The challenge and advancement of annulus fibrosus tissue engineering

European Spine Journal

Volumn 22, Issue 5, 2013, Pages 1090-1100

  Jin, Li ^a   Shimmer, Adam L ^a   Li, Xudong ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Annulus fibrosus; Intervertebral disc degeneration; Scaffolds; Tissue engineering

Indexed keywords

AGGRECAN; ATELOCOLLAGEN; COLLAGEN FIBRIL; COLLAGEN TYPE 1; COLLAGEN TYPE 2; GENIPIN; GLYCOSAMINOGLYCAN; MOLECULAR SCAFFOLD; POLYCAPROLACTONE; POLYCARBONATE; POLYURETHAN; SILK;

CELL EXPANSION; HUMAN; INTERVERTEBRAL DISK; INTERVERTEBRAL DISK DEGENERATION; MESENCHYME; NONHUMAN; PRIORITY JOURNAL; REVIEW; TISSUE ENGINEERING; TISSUE REGENERATION; TOTAL DISC REPLACEMENT;

BIOCOMPATIBLE MATERIALS; HUMANS; INTERVERTEBRAL DISC; INTERVERTEBRAL DISC DEGENERATION; REGENERATION; TISSUE ENGINEERING;

EID: 84878254276     PISSN: 09406719     EISSN: 14320932     Source Type: Journal    
DOI: 10.1007/s00586-013-2663-2     Document Type: Review

References (106)

1. Freemont TJ, LeMaitre C, Watkins A, Hoyland JA (2001) Degeneration of intervertebral discs: current understanding of cellular and molecular events, and implications for novel therapies. Expert Rev Mol Med 2001:1-10
2. Adams MA, Freeman BJ, Morrison HP, Nelson IW, Dolan P (2000) Mechanical initiation of intervertebral disc degeneration. Spine (Phila Pa 1976) 25:1625-1636
3. Mannion AF, Adams MA, Dolan P (2000) Sudden and unexpected loading generates high forces on the lumbar spine. Spine (Phila Pa 1976) 25:842-852
4. Horner HA, Urban JP (2001) Volvo award winner in basic science studies: effect of nutrient supply on the viability of cells from the nucleus pulposus of the intervertebral disc. Spine (Phila Pa 1976) 26:2543-2549
5. Brown MD, Malinin TI, Davis PB (1976) A roentgenographic evaluation of frozen allografts versus autografts in anterior cervical spine fusions. Clin Orthop Relat Res 119:231-236
6. Bibby SR, Urban JP (2004) Effect of nutrient deprivation on the viability of intervertebral disc cells. Eur Spine J 13:695-701
7. Yang X, Li X (2009) Nucleus pulposus tissue engineering: a brief review. Eur Spine J 18:1564-1572
8. Buckwalter JA (1995) Aging and degeneration of the human intervertebral disc. Spine (Phila Pa 1976) 20:1307-1314
9. Haefeli M, Elfering A, Kilian R, Min K, Boos N (2006) Nonoperative treatment for adolescent idiopathic scoliosis: A 10- to 60-year follow-up with special reference to health-related quality of life. Spine (Phila Pa 1976) 31:355-366 discussion 367
10. Anderson DG, Tannoury C (2005) Molecular pathogenic factors in symptomatic disc degeneration. Spine J 5:260S-266S
11. Anderson DG, Albert TJ, Fraser JK, Risbud M, Wuisman P, Meisel HJ, Tannoury C, Shapiro I, Vaccaro AR (2005) Cellular therapy for disc degeneration. Spine (Phila Pa 1976) 30:S14-S19
12. Kurtz SM, Devine JN (2007) PEEK biomaterials in trauma, orthopedic, and spinal implants. Biomaterials 28:4845-4869
13. Kurtz SM, Ong KL, Schmier J, Mowat F, Saleh K, Dybvik E, Karrholm J, Garellick G, Havelin LI, Furnes O, Malchau H, Lau E (2007) Future clinical and economic impact of revision total hip and knee arthroplasty. J Bone Joint Surg Am 89(Suppl 3):144-151
14. Kurtz SM, van Ooij A, Ross R, de Waal Malefijt J, Peloza J, Ciccarelli L, Villarraga ML (2007) Polyethylene wear and rim fracture in total disc arthroplasty. Spine J 7:12-21
15. Punt IM, Visser VM, van Rhijn LW, Kurtz SM, Antonis J, Schurink GW, van Ooij A (2008) Complications and reoperations of the SB charite lumbar disc prosthesis: experience in 75 patients. Eur Spine J 17:36-43
16. Serhan HA, Dooris AP, Parsons ML, Ares PJ, Gabriel SM (2006) In vitro wear assessment of the charite artificial disc according to ASTM recommendations. Spine (Phila Pa 1976) 31:1900-1910
