Adipose stem cells for intervertebral disc regeneration: Current status and concepts for the future: Tissue Engineering Review Series

Journal of Cellular and Molecular Medicine

Volumn 12, Issue 6A, 2008, Pages 2205-2216

  Hoogendoorn, R J W ^a,d   Lu, Z F ^a,d   Kroeze, R J ^a,b,d   Bank, R A ^b,c,d   Wuisman, P I ^a,d   Helder, M N ^a,d  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c TNO   (Netherlands)

^d Skeletal Tissue Engineering Group Amsterdam   (Netherlands)

Author keywords

Adipose tissue; Intervertebral disc degeneration; Mesenchymal stem cells; Regeneration; Scaffold; Stem cell selection

Indexed keywords

ADIPOCYTE; ANIMAL; ARTICLE; HUMAN; IN VITRO STUDY; INTERVERTEBRAL DISK; MESENCHYMAL STEM CELL TRANSPLANTATION; PATHOLOGY; PATHOPHYSIOLOGY; REGENERATION; SPINE DISEASE; SPINE FUSION; TISSUE ENGINEERING; TRANSPLANTATION;

ADIPOCYTES; ANIMALS; HUMANS; INTERVERTEBRAL DISK; MESENCHYMAL STEM CELL TRANSPLANTATION; REGENERATION; SPINAL DISEASES; SPINAL FUSION; TISSUE ENGINEERING;

ANIMALIA; CAPRA HIRCUS;

EID: 57249084243     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2008.00291.x     Document Type: Article

References (142)

1. Dreinhofer KE. The Bone and Joint Decade 2000-2010 - How Far Have We Come? European musculoskeletal review. 2006 Sept : 12 7.
2. Cowan CM, Aalami OO, Shi YY, Chou YF, Mari C, Thomas R, Quarto N, Nacamuli RP, Contag CH, Wu B, Longaker MT. Bone morphogenetic protein 2 and retinoic acid accelerate in vivo bone formation, osteo-clast recruitment, and bone turnover. Tissue Eng. 2005 11 : 645 58.
3. Evans CH, Rosier RN. Molecular biology in orthopaedics: the advent of molecular orthopaedics. J Bone Joint Surg Am. 2005 87 : 2550 64.
4. Bao QB, McCullen GM, Higham PA, Dumbleton JH, Yuan HA. The artificial disc: theory, design and materials. Biomaterials. 1996 17 : 1157 67.
5. Frick SL, Hanley EN Jr., Meyer RA Jr., Ramp WK, Chapman TM. Lumbar inter-vertebral disc transfer. A canine study. Spine. 1994 19 : 1826 34.
6. Melrose J, Roberts S, Smith S, Menage J, Ghosh P. Increased nerve and blood vessel ingrowth associated with proteoglycan depletion in an ovine anular lesion model of experimental disc degeneration. Spine. 2002 27 : 1278 85.
7. Osti OL, Vernon-Roberts B, Moore R, Fraser RD. Annular tears and disc degeneration in the lumbar spine. A postmortem study of 135 discs. J Bone Joint SurgBr. 1992 74 : 678 82.
8. Adams MA, Roughley PJ. What is inter-vertebral disc degeneration, and what causes it? Spine. 2006 31 : 2151 61.
9. Buckwalter JA. Aging and degeneration of the human intervertebral disc. Spine. 1995 20 : 1307 14.
10. Kraemer J. Natural course and prognosis of intervertebral disc diseases. International Society for the Study of the Lumbar Spine Seattle, Washington, June 1994. Spine. 1995 20 : 635 9.
11. Ala-Kokko L. Genetic risk factors for lumbar disc disease. Ann Med. 2002 34 : 42 7.
12. Battie MC, Videman T, Gill K, Moneta GB, Nyman R, Kaprio J, Koskenvuo M. 1991 Volvo Award in clinical sciences. Smoking and lumbar intervertebral disc degeneration: an MRI study of identical twins. Spine. 1991 16 : 1015 21.
13. Battie MC, Videman T, Gibbons LE, Manninen H, Gill K, Pope M, Kaprio J. Occupational driving and lumbar disc degeneration: a case-control study. Lancet. 2002 360 : 1369 74.
