Advances in natural biomaterials for nerve tissue repair

Neuroscience Letters

Volumn 519, Issue 2, 2012, Pages 103-114

  Khaing, Zin Z ^a   Schmidt, Christine E ^a  

^a The University of Texas at Austin   (United States)

Author keywords

Natural biomaterials; Nervous system regeneration

Indexed keywords

AGAROSE; BARSTAR; BIOMATERIAL; BIOTIN; COLLAGEN; FIBRIN; HYALURONIC ACID; THROMBIN; TISSUE SCAFFOLD;

DRUG DELIVERY SYSTEM; EXTRACELLULAR MATRIX; HUMAN; MICROTECHNOLOGY; NERVE DEGENERATION; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE GRAFT; NERVE REGENERATION; NERVOUS SYSTEM INJURY; NEUROFILAMENT; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; REVIEW; SCHWANN CELL; SCIATIC NERVE; SPINAL CORD INJURY; TISSUE GRAFT; WOUND HEALING;

ANIMALS; BIOCOMPATIBLE MATERIALS; COLLAGEN; FIBRIN; HUMANS; HYALURONIC ACID; NERVOUS SYSTEM DISEASES; SEPHAROSE; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TRANSPLANTS;

EID: 84862261045     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2012.02.027     Document Type: Review

References (134)

1. Abaskharoun M., Bellemare M., Lau E., Margolis R.U. Expression of hyaluronan and the hyaluronan-binding proteoglycans neurocan, aggrecan, and versican by neural stem cells and neural cells derived from embryonic stem cells. Brain Res. 2010, 1327:6-15.
2. Aguayo A.J., David S., Bray G.M. Influences of the glial environment on the elongation of axons after injury: transplantation studies in adult rodents. J. Exp. Biol. 1981, 95:231-240.
3. Ahmed T.A., Giulivi A., Griffith M., Hincke M. Fibrin glues in combination with mesenchymal stem cells to develop a tissue-engineered cartilage substitute. Tissue Eng. Part A 2011, 17:323-335.
4. Alilain W.J., Horn K.P., Hu H., Dick T.E., Silver J. Functional regeneration of respiratory pathways after spinal cord injury. Nature 2011, 475:196-200.
5. Baumann M.D., Kang C.E., Stanwick J.C., Wang Y., Kim H., Lapitsky Y., Shoichet M.S. An injectable drug delivery platform for sustained combination therapy. J. Control. Release 2009, 138:205-213.
6. Bellamkonda R., Ranieri J.P., Bouche N., Aebischer P. Hydrogel-based three-dimensional matrix for neural cells. J. Biomed. Mater. Res. 1995, 29:663-671.
7. Bensaid W., Triffitt J.T., Blanchat C., Oudina K., Sedel L., Petite H. A biodegradable fibrin scaffold for mesenchymal stem cell transplantation. Biomaterials 2003, 24:2497-2502.
8. Bhang S.H., Lee Y.E., Cho S.W., Shim J.W., Lee S.H., Choi C.Y., Chang J.W., Kim B.S. Basic fibroblast growth factor promotes bone marrow stromal cell transplantation-mediated neural regeneration in traumatic brain injury. Biochem. Biophys. Res. Commun. 2007, 359:40-45.
9. Bozkurt A., Brook G.A., Moellers S., Lassner F., Sellhaus B., Weis J., Woeltje M., Tank J., Beckmann C., Fuchs P., Damink L.O., Schugner F., Heschel I., Pallua N. In vitro assessment of axonal growth using dorsal root ganglia explants in a novel three-dimensional collagen matrix. Tissue Eng. 2007, 13:2971-2979.
10. Brannvall K., Bergman K., Wallenquist U., Svahn S., Bowden T., Hilborn J., Forsberg-Nilsson K. Enhanced neuronal differentiation in a three-dimensional collagen-hyaluronan matrix. J. Neurosci. Res. 2007, 85:2138-2146.
11. Brazda N., Muller H.W. Pharmacological modification of the extracellular matrix to promote regeneration of the injured brain and spinal cord. Prog. Brain Res. 2009, 175:269-281.