17. Slivka MA, Spenciner DB, Seim HB 3rd, Welch WC, Serhan HA, Turner AS (2006) High rate of fusion in sheep cervical spines following anterior interbody surgery with absorbable and nonabsorbable implant devices. Spine (Phila Pa 1976) 31:2772-2777
18. Lyons G, Eisenstein SM, Sweet MB (1981) Biochemical changes in intervertebral disc degeneration. Biochim Biophys Acta 673:443-453
19. An HS, Masuda K, Cs-Szabo G, Zhang Y, Chee A, Andersson GB, Im HJ, Thonar EJ, Kwon YM (2011) Biologic repair and regeneration of the intervertebral disk. J Am Acad Orthop Surg 19:450-452
20. Cs-Szabo G, Ragasa-San Juan D, Turumella V, Masuda K, Thonar EJ, An HS (2002) Changes in mRNA and protein levels of proteoglycans of the anulus fibrosus and nucleus pulposus during intervertebral disc degeneration. Spine (Phila Pa 1976) 27:2212-2219
21. O'Halloran DM, Pandit AS (2007) Tissue-engineering approach to regenerating the intervertebral disc. Tissue Eng 13:1927-1954
22. Chan SC, Gantenbein-Ritter B (2012) Intervertebral disc regeneration or repair with biomaterials and stem cell therapy-feasible or fiction? Swiss Med Wkly 142:w13598
23. Alini M, Roughley PJ, Antoniou J, Stoll T, Aebi M (2002) A biological approach to treating disc degeneration: not for today, but maybe for tomorrow. Eur Spine J 11(Suppl 2):S215-S220
24. Nesti LJ, Li WJ, Shanti RM, Jiang YJ, Jackson W, Freedman BA, Kuklo TR, Giuliani JR, Tuan RS (2008) Intervertebral disc tissue engineering using a novel hyaluronic acid-nanofibrous scaffold (HANFS) amalgam. Tissue Eng Part A 14:1527-1537
25. Woiciechowsky C, Abbushi A, Zenclussen ML, Casalis P, Kruger JP, Freymann U, Endres M, Kaps C (2012) Regeneration of nucleus pulposus tissue in an ovine intervertebral disc degeneration model by cell-free resorbable polymer scaffolds. J Tissue Eng Regen Med [Epub ahead of print]
26. Pei M, Shoukry M, Li J, Daffner SD, France JC, Emery SE (2012) Modulation of in vitro microenvironment facilitates synovium-derived stem cell-based nucleus pulposus tissue regeneration. Spine (Phila Pa 1976) 37:1538-1547
27. Gupta MS, Cooper ES, Nicoll SB (2011) Transforming growth factor-beta 3 stimulates cartilage matrix elaboration by human marrow-derived stromal cells encapsulated in photocrosslinked carboxymethylcellulose hydrogels: potential for nucleus pulposus replacement. Tissue Eng Part A 17:2903-2910
28. Collin EC, Grad S, Zeugolis DI, Vinatier CS, Clouet JR, Guicheux JJ, Weiss P, Alini M, Pandit AS (2011) An injectable vehicle for nucleus pulposus cell-based therapy. Biomaterials 32:2862-2870
29. Mortisen D, Peroglio M, Alini M, Eglin D (2010) Tailoring thermoreversible hyaluronan hydrogels by "click" chemistry and RAFT polymerization for cell and drug therapy. Biomacromolecules 11:1261-1272
30. Peroglio M, Grad S, Mortisen D, Sprecher CM, Illien-Junger S, Alini M, Eglin D (2012) Injectable thermoreversible hyaluronan-based hydrogels for nucleus pulposus cell encapsulation. Eur Spine J 21(Suppl 6):S839-S849
31. Bowles RD, Gebhard HH, Hartl R, Bonassar LJ (2011) Tissue-engineered intervertebral discs produce new matrix, maintain disc height, and restore biomechanical function to the rodent spine. Proc Natl Acad Sci USA 108:13106-13111
32. Lazebnik M, Singh M, Glatt P, Friis LA, Berkland CJ, Detamore MS (2011) Biomimetic method for combining the nucleus pulposus and annulus fibrosus for intervertebral disc tissue engineering. J Tissue Eng Regen Med 5:e179-e187
33. Schollmeier G, Lahr-Eigen R, Lewandrowski KU (2000) Observations on fiber-forming collagens in the anulus fibrosus. Spine (Phila Pa 1976) 25:2736-2741