14. Videman T, Battie MC. The influence of occupation on lumbar degeneration. Spine. 1999 24 : 1164 8.
15. Gibson JN. Watltlell G. Surgery for degenerative lumbar spondylosis: updated Cochrane Review. Spine. 2005 30 : 2312 20.
16. Leung VY, Chan D, Cheung KM. Regeneration of intervertebral disc by mesenchymal stem cells: potentials, limitations, and future direction. Eur Spine J. 2006 15 : S406 S413.
17. Masuda K, Oegema TR, Jr., An HS. Growth factors and treatment of intervertebral disc degeneration. Spine. 2004 29 : 2757 69.
18. Masuda K, An HS. Prevention of disc degeneration with growth factors. Eur Spine J. 2006 15 : S422 32.
19. Paesold G, Nerlich AG, Boos N. Biological treatment strategies for disc degeneration: potentials and shortcomings. Eur Spine J. 2007 16 : 447 68.
20. Yoon ST, Patel NM. Molecular therapy of the intervertebral disc. Eur Spine J. 2006 15 : S379 88.
21. Lee JY, Hall R, Pelinkovic D, Cassinelli E, Usas A, Gilbertson L, Huard J, Kang J. New use of a three-dimensional pellet culture system for human intervertebral disc cells: initial characterization and potential use for tissue engineering. Spine. 2001 26 : 2316 22.
22. Nishida K. Kang JD. Gilbertson LG. Moon SH. Suh JK. Vogt MT. Robbins PD. Evans CH. Modulation of the biologic activity of the rabbit intervertebral disc by gene therapy: an in vivo study of adenovirus-mediated transfer of the human transforming growth factor beta 1 encoding gene. Spine. 1999 24 : 2419 25.
23. Tan Y, Hu Y, Tan J. Extracellular matrix synthesis and ultrastructural changes of degenerative disc cells transfected by Ad/CMV-hTGF-beta 1. Chin Med J (Engl). 2003 116 : 1399 403.
24. Masuda K. Takegami K. An H. Kumano F. Chiba K. Andersson GB. Schmid T. Thonar E. Recombinant osteogenic protein-1 upregulates extracellular matrix metabolism by rabbit annulus fibrosus and nucleus pulposus cells cultured in alginate beads. J Orthop Res. 2003 21 : 922 30.
25. Zhang Y. An HS. Song S. Toofanfard M. Masuda K. Andersson GB, Thonar EJ. Growth factor osteogenic protein-1: differing effects on cells from three distinct zones in the bovine intervertebral disc. Am J Phys Med Rehabil. 2004 83 : 515 21.
26. Chujo T. An HS, Akeda K. Miyamoto K. Muehleman C. Attawia M. Andersson G. Masuda K. Effects of growth differentiation factor-5 on the intervertebral discm vitro bovine study and in vivo rabbit disc degeneration model study. Spine. 2006 31 : 2909 17.
27. Walsh AJ, Bradford DS, Lotz JC. in vivo growth factor treatment of degenerated intervertebral discs. Spine. 2004 29 : 156 63.
28. Thompson JP. Oegema TR Jr. Bradford DS. Stimulation of mature canine intervertebral disc by growth factors. Spine. 1991 16 : 253 60.
29. Yoon ST, Park JS, Kim KS, Li J, Attallah-Wasif ES, Hutton WC, Boden SD. ISSLS prize winner: LMP-1 upregulates intervertebral disc cell production of proteoglycans and BMPs in vitro and in vivo. Spine. 2004 29 : 2603 11.
30. Paul R, Haydon RC, Cheng H, Ishikawa A, Nenadovich N, Jiang W, Zhou L, Breyer B, Feng T, Gupta P, He TC, Phillips FM. Potential use of Sox9 gene therapy for intervertebral degenerative disc disease. Spine. 2003 28 : 755 63.
31. Hatakeyama Y, Nguyen J, Wang X, Nuckolls GH, Shum L. Smad signaling in mesenchymal and chondroprogenitor cells. J Bone Joint Surg Am. 2003 85 : 13 8.
