Tissue engineered nerve constructs: Where do we stand?

Journal of Cellular and Molecular Medicine

Volumn 10, Issue 2, 2006, Pages 309-317

  Chalfoun, C T ^a   Wirth, G A ^a   Evans, Gregory R D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Extracellular matrices; Growth factors; Nerve tissue engineering; Scaffolds; Schwann cell cultures

Indexed keywords

BIOMIMETIC MATERIAL; NERVE GROWTH FACTOR;

ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECT; EXTRACELLULAR MATRIX; FORECASTING; HUMAN; INJURY; METABOLISM; NERVE REGENERATION; PERIPHERAL NERVE; PHYSIOLOGY; REVIEW; SCHWANN CELL; TISSUE ENGINEERING;

ANIMALS; BIOMIMETIC MATERIALS; CELL PROLIFERATION; CELLS, CULTURED; EXTRACELLULAR MATRIX; FORECASTING; HUMANS; MODELS, NEUROLOGICAL; NERVE GROWTH FACTORS; NERVE REGENERATION; PERIPHERAL NERVES; SCHWANN CELLS; TISSUE ENGINEERING;

EID: 33747179891     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2006.tb00401.x     Document Type: Review

References (85)

1. Bisceglie V. Uber die antineoplastische Immunitat; heterologe Einpflanzung von Tumoten in Huhner-Embryonen. Ztschr Krebsforsch 1933; 40: 122-40.
2. Beazley WC, Milek MA, Reiss BH. Results of nerve grafting in severe soft tissue injuries. Clin Orthop Relat Res. 1984; 188: 208-12.
3. Dellon AL, MacKinnon SE. An alternative to classical nerve graft for the management of the short nerve gap. Plast Reconstr Surg. 1988; 82: 849-56.
4. Schmidt C, Leach JB. Neural tissue engineering: strategies for repair and regeneration. Annu Rev Biomed Eng. 2003; 5: 293-347.
5. Evans GRD. Approaches to tissue engineered peripheral nerve. Clin Plastic Surg. 2003; 30: 559-63.
6. Lee AC, Yu VM, Lowe JB 3rd, Brenner MJ, Hunter DA, Mackinnon SE, Sakiyama-Elbert SE. Controlled release of nerve growth factor enhances sciatic nerve regeneration. Exp Neurol. 2003; 184: 295-303.
7. Ciardelli G, Chiono V. Materials for peripheral nerve regeneration. Macromol Biosci. 2006; 6: 13-26.
8. Ferrara G. Nuova selva di chirurgia divisiain tre parti. Venice: S Combi; 1608.
9. Glück T. Ueber neuroplastik auf dem wege der trans-plantation. Arch Klin Chir. 1880; 25: 606-16.
10. Millesi H, Ganglberger J, Berger A. Erfharungen mit der mikrochirurgie peripherer nerven. Chirurgica Plastica. 1967; 34: 47.
11. Millesi H. Peripheral nerve surgery today: turning point or continuous development? J Hand Surg [Br]. 1990; 15: 28.
12. Millesi H. Progress in peripheral nerve reconstruction. World J Surg. 1990; 14: 733-47.
13. Hudson R, Evans GRD, Schmidt C. Engineering strategies for peripheral nerve repair. Clin Plast Surg. 1999; 4: 617-28.
14. (Reprinted in Orthop Clin N Am. 2000; 31: 485-97.)
15. Williams LR, Longo FM, Powell HC. Spatial-temporal progress of peripheral nerve regeneration within a silicone chamber: parameters for a bioassay. J Comp Neurol. 1983; 218: 460-70.
16. Williams LR, Varon S. Modification of fibrin matrix formation in situ enhances nerve regeneration in silicone chambers. J Comp Neurol. 1985; 231: 209-20.
17. Lundborg G. Alternatives to autologous nerve grafts. Handchir Mikrochir Plast Chir. 2004; 36: 1-7.
18. Raimondo S, Nicolino S, Tos P, Battiston B, Giacobini-Robecchi MG, Perroteau I, Geuna S. Schwann cell behavior after nerve repair by means of tissue-engineered muscle-vein combined guides. J Comp Neurol. 2005; 489: 249-59.
19. DeLustro F, Dasch J, Keefe J. Immune responses to allogeneic and xenogeneic implants of collagen and collagen derivatives. Clin Orthop. 1990; 260: 263-79.
20. Hudson TW, Liu S, Schmidt CE. Engineering an improved acellular nerve graft via optimized chemical processing. Tissue Eng 2004; 10: 1346-58.
21. Sobol JB, Lowe III JB, Yang RK, Sen SK, Hunter DA, Mackinnon SE. Effects of delaying FK506 administration on neuroregeneration in a rodent model. J Reconstr Microsurg. 2003; 19: 113-8.