34. Yu J, Tirlapur U, Fairbank J, Handford P, Roberts S, Winlove CP, Cui Z, Urban J (2007) Microfibrils, elastin fibres and collagen fibres in the human intervertebral disc and bovine tail disc. J Anat 210:460-471
35. Adams P, Eyre DR, Muir H (1977) Biochemical aspects of development and ageing of human lumbar intervertebral discs. Rheumatol Rehabil 16:22-29
36. Hayes AJ, Benjamin M, Ralphs JR (2001) Extracellular matrix in development of the intervertebral disc. Matrix Biol 20:107-121
37. Hayes AJ, Smith SM, Gibson MA, Melrose J (2011) Comparative immunolocalisation of the elastin fibre associated proteins fibrillin-1, LTBP2 and MAGP-1 with components of the collagenous and proteoglycan matrix of the foetal human IVD. Spine (Phila Pa 1976) 36(21):E1365-E1372
38. Eyre DR, Muir H (1976) Types I and II collagens in intervertebral disc. interchanging radial distributions in annulus fibrosus. Biochem J 157:267-270
39. Rufai A, Benjamin M, Ralphs JR (1995) The development of fibrocartilage in the rat intervertebral disc. Anat Embryol (Berl) 192:53-62
40. Hayes AJ, Isaacs MD, Hughes C, Caterson B, Ralphs JR (2011) Collagen fibrillogenesis in the development of the annulus fibrosus of the intervertebral disc. Eur Cell Mater 22:226-241
41. Singh K, Masuda K, Thonar EJ, An HS, Cs-Szabo G (2009) Age-related changes in the extracellular matrix of nucleus pulposus and anulus fibrosus of human intervertebral disc. Spine (Phila Pa 1976) 34:10-16
42. Pattappa G, Li Z, Peroglio M, Wismer N, Alini M, Grad S (2012) Diversity of intervertebral disc cells: phenotype and function. J Anat 221(6):480-496
43. Bruehlmann SB, Rattner JB, Matyas JR, Duncan NA (2002) Regional variations in the cellular matrix of the annulus fibrosus of the intervertebral disc. J Anat 201:159-171
44. Errington RJ, Puustjarvi K, White IR, Roberts S, Urban JP (1998) Characterisation of cytoplasm-filled processes in cells of the intervertebral disc. J Anat 192(Pt 3):369-378
45. Roughley P, Hoemann C, DesRosiers E, Mwale F, Antoniou J, Alini M (2006) The potential of chitosan-based gels containing intervertebral disc cells for nucleus pulposus supplementation. Biomaterials 27:388-396
46. Clouet J, Grimandi G, Pot-Vaucel M, Masson M, Fellah HB, Guigand L, Cherel Y, Bord E, Rannou F, Weiss P, Guicheux J, Vinatier C (2009) Identification of phenotypic discriminating markers for intervertebral disc cells and articular chondrocytes. Rheumatology (Oxford) 48:1447-1450
47. Minogue BM, Richardson SM, Zeef LA, Freemont AJ, Hoyland JA (2010) Transcriptional profiling of bovine intervertebral disc cells: implications for identification of normal and degenerate human intervertebral disc cell phenotypes. Arthritis Res Ther 12:R22
48. Gruber HE, Hoelscher GL, Hanley EN Jr (2010) Annulus cells from more degenerated human discs show modified gene expression in 3D culture compared with expression in cells from healthier discs. Spine J 10:721-727
49. Feng G, Yang X, Shang H, Marks IW, Shen FH, Katz A, Arlet V, Laurencin CT, Li X (2010) Multipotential differentiation of human anulus fibrosus cells: an in vitro study. J Bone Joint Surg Am 92:675-685
50. Risbud MV, Guttapalli A, Tsai TT, Lee JY, Danielson KG, Vaccaro AR, Albert TJ, Gazit Z, Gazit D, Shapiro IM (2007) Evidence for skeletal progenitor cells in the degenerate human intervertebral disc. Spine (Phila Pa 1976) 32:2537-2544
51. Poiraudeau S, Monteiro I, Anract P, Blanchard O, Revel M, Corvol MT (1999) Phenotypic characteristics of rabbit intervertebral disc cells. Comparison with cartilage cells from the same animals. Spine (Phila Pa 1976) 24:837-844