12. Calderon L., Collin E., Velasco-Bayon D., Murphy M., O'Halloran D., Pandit A. Type II collagen-hyaluronan hydrogel - a step towards a scaffold for intervertebral disc tissue engineering. Eur. Cell. Mater. 2010, 20:134-148.
13. Cameron H.A., Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 1994, 61:203-209.
14. Chamberlain L.J., Yannas I.V., Hsu H.P., Strichartz G., Spector M. Collagen-GAG substrate enhances the quality of nerve regeneration through collagen tubes up to level of autograft. Exp. Neurol. 1998, 154:315-329.
15. Chen S.S., Revoltella R.P., Papini S., Michelini M., Fitzgerald W., Zimmerberg J., Margolis L. Multilineage differentiation of rhesus monkey embryonic stem cells in three-dimensional culture systems. Stem Cells 2003, 21:281-295.
16. Cooke M.J., Wang Y., Morshead C.M., Shoichet M.S. Controlled epi-cortical delivery of epidermal growth factor for the stimulation of endogenous neural stem cell proliferation in stroke-injured brain. Biomaterials 2011, 32:5688-5697.
17. Cote M.P., Hanna A., Lemay M.A., Ollivier-Lanvin K., Santi L., Miller K., Monaghan R., Houle J.D. Peripheral nerve grafts after cervical spinal cord injury in adult cats. Exp. Neurol. 2010, 225:173-182.
18. Craig C.G., Tropepe V., Morshead C.M., Reynolds B.A., Weiss S., van der Kooy D. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci. 1996, 16:2649-2658.
19. David S., Aguayo A.J. Axonal regeneration after crush injury of rat central nervous system fibres innervating peripheral nerve grafts. J. Neurocytol. 1985, 14:1-12.
20. Deister C., Aljabari S., Schmidt C.E. Effects of collagen 1, fibronectin, laminin and hyaluronic acid concentration in multi-component gels on neurite extension. J. Biomater. Sci. Polym. Ed. 2007, 18:983-997.
21. Deumens R., Bozkurt A., Brook G.A. US food and drug administration/conformit Europe-approved absorbable nerve conduits for clinical repair of peripheral and cranial nerves. Ann. Plast. Surg. 2010, 65:371. (Commentary).
22. Dodla M.C., Bellamkonda R.V. Anisotropic scaffolds facilitate enhanced neurite extension in vitro. J. Biomed. Mater. Res. A 2006, 78:213-221.
23. Dodla M.C., Bellamkonda R.V. Differences between the effect of anisotropic and isotropic laminin and nerve growth factor presenting scaffolds on nerve regeneration across long peripheral nerve gaps. Biomaterials 2008, 29:33-46.
24. Dubey N., Letourneau P.C., Tranquillo R.T. Guided neurite elongation and Schwann cell invasion into magnetically aligned collagen in simulated peripheral nerve regeneration. Exp. Neurol. 1999, 158:338-350.
25. Dubovy P., Svizenska I., Klusakova I., Zitkova A., Houst'Ava L., Haninec P. Laminin molecules in freeze-treated nerve segments are associated with migrating Schwann cells that display the corresponding alpha6beta1 integrin receptor. Glia 2001, 33:36-44.
26. East E., de Oliveira D.B., Golding J.P., Phillips J.B. Alignment of astrocytes increases neuronal growth in three-dimensional collagen gels and is maintained following plastic compression to form a spinal cord repair conduit. Tissue Eng. Part A 2010, 16:3173-3184.
27. Estes J.M., Adzick N.S., Harrison M.R., Longaker M.T., Stern R. Hyaluronate metabolism undergoes an ontogenic transition during fetal development: implications for scar-free wound healing. J. Pediatr. Surg. 1993, 28:1227-1231.
28. Evans P.J., Mackinnon S.E., Levi A.D., Wade J.A., Hunter D.A., Nakao Y., Midha R. Cold preserved nerve allografts: changes in basement membrane, viability, immunogenicity, and regeneration. Muscle Nerve 1998, 21:1507-1522.
29. Falanga V., Iwamoto S., Chartier M., Yufit T., Butmarc J., Kouttab N., Shrayer D., Carson P. Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng. 2007, 13:1299-1312.