22. Myckatyn T, MacKinnon SE, McDonald JW. Stem cell transplantation and other novel techniques for promoting recovery from spinal cord injury. Transpl Immunol. 2004; 12: 343-58.
23. Bryan DJ, Tang JB, Doherty SA, Hile DD, Trantolo DJ, Wise DL, Summerhayes IC. Enhanced peripheral nerve regeneration through a poled bioresorbable poly(lactic-coglycolic acid) guidance channel. J Neural Eng. 2004; 1: 91-8.
24. Evans GRD. Peripheral nerve injury: a review and approach to tissue engineered constructs. Anat Rec. 2001; 263: 396-104.
25. Martini R. Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerve. J Neurocytol. 1994; 23: 1-28.
26. Tonge DA, Golding JP. Regeneration and repair of the peripheral nervous system. Semin Neurosci. 1993; 5: 385-90.
27. Woerly S, Plant GW, Harvey AR. Neural tissue engineering: from polymer to biohybrid organs. Biomaterials 1996; 17: 301-10.
28. Beier JP, Kneser U, Stern-Strater J, Stark GB, Bach AD. Y chromosome detection of three-dimensional tissue-engineered skeletal muscle constructs in a syngeneic rat animal model. Cell Transplant. 2004; 13: 45-53.
29. Madison RD. Point sources of Schwann cells result in growth into nerve entubulation repair site in the absence of axons: effects of freeze-thawing. Exp Neurol. 1994; 128: 266-75.
30. De Vries GH. Schwann cell proliferation. In: Dyck PJ, Thomas PK, editors. Peripheral neuropathy. Philadelphia: W.B. Saunders; 1993. p. 290-8.
31. Rath EM, Kelly D, Bouldin TW, Popko B. Impaired peripheral nerve regeneration in a mutant strain of mice (Enr) with a Schwann cell defect. J Neurosci. 1995; 15: 7228-37.
32. Hadlock T, Elisseeff J, Langer R, Vacanti J, Cheney M. A tissue-engineered conduit for peripheral nerve repair. Arch Otolaryngol Head Neck Surg. 1998; 124: 1081-6.
33. Zhang Y, Campbell G, Anderson PN, Martini R, Schachner M, Lieberman AR. Molecular basis of interactions between regenerating adult rat thalamic axons and Schwann cells in peripheral nerve grafts II: tenascin-c. J Comp Neurol. 1995; 361: 210-24.
34. Zhang Y, Campbell G, Anderson PN, Martini R, Schachner M, Lieberman AR. Molecular basis of interactions between regenerating adult rat thalamic axons and Schwann cells in peripheral nerve grafts I: neural cell adhesion molecules. J Comp Neurol. 1995; 361: 193-209.
35. Terenghi G. Peripheral nerve injury and regeneration. Histol Histopathol. 1995; 10: 709-18.
36. Brown RE, Erdmann D, Lyons SF, Suchy H. The use of cultured Schwann cells in nerve repair in a rabbit hindlimb model. J Reconstr Microsurg. 1996; 12: 149-52.
37. Levi AD, Guenard V, Aebischer P, Bunge RP. The functional characteristics of Schwann cells cultured from human peripheral nerve after transplantation into a gap within the rat sciatic nerve. J Neurosci. 1994; 14: 1309-19.
38. Guenard V, Kleitman N, Morrissey TK, Bunge RP, Aebischer P. Syngeneic Schwann cells derived from adult nerves seeded in semipermeable guidance channels enhance peripheral nerve regeneration. J Neurosci. 1992; 12: 3310-20.
39. Osawa T, Tohyama K, Ide C. Allogeneic nerve grafts in the rat, with special reference to the role of Schwann cells basal laminae in nerve regeneration. J Neurocytol. 1990; 19: 833-49.
40. Evans GR, Brandt K, Katz S, Chauvin P, Otto L, Bogle M, Wang B, Meszlenyi RK, Lu L, Mikos AG, Patrick CW Jr. Bioactive poly(L-lactic acid) conduits seeded with Schwann cells for peripheral nerve regeneration. Biomaterials 2002; 23: 841-8.
41. Patrick CW, Zheng B, Schmidt M, Herman PS, Chauvin BP, Fan Z, Stark B, Evans GR. Dermal fibroblasts genetically engineered to release NGF. Ann Plast Surg. 2001; 47: 660-5.
42. Jimenez JC, Tyson DR, Dhar S, Nguyen T, Hamai Y, Bradshaw RA, Evans GR. Human embryonic kidney cells (HEK-293): characterization and dose response for modulated release of NGF for nerve regeneration. Plast Reconstr Surg. 2004; 113: 605-10.
