Engineering therapies in the CNS: What works and what can be translated

Neuroscience Letters

Volumn 519, Issue 2, 2012, Pages 147-154

  Shoffstall, Andrew J ^a   Taylor, Dawn M ^a,b   Lavik, Erin B ^a  

^a Case Western Reserve University   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Biomaterials; CNS; Drug delivery; Engineering; Scaffold; Translation

Indexed keywords

BIOMATERIAL; MOLECULAR SCAFFOLD; TISSUE SCAFFOLD;

BIOENGINEERING; CELL DIFFERENTIATION; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; DRUG DELIVERY SYSTEM; EXTRACELLULAR MATRIX; FUNCTIONAL ELECTRICAL STIMULATION; HYDROPHILICITY; HYDROPHOBICITY; INTRACELLULAR SIGNALING; MOLECULAR SIZE; NERVE FIBER GROWTH; NEURITE; PRIORITY JOURNAL; REVIEW; SCIENTIST; STEM CELL; TISSUE GROWTH; TISSUE STRUCTURE; YOUNG MODULUS;

ANIMALS; BIOCOMPATIBLE MATERIALS; BIOMEDICAL ENGINEERING; CENTRAL NERVOUS SYSTEM DISEASES; ELECTRIC STIMULATION; EQUIPMENT DESIGN; EXTRACELLULAR MATRIX; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERDISCIPLINARY COMMUNICATION; PHOTIC STIMULATION; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84862245438     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2012.01.058     Document Type: Review

References (141)

1. Ackery A., Tator C., Krassioukov A. A global perspective on spinal cord injury epidemiology. J. Neurotrauma 2004, 21:1355-1370.
2. Alcala-Barraza S.R., Lee M.S., Hanson L.R., McDonald A.A., Frey W.H., McLoon L.K. Intranasal delivery of neurotrophic factors BDNF, CNTF, EPO, and NT-4 to the CNS. J. Drug Target 2010, 18:179-190.
3. Al-Jamal K.T., Gherardini L., Bardi G., Nunes A., Guo C., Bussy C., Herrero M.A., Bianco A., Prato M., Kostarelos K., Pizzorusso T. Functional motor recovery from brain ischemic insult by carbon nanotube-mediated siRNA silencing. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:10952-10957.
4. Balgude A., Yu X., Szymanski A., Bellamkonda R. Agarose gel stiffness determines rate of DRG neurite extension in 3D cultures. Biomaterials 2001, 22:1077-1084.
5. Batchelor P.E., Wills T.E., Hewa A.P., Porritt M.J., Howells D.W. Stimulation of axonal sprouting by trophic factors immobilized within the wound core. Brain Res. 2008, 1209:49-56.
6. Baumann M.D., Kang C.E., Tator C.H., Shoichet M.S. Intrathecal delivery of a polymeric nanocomposite hydrogel after spinal cord injury. Biomaterials 2010, 31:7631-7639.
7. Becker D., Gary D.S., Rosenzweig E.S., Grill W.M., McDonald J.W. Functional electrical stimulation helps replenish progenitor cells in the injured spinal cord of adult rats. Exp. Neurol. 2010, 222:211-218.
8. Behravesh E., Jo S., Zygourakis K., Mikos A.G. Synthesis of in situ cross-linkable macroporous biodegradable poly(propylene fumarate-co-ethylene glycol) hydrogels. Biomacromolecules 2002, 3:374-381.
9. Belda-Lois J.M., Mena-Del Horno S., Bermejo-Bosch I., Moreno J.C., Pons J.L., Farina D., Iosa M., Molinari M., Tamburella F., Ramos A., Caria A., Solis-Escalante T., Brunner C., Rea M. Rehabilitation of gait after stroke: a review towards a top-down approach. J. Neuroeng. Rehabil. 2011, 8:66.
10. Bellamkonda R.V. Biomimetic materials: marine inspiration. Nat. Mater. 2008, 7:347-348.
11. Bock H.C., Puchner M.J., Lohmann F., Schutze M., Koll S., Ketter R., Buchalla R., Rainov N., Kantelhardt S.R., Rohde V., Giese A. First-line treatment of malignant glioma with carmustine implants followed by concomitant radiochemotherapy: a multicenter experience. Neurosurg. Rev. 2010, 33:441-449.