32. Nohe A, Keating E, Knaus P, Petersen NO. Signal transduction of bone morpho-genetic protein receptors. Cell Signal. 2004 16 : 291 9.
33. Wallach CJ, Sobajima S, Watanabe Y, Kim JS, Georgescu HI, Robbins P, Gilbertson LG, Kang JD. Gene transfer of the catabolic inhibitor TIMP-1 increases measured proteoglycans in cells from degenerated human intervertebral discs. Spine. 2003 28 : 2331 7.
34. Okuma M, An HS, Nakagawa K, Akeda K, Muehleman C. Oral administartion of esculetin prodrug inhibits intervertebral disc degeneration in the rabbit annular needle puncture model. Orthopaedic Research Society Transactions. 2005 370.
35. Ganey T, Libera J, Moos V, Alasevic O, Fritsch KG, Meisel HJ, Hutton WC. Disc chondrocyte transplantation in a canine model: a treatment for degenerated or damaged intervertebral disc. Spine. 2003 28 : 2609 20.
36. Gruber HE, Johnson TL, Leslie K, Ingram JA, Martin D, Hoelscher G, Banks D, Phieffer L, Coldham G, Hanley EN, Jr. Autologous intervertebral disc cell implantation: a model using Psammomys obesus: the sand rat. Spine. 2002 27 : 1626 33.
37. Sato M, Asazuma T, Ishihara M, Ishihara M, Kikuchi T, Kikuchi M, Fujikawa K. An experimental study of the regeneration of the intervertebral disc with an allograft of cultured annulus fibrosus cells using a tissue-engineering method. Spine. 2003 28 : 548 53.
38. Gorensek M, Jaksimovic C, Kregar-Velikonja N, Gorensek M, Knezevic M, Jeras M, Pavlovcic V, Cor A. Nucleus pulposus repair with cultured autologous elastic cartilage derived chondrocytes. Cell Mol Biol Lett. 2004 9 : 363 73.
39. Sakai D, Mochida J, Yamamoto Y, Nomura T, Okuma M, Nishimura K, Nakai T, Ando K, Hotta T. Transplantation of mesenchymal stem cells embedded in Atelocollagen gel to the intervertebral disc: a potential therapeutic model for disc degeneration. Biomaterials. 2003 24 : 3531 41.
40. Sakai D, Mochida J, Iwashina T, Watanabe T, Nakai T, Ando K, Hotta T. Differentiation of mesenchymal stem cells transplanted to a rabbit degenerative disc model: potential and limitations for stem cell therapy in disc regeneration. Spine. 2005 30 : 2379 87.
41. Sakai D, Mochida J, Iwashina T, Hiyama A, Omi H, Imai M, Nakai T, Ando K, Hotta T. Regenerative effects of transplanting mesenchymal stem cells embedded in atelocollagen to the degenerated intervertebral disc. Biomaterials. 2006 27 : 335 45.
42. Zhang YG, Guo X, Xu P, Kang LL, Li J. Bone mesenchymal stem cells transplanted into rabbit intervertebral discs can increase proteoglycans. Clin Orthop Relat Res. 2005 219 26.
43. Moore KA, Lemischka IR. Stem cells and their niches. Science. 2006 311 : 1880 5.
44. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science. 1999 284 : 143 7.
45. Semb H. Human embryonic stem cells: origin, properties and applications. APMIS. 2005 113 : 743 50.
46. Korbling M, Robinson S, Estrov Z, Champlin R, Shpall E. Umbilical cord blood-derived cells for tissue repair. Cytotherapy 2005 7 : 258 61.
47. Vats A, Bielby RC, Tolley NS, Nerem R, Polak JM. Stem cells. Lancet. 2005 366 : 592 602.
48. Fraser JK, Wulur I, Alfonso Z, Hedrick MH. Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol. 2006 24 : 150 4.
49. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang Jl, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell. 2002 13 : 4279 95.
50. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001 7 : 211 28.
51. Castro-Malaspina H, Ebell W, Wang S. Human bone marrow fibroblast colony-forming units (CFU-F). Prog Clin Biol Res. 1984 154 : 209 36.