43. McConnell MP, Dhar S, Nguyen T, Naran S, Calvert JW, Sundine MJ, Bradshaw RA, Evans GR. Nerve growth factor expression response to induction agent booster dosing in transfected human embryonic kidney cells. Plast Reconstr Surg. 2005; 115: 506-14.
44. McConnell MP, Dhar S, Naran S, Nguyen T, Bradshaw RA, Evans GR. In vivo induction and delivery of nerve growth factor, using HEK-293 cells. Tissue Eng. 2004; 10: 1492-501.
45. Knight M, Evans GRD. Tissue engineering: progress and challenges. Plast Reconstr Surg. 2004; 114: 26E-37E.
46. Dezawa M. Future views and challenges to the peripheral nerve regeneration by cell based therapy. Rinsho Shinkeigaku 2005; 45: 877-9.
47. Murakami T, Fujimoto Y, Yasunaga Y, Ishida O, Tanaka N, Ikuta Y, Ochi M. Transplanted neuronal progenitor cells in a peripheral nerve gap promote nerve repair. Brain Res. 2003; 974: 17-24.
48. Heine W, Conant K, Griffin JW, Hoke A. Transplanted neural stem cells promote axonal regeneration through chronically denervated peripheral nerves. Exp Neurol. 2004; 189: 231-40.
49. Morrison SJ, White PM, Zock C, Anderson DJ. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 1999; 96: 737-49.
50. Tohill M, Terenghi G. Stem cell plasticity and therapy for injuries of the peripheral nervous system. Biotechnol Appl Biochem. 2004; 40: 17-24.
51. Amoh Y, Li L, Campillo R, Kawahara K, Katsuoka K, Penman S, Huffman RM. Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. Proc Natl Acad Sci USA. 2005; 102: 17734-8.
52. Cuevas P, Carceller F, Dujovny M, Garcia-Gomez I, Cuevas B, Gonzalez-Corrochano R, Diaz-Gonzalez D, Reimers D. Peripheral nerve regeneration by bone marrow stromal cells. Neurol Res. 2002; 24: 634-8.
53. Cuevas P, Carceller F, Garcia-Gomez I, Yan M, Dujovny M. Bone marrow stromal cell implantation for peripheral nerve repair. Neurol Res. 2004; 26: 230-2.
54. Dezawa M, Takahashi I, Esaki M, Takano M, Sawada H. Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells. Eur J Neurosci. 2001; 14: 1771-6.
55. Choi BH, Zhu SJ, Kim BY, Huh JY, Lee SH, Jung JH. Transplantation of cultured bone marrow stromal cells to improve peripheral nerve regeneration. Oral Maxillofac Surg. 2005; 34: 537-12.
56. Fujimoto E, Mizoguchi A, Hanada K, Yajima M, Ide C. Basic fibroblast growth factor promotes extension of regenerating axons of peripheral nerve: in vivo experiments using a Schwann cell basal lamina tube model. J Neurocytol. 1997; 26: 511-28.
57. Sterne GD, Coulton GR, Brown RA, Green CJ, Terenghi G. Neurotrophin-3 delivered locally via fibronectin mats enhances peripheral nerve regeneration. Eur J Neurosci. 1997; 9: 1388-96.
58. Reichert F, Levitzky R, Rotzhenker S. Interleukin 6 in intact and injured mouse peripheral nerves. Eur J Neurosci. 1996; 8: 530-5.
59. Fu SY, Gordon T. The-cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol. 1997; 14: 67-116.
60. Sjoberg J, Kanje M. Insulin-like growth factor (IGF-I) as a stimulator of regeneration in the freeze-injured rat sciatic nerve. Brain Res. 1989; 485: 102-8.
61. DiStefano PS, Friedman B, Radziejewski C, Alexander C, Boland P, Schick CM, Lindsay RM, Wiegand SJ. The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron 1992; 8: 983-93.
62. Griffin CC, Letourneau PC. Rapid retraction of neurites by sensory neurons in response to increased concentrations of nerve growth factor. J Cell Biol. 1980; 86: 156-61.
63. Kaechi K, Ikegami R, Nakamura N, Nakajima M, Furukawa Y, Furukawa S. 4-Methylcatechol, an inducer of nerve growth factor synthesis, enhances peripheral nerve regeneration across nerve gaps. J Pharmacol Exp Ther. 1995; 272: 1300-4.