12. Branco M.C., Pochan D.J., Wagner N.J., Schneider J.P. The effect of protein structure on their controlled release from an injectable peptide hydrogel. Biomaterials 2010, 31:9527-9534.
13. Brock J.H., Rosenzweig E.S., Blesch A., Moseanko R., Havton L.A., Edgerton V.R., Tuszynski M.H. Local and remote growth factor effects after primate spinal cord injury. J. Neurosci. 2010, 30:9728-9737.
14. Bronstein J.M., Tagliati M., Alterman R.L., Lozano A.M., Volkmann J., Stefani A., Horak F.B., Okun M.S., Foote K.D., Krack P., Pahwa R., Henderson J.M., Hariz M.I., Bakay R.A., Rezai A., Marks W.J., Moro E., Vitek J.L., Weaver F.M., Gross R.E., DeLong M.R. Deep brain stimulation for Parkinson disease: an expert consensus and review of key issues. Arch. Neurol. 2011, 68:165.
15. Butson C.R., Noecker A.M., Maks C.B., McIntyre C.C. StimExplorer: deep brain stimulation parameter selection software system. Acta Neurochir. Suppl. 2007, 97:569-574.
16. Capadona J.R., Shanmuganathan K., Tyler D.J., Rowan S.J., Weder C. Stimuli-responsive polymer nanocomposites inspired by the sea cucumber dermis. Science 2008, 319:1370-1374.
17. C.f.D.C.a.Prevention National Diabetes Fact Sheet: National Estimates and General Information on Diabetes and Prediabetes in the United States, 2011 2011, U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, GA. C.f.D.C.a. Prevention (Ed.).
18. Chae J., Sheffler L., Knutson J. Neuromuscular electrical stimulation for motor restoration in hemiplegia. Top. Stroke Rehabil. 2008, 15:412-426.
19. Chen B.K., Knight A.M., de Ruiter G.C., Spinner R.J., Yaszemski M.J., Currier B.L., Windebank A.J. Axon regeneration through scaffold into distal spinal cord after transection. J. Neurotrauma 2009, 26:1759-1771.
20. Chvatal S.A., Kim Y.T., Bratt-Leal A.M., Lee H., Bellamkonda R.V. Spatial distribution and acute anti-inflammatory effects of methylprednisolone after sustained local delivery to the contused spinal cord. Biomaterials 2008, 29:1967-1975.
21. Collier R. Rapidly rising clinical trial costs worry researchers. CMAJ 2009, 180:277-278.
22. 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.
23. Daly J.J., Ruff R.L. Construction of efficacious gait and upper limb functional interventions based on brain plasticity evidence and model-based measures for stroke patients. ScientificWorldJournal 2007, 7:2031-2045.
24. De Laporte L., Yan A.L., Shea L.D. Local gene delivery from ECM-coated poly(lactide-co-glycolide) multiple channel bridges after spinal cord injury. Biomaterials 2009, 30:2361-2368.
25. Discher D., Janmey P., Wang Y. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
26. Discher D.E., Janmey P., Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
27. Edgerton V.R., Harkema S. Epidural stimulation of the spinal cord in spinal cord injury: current status and future challenges. Expert. Rev. Neurother. 2011, 11:1351-1353.
28. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
29. Designation of an Orphan Drug, 21 C.F.R. Sect. 316.20-30 (2011).
30. Fischer R.S., Gardel M., Ma X., Adelstein R.S., Waterman C.M. Local cortical tension by myosin II guides 3D endothelial cell branching. Curr. Biol. 2009, 19:260-265.
31. Fozdar D.Y., Lee J.Y., Schmidt C.E., Chen S. Hippocampal neurons respond uniquely to topographies of various sizes and shapes. Biofabrication 2010, 2:035005.
32. Fozdar D.Y., Lee J.Y., Schmidt C.E., Chen S. Selective axonal growth of embryonic hippocampal neurons according to topographic features of various sizes and shapes. Int. J. Nanomed. 2011, 6:45-57.