52. Caplan Al. Review: mesenchymal stem cells: cell-based reconstructive therapy in orthopedics. Tissue Eng. 2005 11 : 1198 211.
53. Oedayrajsingh-Varma MJ, van Ham SM, Knippenberg M, Helder MN, Klein-Nulend J, Schouten TE, Ritt MJ, van Milligen FJ. Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy. 2006 8 : 166 77.
54. Prunet-Marcassus B, Cousin B, Caton D, Andre M, Penicaud L, Casteilla L. From heterogeneity to plasticity in adipose tissues: site-specific differences. Exp Cell Res. 2006 312 : 727 36.
55. Afizah H. Yang Z. Hul JHP, Ouyang HW, Lee EH. A comparison between the chondrogenic potential of human bone marrow stem cells (BMSCs) and adipose-derived stem cells (ADSCs) taken from the same donors. Tissue Engineering. 2007 13 : 659 66.
56. Huang Jl, Kazml N, Durbhakula MM, Herlng TM, Yoo JU, Johnstone B. Chondrogenic potential of progenitor cells derived from human bone marrow and adipose tissue: a patient-matched comparison. J Orthop Res. 2005 23 : 1383 9.
57. Ogawa R. Fujimura J, Hanawa H. Hlral Y. Kural T. Mlzuno H. Hyakusoku H. Shlmada T. Comparison of stem cells harvested from adipose tissue and bone marrow. Stood. 2005 106 : 136B.
58. De Ugarte DA, Morlzono K, Elbarbary A, Alfonso Z, Zuk PA, Zhu M, Dragoo JL, Ashjian P, Thomas B, Benhalm P, Chen I, Fraser J, Hedrick MH. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs. 2003 174 : 101 9.
59. Kern S, Elchler H, Stoeve J, Kluter H, Bleback K. Comparative analysis of mesenchymal stem cells from bone marrow: umbilical cord blood, or adipose tissue. Stem Cells. 2006 24 : 1294 301.
60. Shlrasawa S, Seklya I, Sakaguchl Y, Yagishita K, Ichlnose S, Muneta T. in vitro chondrogenesis of human synovium-derived mesenchymal stem cells: optimal condition and comparison with bone marrow-derived cells. J Cell Biochem. 2006 97 : 84 97.
61. Awad HA, Halvorsen YD, Glmble JM, Guilak F. Effects of transforming growth factor betal and dexamethasone on the growth and chondrogenic differentiation of adipose-derived stromal cells. Tissue Eng. 2003 9 : 1301 12.
62. Housman TS, Lawrence N, Mellen BG, George MN, Flllppo JS, Cerveny KA, DeMarco M, Feldman SR, Fleischer AB. The safety of liposuction: results of a national survey. Dermatol Surg. 2002 28 : 971 8.
63. Pountos I, Jones E, Tzloupls C, McGonagle D, Giannoudis PV. Growing bone and cartilage. The role of mesenchymal stem cells. J Bone Joint Surg Br 2006 88 : 421 6.
64. Quarto R, Mastroglacomo M, Cancedda R, Kutepov SM, Mukhachev V, Lavroukov A, Kon E, Marcaccl M. Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med. 2001 344 : 385 6.
65. Helder MN, Knlppenberg M, Kleln-Nulend J, Wuisman PI. Stem cells from adipose tissue allow challenging new concepts for regenerative medicine. Tissue Eng. 2007 13 : 1799 808.
66. Smlt TH, Krijnen MR, van Dijk M, Wuisman PI. Application of polylactides in spinal cages: studies in a goat model. J Mater Sci Mater Med. 2006 17 : 1237 44.
67. van Dijk M, van Diest PJ, Smit TH, Berkhof H, Burger EH, Wuisman PI. Four-year follow-up of poly-L-lactic Acid cages for lumbar interbody fusion in goats. J Long Term Eff Med Implants. 2005 15 : 125 38.
68. Wuisman PI, van Dijk M, Smit TH. Resorbable cages for spinal fusion: an experimental goat model. J Neurosurg. 2002 97 : 433 9.
69. Knippenberg M, Helder MN, Zandieh DB, Wuisman PI, Klein-Nulend J. Osteogenesis versus chondrogenesis by BMP-2 and BMP-7 in adipose stem cells. Biochem Biophys Res Commun. 2006 342 : 902 8.
