A phenotypic comparison of proteoglycan production of intervertebral disc cells isolated from rats, rabbits, and bovine tails; Which animal model is most suitable to study tissue engineering and biological repair of human disc disorders?

Tissue Engineering - Part A

Volumn 15, Issue 12, 2009, Pages 3835-3846

  Miyazaki, Tsuyoshi ^a   Kobayashi, Shigeru ^a,b   Takeno, Kenichi ^a   Meir, Adam ^b   Urban, Jill ^b   Baba, Hisatoshi ^a  

^a UNIVERSITY OF FUKUI   (Japan)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BIOCHEMISTRY; CELLS; IMPLANTS (SURGICAL); METABOLISM; MODELS; RATS; THREE DIMENSIONAL; TISSUE ENGINEERING;

ANIMAL MODEL; CARTILAGINOUS TISSUES; CELL TYPES; CELLS OF RATS; CHONDROCYTES; CHONDROCYTIC; ENERGY METABOLISM; GLYCOSAMINOGLYCANS; HUMAN DISC; INTERVERTEBRAL DISCS; MATRIX COMPONENTS; METABOLIC ACTIVITY; NUCLEUS PULPOSUS; PROTEOGLYCANS; THREE-DIMENSIONAL CULTURE SYSTEM;

CELL CULTURE;

GLYCOSAMINOGLYCAN; PROTEOGLYCAN;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL ISOLATION; CELL STRUCTURE; CELL TYPE; CONTROLLED STUDY; COW; INTERVERTEBRAL DISK; INTERVERTEBRAL DISK DISEASE; MALE; NONHUMAN; NUCLEUS PULPOSUS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN METABOLISM; RABBIT; RAT; TISSUE ENGINEERING;

ANIMALIA; BOS; BOVINAE; ORYCTOLAGUS CUNICULUS; RATTUS;

EID: 72049125623     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2009.0250     Document Type: Article

References (102)