33. Gautier S.E., Oudega M., Fragoso M., Chapon P., Plant G.W., Bunge M.B., Parel J.-M. Poly(α-hydroxyacids) for application in the spinal cord: resorbability and biocompatability with adult rat Schwann cells and spinal cord. J. Biomed. Mater. Res. 1998, 42:642-654.
34. Ghajar C.M., Blevins K.S., Hughes C.C., George S.C., Putnam A.J. Mesenchymal stem cells enhance angiogenesis in mechanically viable prevascularized tissues via early matrix metalloproteinase upregulation. Tissue Eng. 2006, 12:2875-2888.
35. Golub J.S., Kim Y.T., Duvall C.L., Bellamkonda R.V., Gupta D., Lin A.S., Weiss D., Robert Taylor W., Guldberg R.E. Sustained VEGF delivery via PLGA nanoparticles promotes vascular growth. Am. J. Physiol. Heart Circ. Physiol. 2010, 298:H1959-H1965.
36. Guest J.D., Hesse D., Schnell L., Schwab M.E., Bunge M.B., Bunge R.P. Influence of IN-1 antibody and acidic FGF-fibrin glue on the response of injured corticospinal tract axons to human Schwann cell grafts. J. Neurosci. Res. 1997, 50:888-905.
37. Guest J.D., Rao A., Olson L., Bunge M.B., Bunge R.P. The ability of human Schwann cell grafts to promote regeneration in the transected nude rat spinal cord. Exp. Neurol. 1997, 148:502-522.
38. Harkema S., Gerasimenko Y., Hodes J., Burdick J., Angeli C., Chen Y., Ferreira C., Willhite A., Rejc E., Grossman R.G., Edgerton V.R. Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: a case study. Lancet 2011, 377:1938-1947.
39. Heris H.K., Rahmat M., Mongeau L. Characterization of a hierarchical network of hyaluronic acid/gelatin composite for use as a smart injectable biomaterial. Macromol. Biosci. 2012, 12:202-210.
40. Hoffman-Kim D., Mitchel J.A., Bellamkonda R.V. Topography, cell response, and nerve regeneration. Annu. Rev. Biomed. Eng. 2010, 12:203-231.
41. Hollis E.R., Lu P., Blesch A., Tuszynski M.H. IGF-I gene delivery promotes corticospinal neuronal survival but not regeneration after adult CNS injury. Exp. Neurol. 2009, 215:53-59.
42. 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.
43. Hou S., Xu Q., Tian W., Cui F., Cai Q., Ma J., Lee I.S. The repair of brain lesion by implantation of hyaluronic acid hydrogels modified with laminin. J. Neurosci. Methods 2005, 148:60-70.
44. Hou S.P., Xu Q.Y., Tian W.M., Cui F.Z., Cai Q., Ma J., Lee I.S. The repair of brain lesion by implantation of hyaluronic acid hydrogels modified with laminin. J. Neurosci. Methods 2005, 148:60-70.
45. 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.
46. Hurley J.R., Balaji S., Narmoneva D.A. Complex temporal regulation of capillary morphogenesis by fibroblasts. Am. J. Physiol. Cell Physiol. 2010, 299:C444-C453.
47. Hwang D.H., Jeong S.R., Kim B.G. Gene transfer mediated by stem cell grafts to treat CNS injury. Expert Opin. Biol. Ther. 2011, 11:1599-1610.
48. Iannotti C., Li H.Y., Yan P., Lu X.B., Wirthlin L., Xu X.M. Glial cell line-derived neurotrophic factor-enriched bridging transplants promote propriospinal axonal regeneration and enhance myelination after spinal cord injury. Exp. Neurol. 2003, 183:379-393.
49. Ingber D.E. Mechanical control of tissue morphogenesis during embryological development. Int. J. Dev. Biol. 2006, 50:255-266.
50. Ingber D.E., Prusty D., Sun Z., Betensky H., Wang N. Cell shape, cytoskeletal mechanics, and cell cycle control in angiogenesis. J. Biomech. 1995, 28:1471-1484.
