Silk-fibrin/hyaluronic acid composite gels for nucleus pulposus tissue regeneration

Tissue Engineering - Part A

Volumn 17, Issue 23-24, 2011, Pages 2999-3009

  Park, Sang Hyug ^a   Cho, Hongsik ^b   Gil, Eun Seok ^a   Mandal, Biman B ^a   Min, Byoung Hyun ^c,d   Kaplan, David L ^a  

^a Tufts University   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c Ajou University School of Medicine   (South Korea)

^d Ajou University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; BODY FLUIDS; CARTILAGE; GELS; MECHANICAL PROPERTIES; SILK; TISSUE; TISSUE CULTURE;

BIOLOGICAL EVALUATION; CARTILAGE FORMATION; CELLULAR DIFFERENTIATION; CHONDROGENIC; CHONDROGENIC DIFFERENTIATION; COMBINED FEATURES; COMPOSITE GELS; HISTOLOGICAL EXAMINATION; HUMAN CHONDROCYTES; IN-VITRO; MIXED GEL; NO REDUCTION; NUCLEUS PULPOSUS; REGENERATIVE MEDICINE; STUDY GROUPS; THREE-DIMENSIONAL ENVIRONMENT; TISSUE ENGINEERED CARTILAGE; TISSUE REGENERATION;

SCAFFOLDS (BIOLOGY);

COLLAGEN; FIBRIN; GLYCOSAMINOGLYCAN; HYALURONIC ACID; MESSENGER RNA;

ANIMAL; ARTICLE; CELL DIFFERENTIATION; CELL SHAPE; CELL SURVIVAL; CHONDROGENESIS; DRUG EFFECT; GEL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; INFRARED SPECTROSCOPY; INTERVERTEBRAL DISK; MATERIALS TESTING; MECHANICS; METABOLISM; METHODOLOGY; PHYSIOLOGY; REGENERATION; SILK; TISSUE REGENERATION;

ANIMALS; CELL DIFFERENTIATION; CELL SHAPE; CELL SURVIVAL; CHONDROGENESIS; COLLAGEN; FIBRIN; GELS; GENE EXPRESSION REGULATION; GLYCOSAMINOGLYCANS; GUIDED TISSUE REGENERATION; HUMANS; HYALURONIC ACID; IMMUNOHISTOCHEMISTRY; INTERVERTEBRAL DISC; MATERIALS TESTING; MECHANICAL PHENOMENA; REGENERATION; RNA, MESSENGER; SILK; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 82355171778     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2010.0747     Document Type: Article

References (65)