70. Knippenberg M, Helder MN, Doulabi BZ, Semeins CM, Wuisman PI, Klein-Nulend J. Adipose tissue-derived mesenchymal stem cells acquire bone cell-like responsiveness to fluid shear stress on osteogenic stimulation. Tissue Eng. 2005 11 : 1780 8.
71. Steck E, Bertram H, Abel R, Chen B, Winter A, Richter W. Induction of intervertebral disc-like cells from adult mesenchymal stem cells. Stem Cells. 2005 23 : 403 11.
72. Sive Jl, Baird P, Jeziorsk M, Watkins A, Hoyland JA, Freemont AJ. Expression of chondrocyte markers by cells of normal and degenerate intervertebral discs. Mol Pathol. 2002 55 : 91 7.
73. Richardson SM, Walker RV, Parker S, Rhodes NP, Hunt JA, Freemont AJ, Hoyland JA. Intervertebral disc cell-mediated mesenchymal stem cell differentiation. Stem Cells. 2006 24 : 707 16.
74. Yamamoto Y, Mochida J, Sakai D, Nakai T, Nishimura K, Kawada H, Hotta T. 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. 2004 29 : 1508 14.
75. Maroudas A, Stockwell RA, Nachemson A, Urban J. Factors involved in the nutrition of the human lumbar intervertebral disc: cellularity and diffusion of glucose in vitro. JAnat. 1975 120 : 113 30.
76. Li X, Lee JP, Balian G, Greg AD. Modulation of chondrocytic properties of fat-derived mesenchymal cells in co-cultures with nucleus pulposus. Connect Tissue Res. 2005 46 : 75 82.
77. Nicoll SB, Wedrychowska A, Smith NR, Bhatnagar RS. Modulation of proteoglycan and collagen profiles in human dermal fibroblasts by high density micromass culture and treatment with lactic acid suggests change to a chondrogenic phenotype. Connect Tissue Res. 2001 42 : 59 69.
78. Schulze-Tanzil G, de Souza P, Villegas CH, John T, Merker HJ, Scheid A, Shakibaei M. Redifferentiation of dediffer-entiated human chondrocytes in high-density cultures. Cell Tissue Res. 2002 308 : 371 9.
79. Lu ZF, Zandieh DB, Wuisman PI, Bank RA, Helder MN. Differentiation of adipose stem cells by nucleus pulposus cells: configuration effect. Biochem Biophys Res Commun. 2007 359 : 991 6.
80. Campbell A, Wicha MS, Long M. Extracellular matrix promotes the growth and differentiation of murine hematopoietic cells in vitro. J Clin Invest. 1985 75 : 2085 90.
81. Huet C, Pisselet C, Mandon-Pepin B, Monget P, Monniaux D. Extracellular matrix regulates ovine granulosa cell survival, proliferation and steroidogenesis: relationships between cell shape and function. J Endocrinol. 2001 169 : 347 60.
82. Kihara T, Hirose M, Oshima A, Ohgushi H. Exogenous type I collagen facilitates osteogenic differentiation and acts as a substrate for mineralization of rat marrow mesenchymal stem cells in vitro. Biochem Biophys Res Commun. 2006 341 : 1029 35.
83. Guiot BH, Fessler RG. Molecular biology of degenerative disc disease. Neurosurgery 2000 47 : 1034 40.
84. Nerlich AG, Boos N, Wiest I, Aebi M. Immunolocalization of major interstitial collagen types in human lumbar intervertebral discs of various ages. Virchows Arch. 1998 432 : 67 76.
85. Scully SP, Lee JW, Ghert PMA, Qi W. The role of the extracellular matrix in articular chondrocyte regulation. Clin Orthop Relat Res. 2001 S72 S89.
86. Van der Kraan PM, Buma P, van KT, Van Den Berg WB. Interaction of chondrocytes, extracellular matrix and growth factors: relevance for articular cartilage tissue engineering. Osteoarthritis Cartilage. 2002 10 : 631 7.