51. Jain A., Kim Y.T., McKeon R.J., Bellamkonda R.V. In situ gelling hydrogels for conformal repair of spinal cord defects, and local delivery of BDNF after spinal cord injury. Biomaterials 2006, 27:497-504.
52. Jain A., McKeon R.J., Brady-Kalnay S.M., Bellamkonda R.V. Sustained delivery of activated Rho GTPases and BDNF promotes axon growth in CSPG-rich regions following spinal cord injury. PLoS One 2011, 6:e16135.
53. Jesuraj N.J., Nguyen P.K., Wood M.D., Moore A.M., Borschel G.H., Mackinnon S.E., Sakiyama-Elbert S.E. Differential gene expression in motor and sensory Schwann cells in the rat femoral nerve. J. Neurosci. Res. 2012, 90:96-104.
54. Johnson P.J., Parker S.R., Sakiyama-Elbert S.E. Controlled release of neurotrophin-3 from fibrin-based tissue engineering scaffolds enhances neural fiber sprouting following subacute spinal cord injury. Biotechnol. Bioeng. 2009, 104:1207-1214.
55. 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.
56. Kabos P., Matundan H., Zandian M., Bertolotto C., Robinson M.L., Davy B.E., Yu J.S., Krueger R.C. Neural precursors express multiple chondroitin sulfate proteoglycans, including the lectican family. Biochem. Biophys. Res. Commun. 2004, 318:955-963.
57. Kaplan A.V., Baim D.S., Smith J.J., Feigal D.A., Simons M., Jefferys D., Fogarty T.J., Kuntz R.E., Leon M.B. Medical device development: from prototype to regulatory approval. Circulation 2004, 109:3068-3072.
58. Khan T., Dauzvardis M., Sayers S. Carbon filament implants promote axonal growth across the transected rat spinal cord. Brain Res. 1991, 541:139-145.
59. Khatiwala C., Peyton S., Putnam A. Intrinsic mechanical properties of the extracellular matrix affect the behavior of pre-osteoblastic MC3T3-E1 cells. Am. J. Physiol. Cell. Physiol. 2006, 290:C1640-C1650.
60. Kilgore K.L., Peckham P., Keith M.W. Twenty year experience with implanted neuroprostheses. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 2009:7212-7215.
61. Kim B.S., Nikolovski J., Bonadio J., Mooney D.J. Cyclic mechanical strain regulates the development of engineered smooth muscle tissue. Nat. Biotech. 1999, 17:979-983.
62. Kim H., Cooke M.J., Shoichet M.S. Creating permissive microenvironments for stem cell transplantation into the central nervous system. Trends Biotechnol. 2011, 30:55-63.
63. Kim H.M., Hwang D.H., Lee J.E., Kim S.U., Kim B.G. Ex vivo VEGF delivery by neural stem cells enhances proliferation of glial progenitors, angiogenesis, and tissue sparing after spinal cord injury. PLoS One 2009, 4:e4987.
64. Kim Y., Szele F.G. Activation of subventricular zone stem cells after neuronal injury. Cell Tissue Res. 2008, 331:337-345.
65. Kim Y.T., Caldwell J.M., Bellamkonda R.V. Nanoparticle-mediated local delivery of Methylprednisolone after spinal cord injury. Biomaterials 2009, 30:2582-2590.
66. Kong H.J., Polte T.R., Alsberg E., Mooney D.J. FRET measurements of cell-traction forces and nano-scale clustering of adhesion ligands varied by substrate stiffness. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:4300-4305.
67. Kramer R.H., Fortin D.L., Trauner D. New photochemical tools for controlling neuronal activity. Curr. Opin. Neurobiol. 2009, 19:544-552.
68. Kyhn M.V., Klassen H., Johansson U.E., Warfvinge K., Lavik E., Kiilgaard J.F., Prause J.U., Scherfig E., Young M., la Cour M. Delayed administration of glial cell line-derived neurotrophic factor (GDNF) protects retinal ganglion cells in a pig model of acute retinal ischemia. Exp. Eye Res. 2009, 89:1012-1020.