1. Ehrlich, G.E. Low back pain. Bull World Health Organ 81, 671, 2003.
2. Kelsey, J.L., and White, A.A., 3rd. Epidemiology and impact of low-back pain. Spine (Phila Pa 1976) 5, 133, 1980.
3. Gan, J.C., Ducheyne, P., Vresilovic, E.J., Swaim, W., and Shapiro, I.M. Intervertebral disc tissue engineering I: characterization of the nucleus pulposus. Clin Orthop Relat Res (411), 305, 2003.
4. Kitahara, H. Histochemical study of the human intervertebral disc. Nippon Seikeigeka Gakkai Zasshi 53, 817, 1979.
5. 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 (Phila Pa 1976) 28, 2652, 2003.
6. Gruber, H.E., and Hanley, E.N., Jr. Biologic strategies for the therapy of intervertebral disc degeneration. Expert Opin Biol Ther 3, 1209, 2003.
7. Hubbell, J.A. Materials as morphogenetic guides in tissue engineering. Curr Opin Biotechnol 14, 551, 2003.
8. Drury, J.L., and Mooney, D.J. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24, 4337, 2003.
9. Boyd, L.M., and Carter, A.J. Injectable biomaterials and vertebral endplate treatment for repair and regeneration of the intervertebral disc. Eur Spine J 15 Suppl 3, S414, 2006.
10. Sakai, D., Mochida, J., Yamamoto, Y., Nomura, T., Okuma, M., Nishimura, K., Nakai, T., Ando, K., and Hotta, T. Transplantation of mesenchymal stem cells embedded in Atelocollagen gel to the intervertebral disc: a potential therapeutic model for disc degeneration. Biomaterials 24, 3531, 2003.
11. Sakai, D., Mochida, J., Iwashina, T., Watanabe, T., Suyama, K., Ando, K., and Hotta, T. Atelocollagen for culture of human nucleus pulposus cells forming nucleus pulposuslike tissue in vitro: influence on the proliferation and proteoglycan production of HNPSV-1 cells. Biomaterials 27, 346, 2006.
12. Mizuno, H., Roy, A.K., Zaporojan, V., Vacanti, C.A., Ueda, M., and Bonassar, L.J. Biomechanical and biochemical characterization of composite tissue-engineered intervertebral discs. Biomaterials 27, 362, 2006.
13. Mwale, F., Iordanova, M., Demers, C.N., Steffen, T., Roughley, P., and Antoniou, J. Biological evaluation of chitosan salts cross-linked to genipin as a cell scaffold for disk tissue engineering. Tissue Eng 11, 130, 2005.
14. Sha'ban, M., Yoon, S.J., Ko, Y.K., Ha, H.J., Kim, S.H., So, J.W., Idrus, R.B., and Khang, G. Fibrin promotes proliferation and matrix production of intervertebral disc cells cultured in three-dimensional poly(lactic-co-glycolic acid) scaffold. J Biomater Sci Polym Ed 19, 1219, 2008.
15. Gruber, H.E., Leslie, K., Ingram, J., Norton, H.J., and Hanley, E.N. Cell-based tissue engineering for the intervertebral disc: in vitro studies of human disc cell gene expression and matrix production within selected cell carriers. Spine J 4, 44, 2004.
16. Cloyd, J.M., Malhotra, N.R., Weng, L., Chen, W., Mauck, R.L., and Elliott, D.M. Material properties in unconfined compression of human nucleus pulposus, injectable hyaluronic acid-based hydrogels and tissue engineering scaffolds. Eur Spine J 16, 1892, 2007.
17. Kogan, G., Soltes, L., Stern, R., and Gemeiner, P. Hyaluronic acid: a natural biopolymer with a broad range of biomedical and industrial applications. Biotechnol Lett 29, 17, 2007.
18. Broberg, K.B. On the mechanical behaviour of intervertebral discs. Spine (Phila Pa 1976) 8, 151, 1983.
19. Park, S.H., Cui, J.H., Park, S.R., and Min, B.H. Potential of fortified fibrin/hyaluronic acid composite gel as a cell delivery vehicle for chondrocytes. Artificial organs 33, 439, 2009.
20. Park, S.H., Park, S.R., Chung, S.I., Pai, K.S., and Min, B.H. Tissue-engineered cartilage using fibrin/hyaluronan composite gel and its in vivo implantation. Artif Organs 29, 838, 2005.
21. Chou, C.H., Cheng, W.T., Kuo, T.F., Sun, J.S., Lin, F.H., and Tsai, J.C. Fibrin glue mixed with gelatin/hyaluronic acid/chondroitin-6-sulfate tri-copolymer for articular cartilage tissue engineering: the results of real-time polymerase chain reaction. J Biomed Mater Res A 82, 757, 2007.
22. Peretti, G.M., Randolph, M.A., Zaporojan, V., Bonassar, L.J., Xu, J.W., Fellers, J.C., and Yaremchuk, M.J. A biomechanical analysis of an engineered cell-scaffold implant for cartilage repair. Ann Plast Surg 46, 533, 2001.