52. Gruber HE, Fisher EC Jr, Desai B, Stasky AA, Hoelscher G, Hanley EN Jr (1997) Human intervertebral disc cells from the annulus: three-dimensional culture in agarose or alginate and responsiveness to TGF-beta1. Exp Cell Res 235:13-21
53. Maldonado BA, Oegema TR Jr (1992) Initial characterization of the metabolism of intervertebral disc cells encapsulated in microspheres. J Orthop Res 10:677-690
54. Gruber HE, Leslie K, Ingram J, Hoelscher G, Norton HJ, Hanley EN Jr (2004) Colony formation and matrix production by human anulus cells: modulation in three-dimensional culture. Spine (Phila Pa 1976) 29:E267-E274
55. Mizuno H, Roy AK, Vacanti CA, Kojima K, Ueda M, Bonassar LJ (2004) Tissue-engineered composites of anulus fibrosus and nucleus pulposus for intervertebral disc replacement. Spine (Phila Pa 1976) 29:1290-1297 discussion 1297-8
56. Yang X, Wang D, Hao J, Gong M, Arlet V, Balian G, Shen FH, Li XJ (2011) Enhancement of matrix production and cell proliferation in human annulus cells under bioreactor culture. Tissue Eng Part A 17:1595-1603
57. Le Maitre CL, Richardson SM, Baird P, Freemont AJ, Hoyland JA (2005) Expression of receptors for putative anabolic growth factors in human intervertebral disc: implications for repair and regeneration of the disc. J Pathol 207:445-452
58. Tolonen J, Gronblad M, Vanharanta H, Virri J, Guyer RD, Rytomaa T, Karaharju EO (2006) Growth factor expression in degenerated intervertebral disc tissue. An immunohistochemical analysis of transforming growth factor beta, fibroblast growth factor and platelet-derived growth factor. Eur Spine J 15:588-596
59. Kim JH, Studer RK, Vo NV, Sowa GA, Kang JD (2009) p38 MAPK inhibition selectively mitigates inflammatory mediators and VEGF production in AF cells co-cultured with activated macrophage-like THP-1 cells. Osteoarthritis Cartilage 17:1662-1669
60. Gilbert HT, Hoyland JA, Freemont AJ, Millward-Sadler SJ (2011) The involvement of interleukin-1 and interleukin-4 in the response of human annulus fibrosus cells to cyclic tensile strain: an altered mechanotransduction pathway with degeneration. Arthritis Res Ther 13:R8
61. Hegewald AA, Neumann K, Kalwitz G, Freymann U, Endres M, Schmieder K, Kaps C, Thome C (2011) The chemokines CXCL10 and XCL1 recruit human annulus fibrosus cells. Spine (Phila Pa 1976) 37(2):101-107
62. Thonar E, An H, Masuda K (2002) Compartmentalization of the matrix formed by nucleus pulposus and annulus fibrosus cells in alginate gel. Biochem Soc Trans 30:874-878
63. Thompson JP, Oegema TR Jr, Bradford DS (1991) Stimulation of mature canine intervertebral disc by growth factors. Spine (Phila Pa 1976) 16:253-260
64. Masuda K, Takegami K, An H, Kumano F, Chiba K, Andersson GB, Schmid T, Thonar E (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
65. Masuda K, An HS (2006) Prevention of disc degeneration with growth factors. Eur Spine J 15(Suppl 3):S422-S432
66. Takegami K, An HS, Kumano F, Chiba K, Thonar EJ, Singh K, Masuda K (2005) Osteogenic protein-1 is most effective in stimulating nucleus pulposus and annulus fibrosus cells to repair their matrix after chondroitinase ABC-induced in vitro chemonucleolysis. Spine J 5:231-238
67. Gilbertson L, Ahn SH, Teng PN, Studer RK, Niyibizi C, Kang JD (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
68. Cui M, Wan Y, Anderson DG, Shen FH, Leo BM, Laurencin CT, Balian G, Li X (2008) Mouse growth and differentiation factor-5 protein and DNA therapy potentiates intervertebral disc cell aggregation and chondrogenic gene expression. Spine J 8:287-295
69. Shen FH, Zeng Q, Lv Q, Choi L, Balian G, Li X, Laurencin CT (2006) Osteogenic differentiation of adipose-derived stromal cells treated with GDF-5 cultured on a novel three-dimensional sintered microsphere matrix. Spine J 6:615-623