30. Fawcett J.W. Spinal cord repair: from experimental models to human application. Spinal Cord 1998, 36:811-817.
31. Fuhrmann T., Hillen L.M., Montzka K., Woltje M., Brook G.A. Cell-cell interactions of human neural progenitor-derived astrocytes within a microstructured 3D-scaffold. Biomaterials 2010, 31:7705-7715.
32. Goel R.K., Suri V., Suri A., Sarkar C., Mohanty S., Sharma M.C., Yadav P.K., Srivastava A. Effect of bone marrow-derived mononuclear cells on nerve regeneration in the transection model of the rat sciatic nerve. J. Clin. Neurosci. 2009, 16:1211-1217.
33. Gordon M.K., Hahn R.A. Collagens. Cell Tissue Res. 2010, 339:247-257.
34. Gould E. How widespread is adult neurogenesis in mammals?. Nat. Rev. Neurosci. 2007, 8:481-488.
35. Gould E., Tanapat P. Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience 1997, 80:427-436.
36. Gould E., Tanapat P., McEwen B.S., Flugge G., Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:3168-3171.
37. Gros T., Sakamoto J.S., Blesch A., Havton L.A., Tuszynski M.H. Regeneration of long-tract axons through sites of spinal cord injury using templated agarose scaffolds. Biomaterials 2010, 31:6719-6729.
38. Gulati A.K., Cole G.P. Immunogenicity and regenerative potential of acellular nerve allografts to repair peripheral nerve in rats and rabbits. Acta Neurochir. (Wien) 1994, 126:158-164.
39. Gupta D., Tator C.H., Shoichet M.S. Fast-gelling injectable blend of hyaluronan and methylcellulose for intrathecal, localized delivery to the injured spinal cord. Biomaterials 2006, 27:2370-2379.
40. Gwak S.J., Jung J.K., An S.S., Kim H.J., Oh J.S., Pennant W.A., Lee H.Y., Kong M.H., Kim K.N., Yoon D.H., Ha Y. Chitosan/TPP-hyaluronic acid nanoparticles: a new vehicle for gene delivery to the spinal cord. J. Biomater. Sci. Polym. Ed. 2011.
41. Haque R.M., Malone H.R., Bauknight M.W., Kellner M.A., Ogden A.T., Martin J.H., Tanji K., Winfree C.J. Spinal cord bypass surgery with intercostal and spinal accessory nerves: an anatomical feasibility study in human cadavers. J. Neurosurg. Spine 2011.
42. Hess J.R., Brenner M.J., Fox I.K., Nichols C.M., Myckatyn T.M., Hunter D.A., Rickman S.R., Mackinnon S.E. Use of cold-preserved allografts seeded with autologous Schwann cells in the treatment of a long-gap peripheral nerve injury. Plast. Reconstr. Surg. 2007, 119:246-259.
43. Hoffman-Kim D., Mitchel J.A., Bellamkonda R.V. Topography, cell response, and nerve regeneration. Annu. Rev. Biomed. Eng. 2010, 12:203-231.
44. Horn E.M., Beaumont M., Shu X.Z., Harvey A., Prestwich G.D., Horn K.M., Gibson A.R., Preul M.C., Panitch A. Influence of cross-linked hyaluronic acid hydrogels on neurite outgrowth and recovery from spinal cord injury. J. Neurosurg. Spine 2007, 6:133-140.
45. Hou T., Xu J., Li Q., Feng J., Zen L. In vitro evaluation of a fibrin gel antibiotic delivery system containing mesenchymal stem cells and vancomycin alginate beads for treating bone infections and facilitating bone formation. Tissue Eng. Part A 2008, 14:1173-1182.
46. Houle J.D., Tom V.J., Mayes D., Wagoner G., Phillips N., Silver J. Combining an autologous peripheral nervous system " bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J. Neurosci. 2006, 26:7405-7415.
47. Hu J., Zhu Q.T., Liu X.L., Xu Y.B., Zhu J.K. Repair of extended peripheral nerve lesions in rhesus monkeys using acellular allogenic nerve grafts implanted with autologous mesenchymal stem cells. Exp. Neurol. 2007, 204:658-666.