1. Keys, D.C., and Compere, E.L. The normal and pathological physiology of the nucleus pulposus of the intervertebral disc. An anatomical, clinical and experimental study. J Bone Joint Surg 14, 897, 1932.
2. Peacock, A. Observations on the pre-natal sturucture of the intervertebral disc in man. J Anat 85, 260, 1951.
3. Walmsley, R. The development and growth of the inter-vertebral disc. Edinb Med J 60, 341, 1953.
4. Verbout, A.J. The development of the vertebral column. Adv Anat Embryol Cell Biol 90, 80, 1985.
5. Taylor, J.R., and Twomey, L.T. The development of human intervertebral disc. In: Ghosh, P., ed. The Biology of the In-tervertebral Disc. Boca Raton, FL: CRC Press, 1988, pp. 39-82.
6. Coventry, M.B., Ghormley, P.K., and Kernohan, J.W. The intervertebral disc: its microscopic anatomy and pathology. Part I. Anatomy, development and physiology. J Bone Joint Surg 27, 105, 1945.
7. Peacock, A. Obsevations on the postnatal development of the intervertebral disc in man. J Anat 86, 34, 1952.
8. Smith, N.R. The intervertbral discs. Br J Surg 18, 358, 1930.
9. von Luschka, H. Die Halbgelenke des Menschlichen Kör-pers. Berlin: G. Reimer, 1858, pp. 1-144.
10. Hansen, H.J. Comparative views on the pathology of disc degeneration in animals. Lab Invest 8, 1242, 1959.
11. Bulter, W.F. Comparative anatomy and development of the mammalian disc. In: Ghosh, P., ed. The Biology of the Inter-vertebral Disc. Boca Raton, FL: CRC Press, 1988, pp. 84-108.
12. Carlier, E.W. The fate of the notochord and development of the intervertebral disc in the sheep, with observations on the structure of the adult disc in these animals. J Anat Phys 24, 573, 1890.
13. Hansen, H.J. A pathologic-anatomical study on disc degeneration in the dogs: with special reference to the so-called enchondrosis intervertebralis. Acta Orthop Scand 11(Suppl), 1, 1952.
14. Braund, K.G., Ghosh, P., Taylor, T.K.F., and Larsen, L.H. Morphological studies of the canine intervertebral disc: the assignment of the beagle to the achondroplastic classification. Res Vet Sci 19, 167, 1975.
15. Berry, R.J. Genetically controlled degeneration of the nucleus pulposus in the mouse. J Bone Joint Surg 43B, 387, 1961.
16. Williams, E.W. The latter development of the notochord in mammals. Am J Anat 8, 251, 1908.
17. Souter, W.A., and Taylar, T.K.F. Sulphated acid muco-polysaccharide metabolism in the rabbit intervertebral disc. J Bone Joint Surg 52B, 371, 1970.
18. Scott, N.A., Harris, P.F., and Bagnall, K.M. A morphological and histological study of the postnatal development of the intervertebral discs in the lumbar spine of the rabbit. J Anat 130, 75, 1980.
19. Butler, W.F., and Smith, R.W. Age change in the nucleus pulposus of the nonruptured intervertebral disc of the cat. Res Vet Sci 8, 151, 1967.
20. Hunter, C.J., Matyas, J.R., and Duncan, N.A. The three-dimensional architecture of the notochordal nucleus pul-posus: novel observations on cell structures in the canine intervertebral disc. J Anat 202, 279, 2003.
21. Alini, M., Roughley, P.J., Antoniou, J., Stoll, T., and Aebi, M. A biological approach to treating disc degeneration: not for today, but maybe for tomorrow. Eur Spine J 11 (2 Suppl), S215, 2002.
22. Ganey, T.M., and Meisel, H.J. A potential role for cell-based therapeutics in the treatmant of intervertebral disc hernia-tion. Eur Spine J 11, S206, 2002.
23. Masuda, K., Oegema, T.R., Jr., and An, H.S. Growth factors and treatment of intervertebral disc degeneration. Spine 29, 2757, 2004.
24. Shimer, A.L., Chadderdon, R.C., Gilbertson, L.G., and Kang, J.D. Gene therapy approaches for intervertebral disc degeneration. Spine 29, 2770, 2004.