23. Seda Tigli, R., Ghosh, S., Laha, M.M., Shevde, N.K., Daheron, L., Gimble, J., Gumusderelioglu, M., and Kaplan, D.L. Comparative chondrogenesis of human cell sources in 3D scaffolds. J Tissue Eng Regen Med 3, 348, 2009.
24. Kim, H.J., Kim, U.J., Kim, H.S., Li, C., Wada, M., Leisk, G.G., and Kaplan, D.L. Bone tissue engineering with premineralized silk scaffolds. Bone 42, 1226, 2008.
25. Altman, G.H., Diaz, F., Jakuba, C., Calabro, T., Horan, R.L., Chen, J., Lu, H., Richmond, J., and Kaplan, D.L. Silk-based biomaterials. Biomaterials 24, 401, 2003.
26. Altman, G.H., Horan, R.L., Lu, H.H., Moreau, J., Martin, I., Richmond, J.C., and Kaplan, D.L. Silk matrix for tissue engineered anterior cruciate ligaments. Biomaterials 23, 4131, 2002.
27. Wang, X., Kluge, J.A., Leisk, G.G., and Kaplan, D.L. Sonication-induced gelation of silk fibroin for cell encapsulation. Biomaterials 29, 1054, 2008.
28. Kim, U.J., Park, J., Kim, H.J., Wada, M., and Kaplan, D.L. Three-dimensional aqueous-derived biomaterial scaffolds from silk fibroin. Biomaterials 26, 2775, 2005.
29. Kim, H.J., Kim, U.J., Vunjak-Novakovic, G., Min, B.H., and Kaplan, D.L. Influence of macroporous protein scaffolds on bone tissue engineering from bone marrow stem cells. Biomaterials 26, 4442, 2005.
30. Matsumoto, A., Chen, J., Collette, A.L., Kim, U.J., Altman, G.H., Cebe, P., and Kaplan, D.L. Mechanisms of silk fibroin sol-gel transitions. J Phys Chem B 110, 21630, 2006.
31. Choi, K.H., Yoo, B.S., Park, S.R., Choi, B.H., and Min, B.H. Novel imaging analysis system to measure the spatial dimension of engineered tissue construct. Artif Organs 34, 158, 2009.
32. Whitley, C.B., Ridnour, M.D., Draper, K.A., Dutton, C.M., and Neglia, J.P. Diagnostic test for mucopolysaccharidosis. I. Direct method for quantifying excessive urinary glycosaminoglycan excretion. Clin Chem 35, 374, 1989.
33. Rosso, F., Marino, G., Giordano, A., Barbarisi, M., Parmeggiani, D., and Barbarisi, A. Smart materials as scaffolds for tissue engineering. J Cell Physiol 203, 465, 2005.
34. O'Halloran, D.M., and Pandit, A.S. Tissue-engineering approach to regenerating the intervertebral disc. Tissue Eng 13, 1927, 2007.
35. Paesold, G., Nerlich, A.G., and Boos, N. Biological treatment strategies for disc degeneration: potentials and shortcomings. Eur Spine J 16, 447, 2007.
36. Chen, W.H., Liu, H.Y., Lo, W.C., Wu, S.C., Chi, C.H., Chang, H.Y., Hsiao, S.H., Wu, C.H., Chiu, W.T., Chen, B.J., and Deng, W.P. Intervertebral disc regeneration in an ex vivo culture system using mesenchymal stem cells and plateletrich plasma. Biomaterials 30, 5523, 2009.
37. Gruber, H.E., Stasky, A.A., and Hanley, E.N., Jr. Characterization and phenotypic stability of human disc cells in vitro. Matrix Biol 16, 285, 1997.
38. Podskubka, A., Povysil, C., Kubes, R., Sprindrich, J., and Sedlacek, R. [Treatment of deep cartilage defects of the knee with autologous chondrocyte transplantation on a hya-luronic Acid ester scaffolds (Hyalograft C)]. Acta Chir Orthop Traumatol Cech 73, 251, 2006.
39. Robert, H., and Bahuaud, J. Autologous chondrocyte implantation. A review of techniques and preliminary results. Rev Rhum Engl Ed 66, 724, 1999.
40. Gorensek,M., Jaksimovic, C., Kregar-Velikonja, N., Gorensek, M., Knezevic, M., Jeras, M., Pavlovcic, V., and Cor, A. Nucleus pulposus repair with cultured autologous elastic cartilage derived chondrocytes. Cell Mol Biol Lett 9, 363, 2004.
41. Zhang, Y., Li, Z., Thonar, E.J., An, H.S., He, T.C., Pietryla, D., and Phillips, F.M. Transduced bovine articular chondrocytes affect the metabolism of cocultured nucleus pulposus cells in vitro: implications for chondrocyte transplantation into the intervertebral disc. Spine (Phila Pa 1976) 30, 2601, 2005.
42. Humzah, M.D., and Soames, R.W. Human intervertebral disc: structure and function. Anat Rec 220, 337, 1988.
43. Sive, J.I., Baird, P., Jeziorsk, M., Watkins, A., Hoyland, J.A., and Freemont, A.J. Expression of chondrocyte markers by cells of normal and degenerate intervertebral discs. Mol Pathol 55, 91, 2002.