69. Lagali P.S., Balya D., Awatramani G.B., Munch T.A., Kim D.S., Busskamp V., Cepko C.L., Roska B. Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration. Nat. Neurosci. 2008, 11:667-675.
70. Langlois J.A., Rutland-Brown W., Wald M.M. The epidemiology and impact of traumatic brain injury: a brief overview. J. Head Trauma Rehabil. 2006, 21:375-378.
71. Lathia J.D., Patton B., Eckley D.M., Magnus T., Mughal M.R., Sasaki T., Caldwell M.A., Rao M.S., Mattson M.P., Ffrench-Constant C. Patterns of laminins and integrins in the embryonic ventricular zone of the CNS. J. Comp. Neurol. 2007, 505:630-643.
72. Lee K.H., Yoon D.H., Park Y.G., Lee B.H. Effects of glial transplantation on functional recovery following acute spinal cord injury. J. Neurotrauma 2005, 22:575-589.
73. Leipzig N.D., Shoichet M.S. The effect of substrate stiffness on adult neural stem cell behavior. Biomaterials 2009, 30:6867-6878.
74. Man A.J., Davis H.E., Itoh A., Leach J.K., Bannerman P. Neurite outgrowth in fibrin gels is regulated by substrate stiffness. Tissue Eng. Part A 2011, 17:2931-2942.
75. Marchand R., Woerly S. Transected spinal cords grafted with in situ self-assembled collagen matrices. Neuroscientist 1990, 36:45-60.
76. Martin B.C., Minner E.J., Wiseman S.L., Klank R.L., Gilbert R.J. Agarose and methylcellulose hydrogel blends for nerve regeneration applications. J. Neural Eng. 2008, 5:221-231.
77. Matthews R.T., Kelly G.M., Zerillo C.A., Gray G., Tiemeyer M., Hockfield S. Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J. Neurosci. 2002, 22:7536-7547.
78. McCarty J.H. Cell adhesion and signaling networks in brain neurovascular units. Curr. Opin. Hematol. 2009, 16:209-214.
79. McConnell G.C., Rees H.D., Levey A.I., Gutekunst C.A., Gross R.E., Bellamkonda R.V. Implanted neural electrodes cause chronic, local inflammation that is correlated with local neurodegeneration. J. Neural. Eng. 2009, 6:056003.
80. McIntyre C.C., Savasta M., Walter B.L., Vitek J.L. How does deep brain stimulation work? Present understanding and future questions. J. Clin. Neurophysiol. 2004, 21:40-50.
81. Miocinovic S., Noecker A.M., Maks C.B., Butson C.R., McIntyre C.C. Cicerone: stereotactic neurophysiological recording and deep brain stimulation electrode placement software system. Acta Neurochir. Suppl. 2007, 97:561-567.
82. Modolo J., Beuter A. Linking brain dynamics, neural mechanisms, and deep brain stimulation in Parkinson's disease: an integrated perspective. Med. Eng. Phys. 2009, 31:615-623.
83. Moore A.M., Wood M.D., Chenard K., Hunter D.A., Mackinnon S.E., Sakiyama-Elbert S.E., Borschel G.H. Controlled delivery of glial cell line-derived neurotrophic factor enhances motor nerve regeneration. J. Hand Surg. Am. 2010, 35:2008-2017.
84. Moore N., Sakiyama-Elbert S. Analysis of cell binding and internalization of multivalent PEG-based gene delivery vehicles. IEEE Trans Nanobioscience 2011, [Epub ahead of print].
85. Mulcahey M.J., Betz R.R., Kozin S.H., Smith B.T., Hutchinson D., Lutz C. Implantation of the freehand system during initial rehabilitation using minimally invasive techniques. Spinal Cord 2004, 42:146-155.
86. Nagao M., Sugimori M., Nakafuku M. Cross talk between notch and growth factor/cytokine signaling pathways in neural stem cells. Mol. Cell Biol. 2007, 27:3982-3994.
87. Ng T.F., Lavik E., Keino H., Taylor A.W., Langer R.S., Young M.J. Creating an immune-privileged site using retinal progenitor cells and biodegradable polymers. Stem Cells 2007, 25:1552-1559.