48. Huang N.F., Lam A., Fang Q., Sievers R.E., Li S., Lee R.J. Bone marrow-derived mesenchymal stem cells in fibrin augment angiogenesis in the chronically infarcted myocardium. Regen. Med. 2009, 4:527-538.
49. Hudson T.W., Liu S.Y., Schmidt C.E. Engineering an improved acellular nerve graft via optimized chemical processing. Tissue Eng. 2004, 10:1346-1358.
50. Hudson T.W., Zawko S., Deister C., Lundy S., Hu C.Y., Lee K., Schmidt C.E. Optimized acellular nerve graft is immunologically tolerated and supports regeneration. Tissue Eng. 2004, 10:1641-1651.
51. Hyatt A.J., Wang D., Kwok J.C., Fawcett J.W., Martin K.R. Controlled release of chondroitinase ABC from fibrin gel reduces the level of inhibitory glycosaminoglycan chains in lesioned spinal cord. J. Control. Release 2010, 147:24-29.
52. Ide C., Tohyama K., Tajima K., Endoh K., Sano K., Tamura M., Mizoguchi A., Kitada M., Morihara T., Shirasu M. Long acellular nerve transplants for allogeneic grafting and the effects of basic fibroblast growth factor on the growth of regenerating axons in dogs: a preliminary report. Exp. Neurol. 1998, 154:99-112.
53. Jha A.K., Yang W., Kirn-Safran C.B., Farach-Carson M.C., Jia X. Perlecan domain I-conjugated, hyaluronic acid-based hydrogel particles for enhanced chondrogenic differentiation via BMP-2 release. Biomaterials 2009, 30:6964-6975.
54. Johnson A.R. Contact inhibition in the failure of mammalian CNS axonal regeneration. Bioessays 1993, 15:807-813.
55. Johnson P.J., Parker S.R., Sakiyama-Elbert S.E. Fibrin-based tissue engineering scaffolds enhance neural fiber sprouting and delay the accumulation of reactive astrocytes at the lesion in a subacute model of spinal cord injury. J. Biomed. Mater. Res. A 2010, 92:152-163.
56. Johnson P.J., Tatara A., McCreedy D.A., Shiu A., Sakiyama-Elbert S.E. Tissue-engineered fibrin scaffolds containing neural progenitors enhance functional recovery in a subacute model of SCI. Soft Matter 2010, 6:5127-5137.
57. Johnson P.J., Tatara A., Shiu A., Sakiyama-Elbert S.E. Controlled release of neurotrophin-3 and platelet-derived growth factor from fibrin scaffolds containing neural progenitor cells enhances survival and differentiation into neurons in a subacute model of SCI. Cell Transplant. 2010, 19:89-101.
58. Jose A., Krishnan L.K. Effect of matrix composition on differentiation of nestin-positive neural progenitors from circulation into neurons. J. Neural Eng. 2010, 7:036009.
59. Kalbermatten D.F., Pettersson J., Kingham P.J., Pierer G., Wiberg M., Terenghi G. New fibrin conduit for peripheral nerve repair. J. Reconstr. Microsurg. 2009, 25:27-33.
60. Kang C.E., Poon P.C., Tator C.H., Shoichet M.S. A new paradigm for local and sustained release of therapeutic molecules to the injured spinal cord for neuroprotection and tissue repair. Tissue Eng. Part A 2009, 15:595-604.
61. Kehoe S., Zhang X.F., Boyd D. FDA approved guidance conduits and wraps for peripheral nerve injury: a review of materials and efficacy. Injury 2011.
62. Khaing Z.Z., Milman B.D., Vanscoy J.E., Seidlits S.K., Grill R.J., Schmidt C.E. High molecular weight hyaluronic acid limits astrocyte activation and scar formation after spinal cord injury. J. Neural. Eng. 2011, 8:046033.
63. Krekoski C.A., Neubauer D., Zuo J., Muir D. Axonal regeneration into acellular nerve grafts is enhanced by degradation of chondroitin sulfate proteoglycan. J. Neurosci. 2001, 21:6206-6213.