87. Bosnakovski D, Mizuno M, Kim G, Takagi S, Okumura M, Fujinaga T. Chondrogenic differentiation of bovine bone marrow mesenchymal stem cells (MSCs) in different hydrogels: influence of collagen type II extracellular matrix on MSC chondrogenesis. Biotechnol Bioeng. 2006 93 : 1152 63.
88. Chen CW, Tsai YH, Deng WP, Shih SN, Fang CL, Burch JG, Chen WH, Lai WF. Type I and II collagen regulation of chondrogenic differentiation by mesenchymal progenitor cells. J Orthop Res. 2005 23 : 446 53.
89. Loeser RF. Integrins and cell signaling in chondrocytes. Biorheology. 2002 39 : 119 24.
90. Lu ZF, Zandieh DB, Wuisman PI, Bank RA, Helder MN. Influence of collagen type II and nucleus pulposus cells on aggregation and differentiation of adipose tissue-derived stem cells. J Cell Mol Med. 2008 in press.
91. Calvert JW, Marra KG, Cook L, Kumta PN, DiMilla PA, Weiss LE. Characterization of osteoblast-like behavior of cultured bone marrow stromal cells on various polymer surfaces. J Biomed Mater Res. 2000 52 : 279 84.
92. Murphy WL, Hsiong S, Richardson TP, Simmons CA, Mooney DJ. Effects of a bone-like mineral film on phenotype of adult human mesenchymal stem cells In vitro. Biomaterials. 2005 26 : 303 10.
93. Chastain SR, Kundu AK, Dhar S, Calvert JW, Putnam AJ. Adhesion of mesenchymal stem cells to polymer scaffolds occurs via distinct ECM ligands and controls their osteogenic differentiation. J Biomed Mater Res A. 2006 78 : 73 85.
94. Salasznyk RM, Williams WA, Boskey A, Batorsky A, Plopper GE. Adhesion to Vitronectin and Collagen I Promotes Osteogenic Differentiation of Human Mesenchymal Stem Cells. J Biomed Biotechnol. 2004 2004 : 24 34.
95. Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science. 2005 310 : 1139 43.
96. Alini M, Roughley PJ, Antoniou J, Stoll T, Aebi M. A biological approach to treating disc degeneration: not for today but maybe for tomorrow. Eur Spine J. 2002 11 : S215 20.
97. Mwale F, lordanova M, Demers CN, Steffen T, Roughley P, Antoniou J. Biological evaluation of chitosan salts cross-linked to genipin as a cell scaffold for disk tissue engineering. Tissue Eng. 2005 11 : 130 40.
98. Roughley P, Hoemann C, DesRosiers E. Mwale F, Antoniou J, Alini M. The potential of chitosan-based gels containing intervertebral disc cells for nucleus pulposus supplementation. Biomaterials. 2006 27 : 388 96.
99. Crevensten G, Walsh AJ, Ananthakrishnan D, Page P, Wahba GM, Lotz JC, Berven S. Intervertebral disc cell therapy for regeneration: mesenchymal stem cell implantation in rat intervertebral discs. Ann Biomed Eng. 2004 32 : 430 4.
100. Mizuno H, Roy AK, Vacanti CA, Kojima K. Ueda M, Bonassar LJ. Tissue-engineered composites of anulus fibrosus and nucleus pulposus for intervertebral disc replacement. Spine. 2004 29 : 1290 7.
101. Mizuno H, Roy AK, Zaporojan V, Vacanti CA, Ueda M, Bonassar LJ. Biomechanical and biochemical characterization of composite tissue-engineered intervertebral discs. Biomaterials. 2006 27 : 362 70.
102. Li WJ, Laurencin CT, Caterson EJ, Tuan RS, Ko FK. Electrospun nanofibrous structure: a novel scaffold for tissue engineering. J Biomed Mater Res. 2002 60 : 613 21.
103. Ishihara H, Urban JP. Effects of low oxygen concentrations and metabolic inhibitors on proteoglycan and protein synthesis rates in the intervertebral disc. J Orthop Res. 1999 17 : 829 35.
104. Bibby SR, Jones DA, Ripley RM, Urban JP. Metabolism of the intervertebral disc: effects of low levels of oxygen, glucose, and pH on rates of energy metabolism of bovine nucleus pulposus cells. Spine. 2005 30 : 487 96.