70. Walsh AJ, Bradford DS, Lotz JC (2004) In vivo growth factor treatment of degenerated intervertebral discs. Spine (Phila Pa 1976) 29:156-163
71. Hayes AJ, Ralphs JR (2011) The response of foetal annulus fibrosus cells to growth factors: modulation of matrix synthesis by TGF-beta1 and IGF-1. Histochem Cell Biol 136:163-175
72. Masuda K, An HS (2004) Growth factors and the intervertebral disc. Spine J 4:330S-340S
73. Osada R, Ohshima H, Ishihara H, Yudoh K, Sakai K, Matsui H, Tsuji H (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
74. Pratsinis H, Kletsas D (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
75. Chujo T, An HS, Akeda K, Miyamoto K, Muehleman C, Attawia M, Andersson G, Masuda K (2006) Effects of growth differentiation factor-5 on the intervertebral disc-in vitro bovine study and in vivo rabbit disc degeneration model study. Spine (Phila Pa 1976) 31:2909-2917
76. Sobajima S, Vadala G, Shimer A, Kim JS, Gilbertson LG, Kang JD (2008) Feasibility of a stem cell therapy for intervertebral disc degeneration. Spine J 8:888-896
77. Tim Yoon S, Su Kim K, Li J, Soo Park J, Akamaru T, Elmer WA, Hutton WC (2003) The effect of bone morphogenetic protein-2 on rat intervertebral disc cells in vitro. Spine (Phila Pa 1976) 28:1773-1780
78. Zhang Y, Anderson DG, Phillips FM, Thonar EJ, He TC, Pietryla D, An HS (2007) Comparative effects of bone morphogenetic proteins and Sox9 overexpression on matrix accumulation by bovine anulus fibrosus cells: implications for anular repair. Spine (Phila Pa 1976) 32:2515-2520
79. Li X, Leo BM, Beck G, Balian G, Anderson GD (2004) Collagen and proteoglycan abnormalities in the GDF-5-deficient mice and molecular changes when treating disk cells with recombinant growth factor. Spine (Phila Pa 1976) 29:2229-2234
80. Feng G, Wan Y, Balian G, Laurencin CT, Li X (2008) Adenovirus-mediated expression of growth and differentiation factor-5 promotes chondrogenesis of adipose stem cells. Growth Factors 26:132-142
81. Liang H, Ma SY, Feng G, Shen FH, Joshua Li X (2010) Therapeutic effects of adenovirus-mediated growth and differentiation factor-5 in a mice disc degeneration model induced by annulus needle puncture. Spine J 10:32-41
82. Mwale F, Demers CN, Petit A, Roughley P, Poole AR, Steffen T, Aebi M, Antoniou J (2003) A synthetic peptide of link protein stimulates the biosynthesis of collagens II, IX and proteoglycan by cells of the intervertebral disc. J Cell Biochem 88:1202-1213
83. Mwale F, Masuda K, Pichika R, Epure LM, Yoshikawa T, Hemmad A, Roughley PJ, Antoniou J (2011) The efficacy of link N as a mediator of repair in a rabbit model of intervertebral disc degeneration. Arthritis Res Ther 13:R120
84. Petit A, Yao G, Rowas SA, Gawri R, Epure L, Antoniou J, Mwale F (2011) Effect of synthetic link N peptide on the expression of type I and type II collagens in human intervertebral disc cells. Tissue Eng Part A 17:899-904
85. Sato M, Kikuchi M, Ishihara M, Ishihara M, Asazuma T, Kikuchi T, Masuoka K, Hattori H, Fujikawa K (2003) Tissue engineering of the intervertebral disc with cultured annulus fibrosus cells using atelocollagen honeycomb-shaped scaffold with a membrane seal (ACHMS scaffold). Med Biol Eng Comput 41:365-371
86. Sato M, Asazuma T, Ishihara M, Ishihara M, Kikuchi T, Kikuchi M, Fujikawa K (2003) An experimental study of the regeneration of the intervertebral disc with an allograft of cultured annulus fibrosus cells using a tissue-engineering method. Spine (Phila Pa 1976) 28:548-553
87. Saad L, Spector M (2004) Effects of collagen type on the behavior of adult canine annulus fibrosus cells in collagen-glycosaminoglycan scaffolds. J Biomed Mater Res A 71:233-241