64. Lanfer B., Hermann A., Kirsch M., Freudenberg U., Reuner U., Werner C., Storch A. Directed growth of adult human white matter stem cell-derived neurons on aligned fibrillar collagen. Tissue Eng. Part A 2010, 16:1103-1113.
65. Layman H., Rahnemai-Azar A.A., Pham S.M., Tsechpenakis G., Andreopoulos F.M. Synergistic angiogenic effect of codelivering fibroblast growth factor 2 and granulocyte-colony stimulating factor from fibrin scaffolds and bone marrow transplantation in critical limb ischemia. Tissue Eng. Part A 2011, 17:243-254.
66. Lee Y.S., Zdunowski S., Edgerton V.R., Roy R.R., Zhong H., Hsiao I., Lin V.W. Improvement of gait patterns in step-trained, complete spinal cord-transected rats treated with a peripheral nerve graft and acidic fibroblast growth factor. Exp. Neurol. 2010, 224:429-437.
67. Leuner B., Gould E., Shors T.J. Is there a link between adult neurogenesis and learning?. Hippocampus 2006, 16:216-224.
68. Little A.R., O'Callagha J.P. Astrogliosis in the adult and developing CNS: is there a role for proinflammatory cytokines?. Neurotoxicology 2001, 22:607-618.
69. Liu H., Collins S.F., Suggs L.J. Three-dimensional culture for expansion and differentiation of mouse embryonic stem cells. Biomaterials 2006, 27:6004-6014.
70. Longaker M.T., Chiu E.S., Harrison M.R., Crombleholme T.M., Langer J.C., Duncan B.W., Adzick N.S., Verrier E.D., Stern R. Studies in fetal wound healing. IV. Hyaluronic acid-stimulating activity distinguishes fetal wound fluid from adult wound fluid. Ann. Surg. 1989, 210:667-672.
71. Lord S.T. Fibrinogen and fibrin: scaffold proteins in hemostasis. Curr. Opin. Hematol. 2007, 14:236-241.
72. Lu P., Jones L.L., Tuszynski M.H. Axon regeneration through scars and into sites of chronic spinal cord injury. Exp. Neurol. 2007, 203:8-21.
73. Ma J., Tian W.M., Hou S.P., Xu Q.Y., Spector M., Cui F.Z. An experimental test of stroke recovery by implanting a hyaluronic acid hydrogel carrying a Nogo receptor antibody in a rat model. Biomed. Mater. 2007, 2:233-240.
74. Marchand R., Woerly S., Bertrand L., Valdes N. Evaluation of two cross-linked collagen gels implanted in the transected spinal cord. Brain Res. Bull. 1993, 30:415-422.
75. Margolis R.K., Margolis R.U., Preti C., Lai D. Distribution and metabolism of glycoproteins and glycosaminoglycans in subcellular fractions of brain. Biochemistry 1975, 14:4797-4804.
76. Martens T.P., Godier A.F., Parks J.J., Wan L.Q., Koeckert M.S., Eng G.M., Hudson B.I., Sherman W., Vunjak-Novakovic G. Percutaneous cell delivery into the heart using hydrogels polymerizing in situ. Cell Transplant. 2009, 18:297-304.
77. McGraw J., Hiebert G.W., Steeves J.D. Modulating astrogliosis after neurotrauma. J. Neurosci. Res. 2001, 63:109-115.
78. Michelini M., Franceschini V., Sihui Chen S., Papini S., Rosellini A., Ciani F., Margolis L., Revoltella R.P. Primate embryonic stem cells create their own niche while differentiating in three-dimensional culture systems. Cell Prolif. 2006, 39:217-229.
79. Nagao R.J., Lundy S., Khaing Z.Z., Schmidt C.E. Functional characterization of optimized acellular peripheral nerve graft in a rat sciatic nerve injury model. Neurol. Res. 2011, 33:600-608.
80. Nakayama K., Takakuda K., Koyama Y., Itoh S., Wang W., Mukai T., Shirahama N. Enhancement of peripheral nerve regeneration using bioabsorbable polymer tubes packed with fibrin gel. Artif. Organs 2007, 31:500-508.