25. Brisby, H., Tao, H., Ma, D.D., and Diwan, A.D. Cell therapy for disc degeneration. Potentials and pitfalls. Orthop Clin North Am 35, 85, 2004.
26. Richardson, S.M., Mobasheri, A., Freemont, A.J., and Hoyland, J.A. Intervertebral disc biology, degeneration and novel tissue engineering and regenerative medicine therapies. Histol Histopathol 22, 1033, 2007.
27. O'Halloran, D.M., and Pandit, A.S. Tissue-engineering approach to regenerating the intervertebral disc. Tissue Eng 13, 1927, 2007.
28. Sebastine, I.M., and Williams, D.J. Current developments in tissue engineering of nucleus pulposus for the treatment of intervertebral disc degeneration. Conf Proc IEEE Eng Med Biol Soc 2007, 6401, 2007.
29. Kalson, N.S., Richardson, S.M., and Hoyland, J.A. Strategies for regeneration of the intervertebral disc. Regen Med 3, 717, 2008.
30. Walsh, A.L., Lotz, J., and Bradford, D. Single and multiple injections of GDF-5, IGF-1, or TGF beta into degenerated intervertebral discs. Orthop Res Soc Trans 27, 820, 2002.
31. Yoon, S.T., Kim, K.S., Li, J., Park, J.S., Akamaru, T., Elmer, W.A., and Hutton, W.C. The effect of bone morphogenetic protein-2 on rat intervertebral disc cells in vitro. Spine 28, 1773, 2003.
32. Risbud, M.V., Izzo, M.W., Adams, C.S., Arnold, W.W., Hillibrand, A.S., Vresilovic, E.J., Vaccaro, A.R., Albert, T.J., and Shapiro, I.M. An organ culture system for the study of the nucleus pulposus: description of the system and evaluation of the cells. Spine 28, 2652, 2003.
33. Nishida, K., Kang, J.D., Gilbertson, L.G., Moon, S.H., Suh, J.K., Vogt, M.T., Robbins, P.D., and Evans, C.H. 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 24, 2419, 1999.
34. Okuma, M., Mochida, J., Nishimura, K., Sakabe, K., and Seiki, K. Reinsertion of stimulated nucleus pulposus cells retards intervertebral disc degeneration: an in vitro and in vivo experimental study. J Orthop Res 18, 988, 2000.
35. Kroeber, M.W., Unglaub, F., Wang, H., Schmid, C., Thomsen, M., Nerlich, A., and Richter, W. New in vivo animal model to create intervertebral disc degeneration and to investigate the effects of therapeutic strategies to stimulate disc regeneration. Spine 27, 2684, 2002.
36. Yoon, S.T., Li, J., Kim, K.S., Park, J.S., and Hutton, W. BMP-2 stimulates disc cell matrix production and other BMPs. Spine J 3, 144S, 2003.
37. Masuda, K., Takegami, K., An, H., Kumano, F., Chiba, K., Andersson, G.B.J., Schmid, T., and 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 21, 922, 2003.
38. An, H., Takegami, K., Kamada, H., Nguten, C.M., Thonar, E.J-M.A., Singh, K., Andersson, G.B., and Masuda, K. In-tradiscal administration of osteogenic protein-1 increases intervertebral disc height and proteoglycan content in the nucleus pulposus in normal adolescent rabbits. Spine 30, 25, 2005.
39. Sakai, D., Mochida, J., Iwashina, T., Hiyama, A., Omi, H., Imai, M., Nakai, T., Ando, K., and Hotta, T. Regenerative effects of transplanting mesenchymal stem cells embedded in atelocollagen to the degenerated intervertebral disc. Biomaterials 27, 335, 2006.
40. Iwashina, T., Mochida, J., Sakai, D., Yamamoto, Y., Miya-zaki, T., Ando, K., and Hotta, T. Feasibility of using a human nucleus pulposus cell line as a cell source in cell transplantation therapy for intervertebral disc degeneration. Spine 31, 1177, 2006.
41. Baer, A.E., Wang, J.Y., Kraus, V.B., and Setton, L.A. Collagen gene expression and mechanical properties of intervertebral disc cell-alginate cultures. J Orthop Res 19, 2, 2001.
42. Chen, J., Yan, W., and Setton, L.A. Static compression induces zonal-specific changes in gene expression for extracellular matrix and cytoskeletal proteins in intervertebral disc cells in vitro. Matrix Biol 22, 573, 2004.