88. Shao X, Hunter CJ (2007) Developing an alginate/chitosan hybrid fiber scaffold for annulus fibrosus cells. J Biomed Mater Res A 82:701-710
89. Wan Y, Feng G, Shen FH, Balian G, Laurencin CT, Li X (2007) Novel biodegradable poly(1,8-octanediol malate) for annulus fibrosus regeneration. Macromol Biosci 7:1217-1224
90. Helen W, Gough JE (2008) Cell viability, proliferation and extracellular matrix production of human annulus fibrosus cells cultured within PDLLA/Bioglass composite foam scaffolds in vitro. Acta Biomater 4:230-243
91. Helen W, Merry CL, Blaker JJ, Gough JE (2007) Three-dimensional culture of annulus fibrosus cells within PDLLA/Bioglass composite foam scaffolds: assessment of cell attachment, proliferation and extracellular matrix production. Biomaterials 28:2010-2020
92. Chang G, Kim HJ, Vunjak-Novakovic G, Kaplan DL, Kandel R (2010) Enhancing annulus fibrosus tissue formation in porous silk scaffolds. J Biomed Mater Res A 92:43-51
93. Chang G, Kim HJ, Kaplan D, Vunjak-Novakovic G, Kandel RA (2007) Porous silk scaffolds can be used for tissue engineering annulus fibrosus. Eur Spine J 16:1848-1857
94. Schek RM, Michalek AJ, Iatridis JC (2011) Genipin-crosslinked fibrin hydrogels as a potential adhesive to augment intervertebral disc annulus repair. Eur Cell Mater 21:373-383
95. Yang L, Kandel RA, Chang G, Santerre JP (2009) Polar surface chemistry of nanofibrous polyurethane scaffold affects annulus fibrosus cell attachment and early matrix accumulation. J Biomed Mater Res A 91:1089-1099
96. Yeganegi M, Kandel RA, Santerre JP (2010) Characterization of a biodegradable electrospun polyurethane nanofiber scaffold: mechanical properties and cytotoxicity. Acta Biomater 6:3847-3855
97. Koepsell L, Zhang L, Neufeld D, Fong H, Deng Y (2011) Electrospun nanofibrous polycaprolactone scaffolds for tissue engineering of annulus fibrosus. Macromol Biosci 11:391-399
98. Nerurkar NL, Elliott DM, Mauck RL (2007) Mechanics of oriented electrospun nanofibrous scaffolds for annulus fibrosus tissue engineering. J Orthop Res 25:1018-1028
99. Vadala G, Mozetic P, Rainer A, Centola M, Loppini M, Trombetta M, Denaro V (2012) Bioactive electrospun scaffold for annulus fibrosus repair and regeneration. Eur Spine J 21(Suppl 1):S20-S26
100. Bhattacharjee M, Miot S, Gorecka A, Singha K, Loparic M, Dickinson S, Das A, Bhavesh NS, Ray AR, Martin I, Ghosh S (2012) Oriented lamellar silk fibrous scaffolds to drive cartilage matrix orientation: towards annulus fibrosus tissue engineering. Acta Biomater 8:3313-3325
101. Saeidi N, Karmelek KP, Paten JA, Zareian R, Dimasi E, Ruberti JW (2012) Molecular crowding of collagen: a pathway to produce highly-organized collagenous structures. Biomaterials 33:7366-7374
102. Wan Y, Feng G, Shen FH, Laurencin CT, Li X (2008) Biphasic scaffold for annulus fibrosus tissue regeneration. Biomaterials 29:643-652
103. Mizuno H, Roy AK, Zaporojan V, Vacanti CA, Ueda M, Bonassar LJ (2006) Biomechanical and biochemical characterization of composite tissue-engineered intervertebral discs. Biomaterials 27:362-370
104. See EY, Toh SL, Goh JC (2012) Simulated intervertebral disc-like assembly using bone marrow-derived mesenchymal stem cell sheets and silk scaffolds for annulus fibrosus regeneration. J Tissue Eng Regen Med 6:528-535
105. Park SH, Gil ES, Cho H, Mandal BB, Tien LW, Min BH, Kaplan DL (2012) Intervertebral disk tissue engineering using biphasic silk composite scaffolds. Tissue Eng Part A 18:447-458
106. Bowles RD, Gebhard HH, Dyke JP, Ballon DJ, Tomasino A, Cunningham ME, Hartl R, Bonassar LJ (2011) Image-based tissue engineering of a total intervertebral disc implant for restoration of function to the rat lumbar spine. NMR Biomed 25(3):443-451