81. Nakayama K., Takakuda K., Koyama Y., Itoh S., Wang W., Shirahama N., Mukai T. Regeneration of peripheral nerves by bioabsorbable polymer tubes with fibrin gel. J. Nanosci. Nanotechnol. 2007, 7:730-733.
82. Nectow A., Marra K., Kaplan D.L. Biomaterials for the development of peripheral nerve guidance conduits. Tissue Eng. Part B Rev. 2011.
83. Novak U., Kaye A.H. Extracellular matrix and the brain: components and function. J. Clin. Neurosci. 2000, 7:280-290.
84. Paino C.L., Fernandez-Valle C., Bates M.L., Bunge M.B. Regrowth of axons in lesioned adult rat spinal cord: promotion by implants of cultured Schwann cells. J. Neurocytol. 1994, 23:433-452.
85. Pan L., Ren Y., Cui F., Xu Q. Viability and differentiation of neural precursors on hyaluronic acid hydrogel scaffold. J. Neurosci. Res. 2009, 87:3207-3220.
86. Park K.H., Kim H., Moon S., Na K. Bone morphogenic protein-2 (BMP-2) loaded nanoparticles mixed with human mesenchymal stem cell in fibrin hydrogel for bone tissue engineering. J. Biosci. Bioeng. 2009, 108:530-537.
87. Pawar K., Mueller R., Caioni M., Prang P., Bogdahn U., Kunz W., Weidner N. Increasing capillary diameter and the incorporation of gelatin enhance axon outgrowth in alginate-based anisotropic hydrogels. Acta Biomater. 2011, 7:2826-2834.
88. Perry G.W., Krayanek S.R., Wilson D.L. Effects of a conditioning lesion on bullfrog sciatic nerve regeneration: analysis of fast axonally transported proteins. Brain Res. 1987, 423:1-12.
89. Perry V.H., Brown M.C., Gordon S. The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration. J. Exp. Med. 1987, 165:1218-1223.
90. Petter-Puchner A.H., Froetscher W., Krametter-Froetscher R., Lorinson D., Redl H., van Griensven M. The long-term neurocompatibility of human fibrin sealant and equine collagen as biomatrices in experimental spinal cord injury. Exp. Toxicol. Pathol. 2007, 58:237-245.
91. Pettersson J., Kalbermatten D., McGrath A., Novikova L.N. Biodegradable fibrin conduit promotes long-term regeneration after peripheral nerve injury in adult rats. J. Plast. Reconstr. Aesthet. Surg. 2010, 63:1893-1899.
92. Pettersson J., McGrath A., Kalbermatten D.F., Novikova L.N., Wiberg M., Kingham P.J., Novikov L.N. Muscle recovery after repair of short and long peripheral nerve gaps using fibrin conduits. Neurosci. Lett. 2011, 500:41-46.
93. Phillips J.B., Bunting S.C., Hall S.M., Brown R.A. Neural tissue engineering: a self-organizing collagen guidance conduit. Tissue Eng. 2005, 11:1611-1617.
94. Preston M., Sherman L.S. Neural stem cell niches: roles for the hyaluronan-based extracellular matrix. Front. Biosci. (Schol Ed) 2011, 3:1165-1179.
95. Qiu J., Cai D., Filbin M.T. Glial inhibition of nerve regeneration in the mature mammalian CNS. Glia 2000, 29:166-174.
96. Rampon C., Weiss N., Deboux C., Chaverot N., Miller F., Buchet D., Tricoire-Leignel H., Cazaubon S., Baron-Van Evercooren A., Couraud P.O. Molecular mechanism of systemic delivery of neural precursor cells to the brain: assembly of brain endothelial apical cups and control of transmigration by CD44. Stem Cells 2008, 26:1673-1682.
97. Sandrow H.R., Shumsky J.S., Amin A., Houle J.D. Aspiration of a cervical spinal contusion injury in preparation for delayed peripheral nerve grafting does not impair forelimb behavior or axon regeneration. Exp. Neurol. 2008, 210:489-500.
98. Saxena S., Caroni P. Mechanisms of axon degeneration: from development to disease. Prog. Neurobiol. 2007, 83:174-191.
