsas D.C. Jaffray S.M. Eisenstein 2006 Senescence in human intervertebral discs Eur Spine J 15 S312 S316 16773379 10.1007/s00586-006-0126-8 (Pubitemid 44371008)
105. H.W. Zhou S.X. Hou W.L. Shang F. Mei 2006 Effect of P16INK4a vs Fas on function of intervertebral disc Chin J Exp Surg 23 1505 1507 1:CAS:528:DC%2BD1cXis1SltbY%3D
106. T. Nakai J. Mochida D. Sakai 2008 Synergistic role of c-Myc and ERK1/2 in the mitogenic response to TGF beta-1 in cultured rat nucleus pulposus cells Arthritis Res Ther 10 R140 19061498 10.1186/ar2567 1:CAS:528:DC%2BD1MXntlKn
107. H.E. Gruber G.L. Hoelscher J.A. Ingram S. Bethea E.N. Hanley 2008 IGF-1 rescues human intervertebral annulus cells from in vitro stress-induced premature senescence Growth Factors 26 220 225 1:CAS:528:DC%2BD1cXhtVyrsLnK 19021034 10.1080/08977190802273814
108. C.C. Niu L.J. Yuan S.S. Lin L.H. Chen W.J. Chen 2009 Mesenchymal stem cell and nucleus pulposus cell coculture modulates cell profile Clin Orthop 467 3263 3272 19034596 10.1007/s11999-008-0623-7
109. G. Lepperdinger R. Brunauer A. Jamnig G. Laschober M. Kassem 2008 Controversial issue: is it safe to employ mesenchymal stem cells in cell-based therapies? Exp Gerontol 43 1018 1023 1:CAS:528:DC%2BD1cXhtlansr%2FM 18694815 10.1016/j.exger.2008.07.004
110. E.N. Momin G. Vela H.A. Zaidi A. Quiñones-Hinojosa 2010 The oncogenic potential of mesenchymal stem cells in the treatment of cancer: directions for future research Curr Immunol Rev 6 137 148 1:CAS:528: DC%2BC3cXhtl2msbjL 20490366 10.2174/157339510791111718
111. D. Sakai 2008 Future perspectives of cell-based therapy for intervertebral disc disease Eur Spine J 17 S452 S458 10.1007/s00586-008-0743-5