43. Thompson, J.P., Oegema, T.J., and Bradford, D.S. Stimulation of mature canine intervertebral disc by growth factors. Spine 16, 253, 1991.
44. Ganey, T., Libera, J., Moos, V., Alasevic, O., Fritsch, K.G., Meisel, H.J., and Hutton, W.C. Disc chondrocyte transplantation in a canine model: a treatment for degenerated or damaged intervertebral disc. Spine 28, 2609, 2003.
45. Hohaus, C., Ganey, T.M., Minkus, Y., and Meisel, H.J. Cell transplantation in lumbar spine disc degeneration disease. Eur Spine J 17, 492, 2008.
46. Sun, Y., Hurtig, M., Pilliar, R.M., Grynpas, M., and Kandel, R.A. Characterization of nucleus pulposus-like tissue formed in vitro. J Orthop Res 19, 1078, 2001.
47. Mizuno, H., Roy, A.K., Vacanti, C.A., Kojima, K., Ueda, M., and Bonassar, L.J. Tissue-engineered composites of annulus fibrosus and nucleus pulposus for intervertebral disc replacement. Spine 29, 1290, 2004.
48. Osada, R., Ohshima, H., Ishihara, H., Yudoh, K., Sakai, K., Matsui, H., and Tsuji, H. 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, 1996.
49. Matsumoto, T., Masuda, K., An, H., Chen, S., Williamson, A., Sah, R., Andersson, G., Rueger, D., and Thonar, E. Formation of transplantable disc-shaped tissues by nucleus pulposus and annulus fibrosus cells: biochemical and bio-mechanical properties. Orthop Res Soc Trans 26, 897, 2001.
50. Alini, M., Li, W., Markovic, P., Aebi, M., Spiro, R.C., and Roughley, P.J. The potential and limitations of a cell-seeded collagen/hyaluronan scaffold to engineer an intervertebral disc-like matrix. Spine 28, 446, 2003.
51. Hamilton, D.J., Séguin, C.A., Wang, J., Pilliar, R.M., and Kandel, R.A. Formation of a nucleus pulposus-cartilage endplate construct in vitro. Biomaterials 27, 397, 2005.
52. Alini, M., Eisenstein, S.M., Ito, K., Little, C., Kettler, A.A., Masuda, K., Melrose, J., Ralphs, J., Stokes, I., and Wilke, H.J. Are animal models useful for studing human disc disorders/degeneration? Eur Spine J 17, 2, 2008.
53. Hunter, C.J., Matyas, J.R., and Duncan, N.A. The noto-chordal cell in the nucleus pulposus: a review in the content of tissue engineering. Tissue Eng 9, 667, 2003.
54. Holm, S., Maroudas, A., Urban, J.P., and Nachemson, A. Nutrition of the intervertebral disc: solute transport and metabolism. Connect Tissue Res 8, 101, 1981.
55. Lee, R.B., and Urban, J.P. Evidence for a negative Pasteur effect in articular cartilage. Biochem J 321, 95, 1997.
56. Farndale, R.W., Buttle, D.J., and Barrett, A.J. An improved quantitation and discrimination of sulphated glycosami-noglycans by use of the dye dimethylmethylene blue. Bio-chem Biophys Acta 883, 173, 1986.
57. Trout, J.J., Buckwalter, J.A., Moore, K.C., and Landas, S.K. Ultrastructure of the human intervertebral disc. I. Changes in notochordal cells with age. Tissue Cell 14, 359, 1982.
58. Trout, J.J., Buckwalter, J.A., and Moore, K.C. Ultrastructure of the human intervertebral disc. II. Cells of the nucleus pulposus. Anat Rec 204, 307, 1982.
59. Happy, F., and Bradford, A.G.J. Preliminary observations concerning the fine structure of the intervertebral disc. J Bone Joint Surg 46B, 563, 1964.
60. Happy, F., Pearson, C.H., Naylor, A., and Turner, R.L. The aging of the human intervertebral disc. Gerontologia 15, 174, 1969.
61. Adler, J.H., Schoenbaum, M., and Silberberg, R. Early onset of disk degeneration and spondylosis in sand rats (Psammomys cbesus). Vet Pathol 20, 13, 1983.
62. Moskowitz, R.W., Ziv, I., Denko, C.W., Boja, B., Jones, P.K., and Adler, J.H. Spondylosis in sand rats: a model of in-tervertebral disc degeneration and hyperostosis. J Orthop Res 8, 40, 1990.