99. Schmidt C.E., Leach J.B. Neural tissue engineering: strategies for repair and regeneration. Annu. Rev. Biomed. Eng. 2003, 5:293-347.
100. Seckel B.R., Jones D., Hekimian K.J., Wang K.K., Chakalis D.P., Costas P.D. Hyaluronic acid through a new injectable nerve guide delivery system enhances peripheral nerve regeneration in the rat. J. Neurosci. Res. 1995, 40:318-324.
101. Seidlits S.K., Khaing Z.Z., Petersen R.R., Nickels J.D., Vanscoy J.E., Shear J.B., Schmidt C.E. The effects of hyaluronic acid hydrogels with tunable mechanical properties on neural progenitor cell differentiation. Biomaterials 2010, 31:3930-3940.
102. Seidlits S.K., Schmidt C.E., Shear J.B. High-resolution patterning of hydrogels in three dimensions using direct-write photofabrication for cell guidance (vol. 19, p. 3543, 2009). Adv. Funct. Mater. 2010, 20:1368.
103. Shibuya S., Yamamoto T., Itano T. Glial and axonal regeneration following spinal cord injury. Cell Adhes. Migr. 2009, 3:99-106.
104. Shingo T., Sorokan S.T., Shimazaki T., Weiss S. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J. Neurosci. 2001, 21:9733-9743.
105. Siebert J.R., Osterhout D.J. The inhibitory effects of chondroitin sulfate proteoglycans on oligodendrocytes. J. Neurochem. 2011, 119:176-188.
106. Sondell M., Lundborg G., Kanje M. Regeneration of the rat sciatic nerve into allografts made acellular through chemical extraction. Brain Res. 1998, 795:44-54.
107. Stokols S., Sakamoto J., Breckon C., Holt T., Weiss J., Tuszynski M.H. Templated agarose scaffolds support linear axonal regeneration. Tissue Eng. 2006, 12:2777-2787.
108. Stokols S., Tuszynski M.H. The fabrication and characterization of linearly oriented nerve guidance scaffolds for spinal cord injury. Biomaterials 2004, 25:5839-5846.
109. Stokols S., Tuszynski M.H. Freeze-dried agarose scaffolds with uniaxial channels stimulate and guide linear axonal growth following spinal cord injury. Biomaterials 2006, 27:443-451.
110. Struve J., Maher P.C., Li Y.Q., Kinney S., Fehlings M.G., Kuntz C.t., Sherman L.S. Disruption of the hyaluronan-based extracellular matrix in spinal cord promotes astrocyte proliferation. Glia 2005, 52:16-24.
111. Suri S., Han L.H., Zhang W., Singh A., Chen S., Schmidt C.E. Solid freeform fabrication of designer scaffolds of hyaluronic acid for nerve tissue engineering. Biomed. Microdevices 2011, 13:983-993.
112. Surini S., Akiyama H., Morishita M., Nagai T., Takayama K. Release phenomena of insulin from an implantable device composed of a polyion complex of chitosan and sodium hyaluronate. J. Control. Release 2003, 90:291-301.
113. Taylor S.J., McDonald J.W., Sakiyama-Elbert S.E. Controlled release of neurotrophin-3 from fibrin gels for spinal cord injury. J. Control. Release 2004, 98:281-294.
114. Thompson D.M., Buettner H.M. Neurite outgrowth is directed by Schwann cell alignment in the absence of other guidance cues. Ann. Biomed. Eng. 2006, 34:669-676.
115. Tian W.M., Hou S.P., Ma J., Zhang C.L., Xu Q.Y., Lee I.S., Li H.D., Spector M., Cui F.Z. Hyaluronic acid-poly-d-lysine-based three-dimensional hydrogel for traumatic brain injury. Tissue Eng. 2005, 11:513-525.
116. Tobin G.R., Chvapil M., Gildenberg P.L. Collagen biosynthesis in healing spinal cord wounds. Surg. Forum 1979, 30:454-456.
117. Uibo R., Laidmae I., Sawyer E.S., Flanagan L.A., Georges P.C., Winer J.P., Janmey P.A. Soft materials to treat central nervous system injuries: evaluation of the suitability of non-mammalian fibrin gels. Biochim. Biophys. Acta 2009, 1793:924-930.