64. Yip HK, Rich KM, Lampe PA, Johnson EM Jr. The effects of nerve growth factor and its antiserum on the postnatal development and survival after injury of sensory neurons in the rat dorsal root ganglia. J Neurosci. 1984; 4: 2986-92.
65. Otto D, Unsicker K, Grothe C. Pharmacological effects of nerve growth factor and fibroblast growth factor applied to the transectioned sciatic nerve on neuron death in adult dorsal root ganglia. Neurosci Lett. 1987; 83: 156-60.
66. Rich KM, Luszczynski JR, Osborne PA, Johnson EM Jr. Nerve growth factor protects adult sensory neurons from cell death and atrophy caused by nerve injury. J Neurocytol. 1987; 16: 261-8.
67. Melville S, Sherburn TE, Coggeshall RE. Preservation of sensory cells by placing stumps of transected nerve in an impermeable tube. Exp Neurol. 1989; 105: 311-5.
68. Anton ES, Weskamp G, Reichardt LF, Matthew WD. Nerve growth factor and its low-affinity receptor promote Schwann cell migration. Proc Natl Acad Sci USA. 1994; 91: 2795-9.
69. Friedlander DR, Grumet M, Edleman GM. Nerve growth factor enhances expression of neuron-glia cell adhesion molecule in PC 12 cells. J Cell Biol. 1986; 102: 413-9.
70. Bampton ETW, Taylor JSH. Effects of Schwann cell secreted factors on PC12 cell neuritogenesis and survival. J Neurobiol. 2005; 63: 29-48.
71. Piotrowicz, A, Shoichet MS. Nerve guidance channels as drug delivery vehicles. Biomaterials 2006;27: 2018-27.
72. Whitaker MJ, Quirk RA, Howdle SM, Shakesheff KM. Growth factor release from tissue engineering scaffolds. J Pharm Pharmacol 2001;53: 1427-37.
73. Rose FRA, Oreffo ROC. Bone tissue engineering: hope vs. hype. Biochem Biophys Res Commun. 2002; 292: 1-7.
74. Howdle SM, Watson MS, Whitaker MJ, et al. Supercritical fluid mixing: preparation of thermally sensitive polymer composites containing bioactive materials. Chem Commun 2001; 109-10.
75. Madison RD, Da Silva CF, Dikkes P. Increased rate of peripheral nerve regeneration using bioresorbable nerve guides and a laminin-containing gel. Exp Neurol. 1985; 88: 767-72.
76. Madison RD, da Silva C, Dikkes P, Sidman RL, Chiu TH. Peripheral nerve regeneration with entubulation repair: comparison of biodegradable nerve guides versus polyethylene tubes and the effects of a laminin-containing gel. Exp Neurol. 1987; 95: 378-90.
77. Rosen JM, Padilla JA, Nguyen KD, Siedman J, Pham HN. Artificial nerve graft using collagen as an extracellular matrix for nerve repair compared with sutured autograft in a rat model. Ann Plast Surg. 1990; 25: 375-87.
78. Satou T, Nishida S, Hiruma S, Tanji K, Takahashi M, Fujita S, Mizuhara Y, Akai F, Hashimoto S. A morphological study on the effects of collagen gel matrix on regeneration of severed rat sciatic nerve in silicone tubes. Acta Pathol Jpn. 1986; 36: 199-208.
79. Yuan Y, Zhang P, Yang Y, Wang X, Gu X. The interaction of Schwann cells with chitosan membranes and fibers in vitro. Biomaterials 2004; 25: 4273-8.
80. Young RC, Wiberg M, Terenghi G. Poly-3-hydroxybutyrate (PHB): a resorbable conduit for long-gap repair in peripheral nerves. Br J Plast Surg. 2002; 55: 235-40.
81. Horch RE, Kopp J, Kneser U, Beier J, Bach AD. Tissue engineering of cultured skin substitutes. J Cell Mol Med. 2005; 9: 592-608
82. Horch RE. Future perspectives in tissue engineering. J Cell Mol Med. 2006; 10: 4-6.
83. Stern-Straeter J, Bach AD, Stangenberg L, Foerster VT, Horch RE, Stark GB, Beier JP. Impact of electrical stimulation on three-dimensional myoblast cultures - a realtime RT-PCR-study. J Cell Mol Med. 2005; 9: 883-92.
84. Kneser U, Schaefer DJ, Polykandriotis E, Horch RE. Tissue engineering of bone: the reconstructive surgeon's point of view. J Cell Mol Med. 2006; 10: 7-19.
85. Bach AD, Beier JP, Sternstaetter J, Horch RE. Skeletal muscle tissue engineering. J Cell Mol Med. 2004; 8: 413-22.