63. Smith, J.W., and Serafini-Fracassini, A. The distribution of the protein-polysaccaride complex in the nucleus pulposus matrix in young rabbits. J Cell Sci 3, 33, 1968.
64. Kobayashi, S., Baba, H., Takeno, K., Miyazaki, T., Uchida, K., Kokubo, Y., Nomura, E., Morita, C., Yoshizawa, H., and Adam, M. Fine structure of catilage canal and vascular buds in the vertebral end-plate. J Neurosurg Spine 9, 96, 2008.
65. Lawrence, T.E., Whatley, J.D., Montgomery, T.H., and Perino, L.J. A comparison of the USDA ossification-based maturity system to a system based on dentition. J Anim Sci 79, 1683, 2001.
66. Hansen, H.J. Studies on the pathology of the lumbosacral disc in female cattle. Acta Orthop Scand 25, 161, 1956.
67. Maroudas, A., Stockwell, R.A., Nachenson, A., and Urban, J. Factors involved in the nutrition of the human lumbar intervertebral disc: cellularity and diffision of glucose in vitro. J Anat 120, 113, 1975.
68. Race, A., Broom, N.D., and Robertson, P. Effect of loading rate and hydration on the mechanical properties of the disc. Spine 25, 662, 2000.
69. Ohshima, H., Ishihara, H., Urban, J.P., and Tsuji, H. The use of coccygeal discs to study intervertebral disc metabolism. J Orthop Res 11, 332, 1993.
70. Ishihara, H., McNally, D.S., Urban, J.P., and Hall, A.C. Effects of hydrostatic pressure on matrix synthesis in different regions of the intervertebral disk. J Appl Physiol 80, 839, 1996.
71. Ohshima, H., Urban, J.P.G., and Bergel, D.H. Effect of static load on matrix synthesis rates in the intervertebral disc measured in vitro by a new perfusion technique. J Orthop Res 13, 22, 1995.
72. Roberts, S., Menage, J., Duance, V., and Wotton, S.F. Collagen types around the cells of the intervertbral disc and cartilage end plate: an imminolocalization study. Spine 16, 1030, 1991.
73. Kim, K.W., Lim, T.H., Lim, J.G., Jeong, S.T., Masuda, K., and An, H.S. The origin of chondrocytes in the nucleus pulposus and histologic findings associated with the transition of a notochordal nucleus pulposus to a fibro-cartolagious nucleus pulposus in intact rabbit interverte-bral discs. Spine 28, 982, 2003.
74. Grodzinsky, A.J. Electromechanical and physicochemical properties of connective tissue. Crit Rev Biomed Eng 9, 133, 1983.
75. Maroudas, A., and Bannon, C. Measurement of swelling pressure in cartilage and comparison with the osmotic pressure of constituent proteoglycans. Biorheology 18, 619, 1981.
76. Kempson, G.E., Muir, H., Swanson, S.A., and Freeman, M.A.R. Correlations between stiffness and the chemical constituents of cartilage on the human femoral head. Bio-chim Biophys Acta 215, 70, 1970.
77. Treppo, S., Koepp, H., Quan, E.C., Cole, A.A., Kuettner, K.E., and Grodzinsky, A.J. Comparison of biomechanical and biochemical properties of cartilage from human knee and ankle pairs. J Orthop Res 18, 739, 2000.
78. Adams, M.A., and Hutton, W.C. Prolapsed intervertebral disc. A hyperflexion injury. Spine 7, 184, 1982.
79. Cole, T.C., Buckhardt, D., Frost, L., and Gosh, P. The pro-teoglycans of the canine intervertebral disc. Biochim Bio-phys Acta 829, 127, 1985.
80. Gage, E.D. Incidence of clinical disc disease in the dog. J Am Anim Hosp Assoc 11, 135, 1975.
81. Priester, W.A. Canine intervertebral disc disease: occurrence by age, breed, and sex among 8117 cases. Theriogenology 6, 293, 1976.
82. Bayliss, M.T., Johnstone, B., and O'Brien, J.P. Proteoglycan synthesis in the human intervertebral disc. Variation with age, region and pathology. Spine 13, 972, 1988.
83. Johnstone, B., and Bayliss, M.T. The large proteoglycan of the human intervertebral disc. Changes in their biosynthesis and structure with age, topography, and pathology. Spine 20, 674, 1995.