118. Wang K.K., Nemeth I.R., Seckel B.R., Chakalis-Haley D.P., Swann D.A., Kuo J.W., Bryan D.J., Cetrulo C.L. Hyaluronic acid enhances peripheral nerve regeneration in vivo. Microsurgery 1998, 18:270-275.
119. Wang T.W., Spector M. Development of hyaluronic acid-based scaffolds for brain tissue engineering. Acta Biomater. 2009, 5:2371-2384.
120. Wang Y., Wei Y.T., Zu Z.H., Ju R.K., Guo M.Y., Wang X.M., Xu Q.Y., Cui F.Z. Combination of hyaluronic acid hydrogel scaffold and PLGA microspheres for supporting survival of neural stem cells. Pharm. Res. 2011, 28:1406-1414.
121. Wang Y., Yao M., Zhou J., Zheng W., Zhou C., Dong D., Liu Y., Teng Z., Jiang Y., Wei G., Cui X. The promotion of neural progenitor cells proliferation by aligned and randomly oriented collagen nanofibers through beta1 integrin/MAPK signaling pathway. Biomaterials 2011, 32:6737-6744.
122. Watanabe K., Nakamura M., Okano H., Toyama Y. Establishment of three-dimensional culture of neural stem/progenitor cells in collagen type-1 gel. Restor. Neurol. Neurosci. 2007, 25:109-117.
123. Weisel J.W. Structure of fibrin: impact on clot stability. J. Thromb. Haemost. 2007, 5(Suppl. 1):116-124.
124. Weiss S., Dunne C., Hewson J., Wohl C., Wheatley M., Peterson A.C., Reynolds B.A. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 1996, 16:7599-7609.
125. Whitlock E.L., Tuffaha S.H., Luciano J.P., Yan Y., Hunter D.A., Magill C.K., Moore A.M., Tong A.Y., Mackinnon S.E., Borschel G.H. Processed allografts and type I collagen conduits for repair of peripheral nerve gaps. Muscle Nerve 2009, 39:787-799.
126. Willerth S.M., Rader A., Sakiyama-Elbert S.E. The effect of controlled growth factor delivery on embryonic stem cell differentiation inside fibrin scaffolds. Stem Cell Res. 2008, 1:205-218.
127. Willerth S.M., Sakiyama-Elbert S.E. Combining Stem Cells and Biomaterial Scaffolds for Constructing Tissues and Cell Delivery 2008.
128. Wylie R.G., Ahsan S., Aizawa Y., Maxwell K.L., Morshead C.M., Shoichet M.S. Spatially controlled simultaneous patterning of multiple growth factors in three-dimensional hydrogels. Nat. Mater. 2011, 10:799-806.
129. Yoshii S., Oka M., Shima M., Taniguchi A., Akagi M. Bridging a 30-mm nerve defect using collagen filaments. J. Biomed. Mater. Res. Part A 2003, 67A:467-474.
130. Yoshii S., Oka M., Shima M., Taniguchi A., Taki Y., Akagi M. Restoration of function after spinal cord transection using a collagen bridge. J. Biomed. Mater. Res. A 2004, 70:569-575.
131. Yu X., Dillon G.P., Bellamkonda R.B. A laminin and nerve growth factor-laden three-dimensional scaffold for enhanced neurite extension. Tissue Eng. 1999, 5:291-304.
132. Zhang G., Nakamura Y., Wang X., Hu Q., Suggs L.J., Zhang J. Controlled release of stromal cell-derived factor-1 alpha in situ increases c-kit+ cell homing to the infarcted heart. Tissue Eng. 2007, 13:2063-2071.
133. Zhang H., Wei Y.T., Tsang K.S., Sun C.R., Li J., Huang H., Cui F.Z., An Y.H. Implantation of neural stem cells embedded in hyaluronic acid and collagen composite conduit promotes regeneration in a rabbit facial nerve injury model. J. Transl. Med. 2008, 6:67.
134. Zhong Y., Bellamkonda R.V. Biomaterials for the central nervous system. J. R. Soc. Interface 2008, 5:957-975.