44. Roberts, S., Menage, J., Duance, V., Wotton, S., and Ayad, S. VolvoAward in basic sciences. Collagen types around the cells of the intervertebral disc and cartilage end plate: an immunolocalization study. Spine (Phila Pa 1976) 16, 1030, 1991.
45. Tapp, H., Hanley, E.N., Jr., Patt, J.C., and Gruber, H.E. Adipose-derived stem cells: characterization and current application in orthopaedic tissue repair. Exp Biol Med (Maywood) 234, 1, 2009.
46. Hiyama, A., Mochida, J., and Sakai, D. Stem cell applications in intervertebral disc repair. Cell Mol Biol (Noisy-le-grand) 54, 24, 2008.
47. Gruber, H.E., Fisher, E.C., Jr., Desai, B., Stasky, A.A., Hoelscher, G., and Hanley, E.N., Jr. Human intervertebral disc cells from the annulus: three-dimensional culture in agarose or alginate and responsiveness to TGF-beta1. Exp Cell Res 235, 13, 1997.
48. 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 (Phila Pa 1976) 28, 446, 2003.
49. Thompson, J.P., Oegema, T.R., Jr., and Bradford, D.S. Stimulation of mature canine intervertebral disc by growth factors. Spine (Phila Pa 1976) 16, 253, 1991.
50. Leung, V.Y., Chan, D., and Cheung, K.M. Regeneration of intervertebral disc by mesenchymal stem cells: potentials, limitations, and future direction. Eur Spine J 15 Suppl 3, S406, 2006.
51. Chiba, K., Andersson, G.B., Masuda, K., and Thonar, E.J. Metabolism of the extracellular matrix formed by intervertebral disc cells cultured in alginate. Spine (Phila Pa 1976) 22, 2885, 1997.
52. Raghunath, J., Rollo, J., Sales, K.M., Butler, P.E., and Seifalian, A.M. Biomaterials and scaffold design: key to tissueengineering cartilage. Biotechnol Appl Biochem 46, 73, 2007.
53. 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.
54. Perka, C., Arnold, U., Spitzer, R.S., and Lindenhayn, K. The use of fibrin beads for tissue engineering and subsequential transplantation. Tissue Eng 7, 359, 2001.
55. Yoon, D.M., Curtis, S., Reddi, A.H., and Fisher, J.P. Addition of hyaluronic acid to alginate embedded chondrocytes interferes with IGF-1 signaling in vitro and in vivo. Tissue Eng Part A 15, 3449, 2009.
56. Perka, C., Schultz, O., Lindenhayn, K., Spitzer, R.S., Muschik, M., Sittinger, M., and Burmester, G.R. Joint cartilage repair with transplantation of embryonic chondrocytes embedded in collagen-fibrin matrices. Clin Exp Rheumatol 18, 13, 2000.
57. Buckwalter, J.A., Smith, K.C., Kazarien, L.E., Rosenberg, L.C., and Ungar, R. Articular cartilage and intervertebral disc proteoglycans differ in structure: an electron microscopic study. J Orthop Res 7, 146, 1989.
58. Chung, C., Mesa, J., Miller, G.J., Randolph, M.A., Gill, T.J., and Burdick, J.A. Effects of auricular chondrocyte expansion on neocartilage formation in photocrosslinked hyaluronic acid networks. Tissue Eng 12, 2665, 2006.
59. Kawasaki, K., Ochi, M., Uchio, Y., Adachi, N., and Matsusaki, M. Hyaluronic acid enhances proliferation and chondroitin sulfate synthesis in cultured chondrocytes embedded in collagen gels. J Cell Physiol 179, 142, 1999.
60. Crevensten, G., Walsh, A.J., Ananthakrishnan, D., Page, P., Wahba, G.M., Lotz, J.C., and Berven, S. Intervertebral disc cell therapy for regeneration: mesenchymal stem cell implantation in rat intervertebral discs. Ann Biomed Eng 32, 430, 2004.
61. Stern, S., Lindenhayn, K., Schultz, O., and Perka, C. Cultivation of porcine cells from the nucleus pulposus in a fibrin/hyaluronic acid matrix. Acta Orthop Scand 71, 496, 2000.
62. Park, S.H., Park, S.R., and Min, B.H. Reinforcement fibrinhyaluronic acid composite gel for tissue engineering cartilage genesis. Key Eng Mat 342-343, 253, 2007.
63. Eyrich, D., Brandl, F., Appel, B., Wiese, H., Maier, G., Wenzel, M., Staudenmaier, R., Goepferich, A., and Blunk, T. Long-term stable fibrin gels for cartilage engineering. Biomaterials 28, 55, 2007.
64. Numata, K., Cebe, P., and Kaplan, D.L. Mechanism of enzymatic degradation of beta-sheet crystals. Biomaterials 31, 2926, 2010.
65. Wang, Y., Kim, U.J., Blasioli, D.J., Kim, H.J., and Kaplan, D.L. In vitro cartilage tissue engineering with 3D porous aqueous-derived silk scaffolds and mesenchymal stem cells. Biomaterials 26, 7082, 2005.