105. Malladi P, Xu Y, Chiou M, Giaccia AJ, Longaker MT. Effect of reduced oxygen tension on chondrogenesis and osteogenesis in adipose-derived mesenchymal cells. Am J Physiol Cell Physiol. 2006 290 : C1139 46.
106. Robins JC, Akeno N, Mukherjee A, Dalai RR, Aronow BJ, Koopman P, Clemens TL. Hypoxia induces chondrocyte-specific gene expression in mesenchymal cells in association with transcriptional activation of Sox9. Bone. 2005 37 : 313 22.
107. Malda J, Martens DE, Tramper J, van Blitterswijk CA, Riesle J. Cartilage tissue engineering: controversy in the effect of oxygen. Crit Rev Biotechnol. 2003 23 : 175 94.
108. Razaq S, Wilkins RJ, Urban JP. The effect of extracellular pH on matrix turnover by cells of the bovine nucleus pulposus. Eur Spine J. 2003 12 : 341 9.
109. Lotz JC. Animal models of intervertebral disc degeneration: lessons learned. Spine. 2004 29 : 2742 50.
110. Holm S, Holm AK, Ekstrom L, Karladani A, Hansson T. Experimental disc degeneration due to endplate injury. J Spinal Disord Tech. 2004 17 : 64 71.
111. latridis JC, Mente PL, Stokes IA, Aronsson DD, Alini M. Compression-induced changes in intervertebral disc properties in a rat tail model. Spine. 1999 24 : 996 1002.
112. Lipson SJ, Muir H. 1980 Volvo award in basic science. Proteoglycans in experimental intervertebral disc degeneration. Spine. 1981 6 : 194 210.
113. Masuda K, Aota Y, Muehleman C, Imai Y, Okuma M, Thonar EJ, Andersson GB, An HS. A novel rabbit model of mild, reproducible disc degeneration by an anulus needle puncture: correlation between the degree of disc injury and radiological and histological appearances of disc degeneration. Spine. 2005 30 : 5 14.
114. Sobajima S, Kompel JF, Kim JS, Wallach CJ, Robertson DD, Vogt MT, Kang JD, Gilbertson LG. A slowly progressive and reproducible animal model of intervertebral disc degeneration characterized by MRI, X-ray, and histology. Spine. 2005 30 : 15 24.
115. Cotterill PC, Kostuik JP, D'Angelo G, Fernie GR, Maki BE. An anatomical comparison of the human and bovine thora-columbar spine. J Orthop Res. 1986 4 : 298 303.
116. Lim TH, Goel VK, Weinstein JN, Kong W. Stress analysis of a canine spinal motion segment using the finite element technique. J Biomech. 1994 27 : 1259 69.
117. Wilke HJ, Kettler A, Wenger KH, Claes LE. Anatomy of the sheep spine and its comparison to the human spine. Anat Rec. 1997 247 : 542 55.
118. Hunter CJ, Matyas JR, Duncan NA. Cytomorphology of notochordal and chondrocytic cells from the nucleus pulposus: a species comparison. J Anat. 2004 205 : 357 62.
119. PEACOCK A. Observations on the postnatal structure of the intervertebral disc in man. J Anat. 1952 86 : 162 79.
120. Aguiar DJ, Johnson SL, Oegema TR. Notochordal cells interact with nucleus pulposus cells: regulation of proteoglycan synthesis. Exp Cell Res. 1999 246 : 129 37.
121. Hunter CJ, Matyas JR, Duncan NA. The three-dimensional architecture of the notochordal nucleus pulposus: novel observations on cell structures in the canine intervertebral disc. JAnat. 2003 202 : 279 91.
122. Hoogendoorn RJ, Wuisman P, Smit TH, Everts VE, Helder MN. Experimental Intervertebral Disc Degeneration induced by Chondroitinase ABC in the Goat. Spine. 2007 32 : 1816 25.
123. Meisel HJ, Ganey T, Hutton WC, Libera J, Minkus Y, Alasevic O. Clinical experience in cell-based therapeutics: intervention and outcome. Eur Spine J. 2006 15 : S397 05.