84. Aguiar, D.J., Johnson, S.L., and Oegema, T.R. Notochordal cells interact with nucleus pulposus cells: regulation of proteoglycan synthesis. Exp Cell Res 246, 129, 1999.
85. Cappello, R., Bird, J.L.E., Pfeiffer, D., Bayliss, M.T., and Dudhia, J. Notochordal cell produce and assemble extracellular matrix in a distinct manner, which may be responsible for the maintenance of healthy nucleus pulposus. Spine 31, 873, 2006.
86. Erwin, W.M., and Inman, R.D. Notochord cells regulate intervertebral disc chondrocyte proteoglycan production and cell proliferation. Spine 31, 1094, 2006.
87. Urban, J.P.G., and Roberts, S. Development and degeneration of the intervertebral discs. Mol Med Today 1, 329, 1995.
88. Roughley, P.J. Biology of intervertebral disc aging and degeneration: involvement of the extracellular matrix. Spine 29, 2691, 2004.
89. Verzijl, N., DeGoot, J., Thorpe, S.R., Bank, R.A., Shaw, J.N., Lyors, T.J., Bijlsma, J.W., Lafeber, F.P., Baynes, J.W., and TeKoppele, J.M. Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem 275, 39027, 2000.
90. Bibby, S.R., Jones, D.A., Ripley, R.M., and Urban, J. 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 30, 487, 2005.
91. Urban, J.P.G., and Maroudas, A. Measurement of fixed charge density in the vertebral disc. Biochem Biophys Acta 586, 166, 1979.
92. Maroudas, A. Metabolism of cartilaginous tissue, a quantitative approach. In: Maroudas, A., and Holborow, J., eds. Studies in Joint Disease 1. London: Pitman Medical, 1981, pp. 59-86.
93. Ishihara, H., Warensjo, K., Roberts, S., and Urban, J.P. Pro-teoglycan synthesis in the intervertebral disk nucleus: the role of extracellular osmolality. Am J Physiol 272, C1499, 1997.
94. Takeno, K., Kobayashi, S., Negoro, K., Uchida, K., Miyazaki, T., Yayama, T., Shimada, S., and Baba, H. Physical limitations to tissue engineering of intervertabral disc cells: effect of extracellular osmotic change on glycosaminoglycan production and cell metabolism. J Neurosurg Spine 7, 637, 2007.
95. Negoro, K., Kobayashi, S., Taneno, K., Uchida, K., and Baba, H. Effect of osmolarity on glycosaminoglycan production and cell metabolism of articular chondrocyte under three dimensional culture system. Clin Exp Rheumatol 26, 527, 2008.
96. Ohshima, H., and Urban, J.P.G. The effect of lactate and pH on proteoglycan and protein synthesis rates in the inter-vertebral disc. Spine 17, 1079, 1992.
97. Razaq, S., Wilkins, R.J., and Urban, J.P.G. The effect of extracellular pH on matrix turnover by cells of the bovine nucleus pulposus. Eur Spine J 13, 685, 2004.
98. Nachemson, A., Lewin, T., Maroudas, A., and Freeman, M.A.F. In vitro diffusion of dye through the end-plates and annulus fibrosus of human lumbar intervertebral discs. Acta Orthop Scand 41, 589, 1970.
99. Rajasekaran, S., Babu, J.N., Arun, R., Armstrong, B.R.W., Shetty, A.P., and Murugan, S. A study of diffusion in human lumbar discs: a serial magnetic resonance imaging study documenting the influence of the endplate on diffusion in normal and degenerate discs. Spine 29, 2654, 2004.
100. Kobayashi, S., Meir, A., and Urban, J. Effect of cell density on the rate of glycosaminoglycan accumulation by disc and cartilage cells in vitro. J Orthop Res 26, 493, 2008.
101. Boden, S.D., McCowin, P.R., Davis, D.O., Dina, T.S., Mark, A.S., and Wiesel, S. Abnormal magnetic-resonance scans of the cervical spine in asymptomatic subjects. A prospective investigation. J Bone Joint Surg 72A, 1178, 1990.
102. Jensen, M.C., Brant-Zawadzki, M.N., Obuchowski, N., Modic, M.T., Malkasian, D., and Ross, J.S. Magnetic resonance imaging of the lumbar spine in people without back pain. N Engl J Med 331, 69, 1994.