124. Meisel HJ. Siodla V, Ganey T. Minkus Y. Hutton WC. Alasevic OJ. Clinical experience in cell-based therapeutics: disc chondrocyte transplantation A treatment for degenerated or damaged intervertebral disc. BiomolEng. 2007 24 : 5 21.
125. Nishimura K, Mochida J. Percutaneous reinsertion of the nucleus pulposus. An experimental study. Spine. 1998 23 : 1531 8.
126. Okuma M. Mochida J, Nishimura K. Sakabe K, Seiki K. Reinsertion of stimulated nucleus pulposus cells retards intervertebral disc degeneration: an in vitro and in vivo experimental study. J Orthop Res. 2000 18 : 988 97.
127. Noel D. Gazit D. Bouquet C. Apparailly F. Bony C. Plence P. Millet V, Turgeman G. Perricaudet M. Sany J, Jorgensen C. Short-term BMP-2 expression is sufficient for in vivo osteochondral differentiation of mesenchymal stem cells. Stem Cells. 2004 22 : 74 85.
128. Yang M. Ma QJ. Dang GT. Ma K. Chen P. Zhou CY. in vitro and in vivo induction of bone formation based on ex vivo gene therapy using rat adipose-derived adult stem cells expressing BMP-7. Cytotherapy. 2005 7 : 273 81.
129. Bhardwaj R, Midha R. Synchronous lumbar disc herniation in adult twins. Case report. Can J Neurol Sci. 2004 31 : 554 7.
130. Jim JJ. Noponen-Hietala N. Cheung KM, Ott J, Karppinen J, Sahraravand A, Luk KD. Yip SP Sham PC, Song YQ. Leong JC. Cheah KS. Ala-Kokko L. Chan D. The TRP2 allele of C0L9A2 is an age-dependent risk factor for the development and severity of intervertebral disc degeneration. Spine. 2005 30 : 2735 42.
131. Sethe S. Scutt A, Stolzing A. Aging of mesenchymal stem cells. Ageing Res Rev. 2006 5 : 91 116.
132. Nomura T. Mochida J, Okuma M. Nishimura K. Sakabe K. Nucleus pulposus allograft retards intervertebral disc degeneration. Clin Orthop Relat Res. 2001 94 101.
133. Liu H. Kemeny DM, Heng BC. Ouyang HW. Melentlez AJ. Cao T. The immunogenicity and immunomodulatory function of osteogenic cells differentiated from mesenchymal stem cells. J Immunol. 2006 176 : 2864 71.
134. Ryan JM, Barry FP. Murphy JM, Mahon BP. Mesenchymal stem cells avoid allogeneic rejection. J Inflamm. 2005 2 : 8.
135. Zhang YG. Guo X, Xu P. Kang LL. Li J. Bone mesenchymal stem cells transplanted into rabbit intervertebral discs can increase proteoglycans. Clin Orthop Relat Res. 2005 219 26.
136. Homer HA, Roberts S, Bielby RC, Menage J, Evans H, Urban JP. Cells from different regions of the intervertebral disc: effect of culture system on matrix expression and cell phenotype. Spine. 2002 27 : 1018 28.
137. Chiba K, Andersson GB, Masuda K, Thonar EJ. Metabolism of the extracellular matrix formed by intervertebral disc cells cultured in alginate. Spine. 1997 22 : 2885 93.
138. Urban JP, Smith S, Fairbank JC. Nutrition of the intervertebral disc. Spine. 2004 29 : 2700 9.
139. Ruan D, He Q, Ding Y, Hou L, Li J, Luk KD. Intervertebral disc transplantation in the treatment of degenerative spine disease: a preliminary study. Lancet. 2007 369 : 993 9.
140. Nomura T, Mochida J, Okuma M, Nishimura K, Sakabe K. Nucleus pulposus allograft retards intervertebral disc degeneration. Clin Orthop Relat Res. 2001 94 101.
141. Parson A. The long journey from stem cells to medical product. Cell. 2006 125 : 9 11.
142. Halme DG, Kessler DA. FDA regulation of stem-cell-based therapies. N Engl J Med. 2006 355 : 1730 5.