88. Noonan C.W., Williamson D.M., Henry J.P., Indian R., Lynch S.G., Neuberger J.S., Schiffer R., Trottier J., Wagner L., Marrie R.A. The prevalence of multiple sclerosis in 3 US communities. Prev. Chronic Dis. 2010, 7:A12.
89. The 2010 Annual Statistical Report: For the Spinal Cord Injury Model Systems 2010, 1-76. University of Alabama at Birmingham, Birmingam, Alabama. N.S.C.I.S. Center (Ed.).
90. 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.
91. Park J., Lim E., Back S., Na H., Park Y., Sun K. Nerve regeneration following spinal cord injury using matrix metalloproteinase-sensitive, hyaluronic acid-based biomimetic hydrogel scaffold containing brain-derived neurotrophic factor, J. Biomed. Mater. Res. A 2010, 93:1091-1099.
92. Pashuck E.T., Cui H., Stupp S.I. Tuning supramolecular rigidity of peptide fibers through molecular structure. J. Am. Chem. Soc. 2010, 132:6041-6046.
93. Patist C.M., Mulder M.B., Gautier S.E., Maquet V., Jerome R., Oudega M. Freeze-dried poly(d,l-lactic acid) macroporous guidance scaffolds impregnated with brain-derived neurotrophic factor in the transected adult rat thoracic spinal cord. Biomaterials 2004, 25:1569-1582.
94. 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.
95. Peckham P.H., Knutson J.S. Functional electrical stimulation for neuromuscular applications. Annu. Rev. Biomed. Eng. 2005, 7:327-360.
96. Peyton S.R., Putnam A.J. Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J. Cell. Physiol. 2005, 204:198-209.
97. Piantino J., Burdick J.A., Goldberg D., Langer R., Benowitz L.I. An injectable, biodegradable hydrogel for trophic factor delivery enhances axonal rewiring and improves performance after spinal cord injury. Exp. Neurol. 2006, 201:359-367.
98. Popovic D.B., Popovic M.B. Advances in the use of electrical stimulation for the recovery of motor function. Prog. Brain Res. 2011, 194:215-225.
99. Preston M., Sherman L.S. Neural stem cell niches: roles for the hyaluronan-based extracellular matrix. Front Biosci. (Schol. Ed.) 2011, 3:1165-1179.
100. Ramón-Cueto A., Cordero M.I., Santos-Benito F.F., Avila J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 2000, 25:425-435.
101. Robinson J. Engineering Thinking and Rhetoric. J. Eng. Educ. 1998, (July):227-229.
102. Rosamond W., Flegal K., Furie K., Go A., Greenlund K., Haase N., Hailpern S.M., Ho M., Howard V., Kissela B., Kittner S., Lloyd-Jones D., McDermott M., Meigs J., Moy C., Nichol G., O'Donnell C., Roger V., Sorlie P., Steinberger J., Thom T., Wilson M., Hong Y. Heart disease and stroke statistics - 2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2008, 117:e25-e146.
103. Saha K., Keung A.J., Irwin E.F., Li Y., Little L., Schaffer D.V., Healy K.E. Substrate modulus directs neural stem cell behavior. Biophys. J. 2008, 95:4426-4438.
104. Sarig-Nadir O., Seliktar D. The role of matrix metalloproteinases in regulating neuronal and nonneuronal cell invasion into PEGylated fibrinogen hydrogels. Biomaterials 2010, 31:6411-6416.
105. Saunders R.L., Hammer D.A. Assembly of human umbilical vein endothelial cells on compliant hydrogels. Cell Mol. Bioeng. 2010, 3:60-67.
106. Scott R., Marquardt L., Willits R.K. Characterization of poly(ethylene glycol) gels with added collagen for neural tissue engineering. J. Biomed. Mater. Res. A 2010, 93:817-823.
107. 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 2010, Biomaterials.
108. Seidlits S.K., Drinnan C.T., Petersen R.R., Shear J.B., Suggs L.J., Schmidt C.E. Fibronectin-hyaluronic acid composite hydrogels for three-dimensional endothelial cell culture. Acta Biomater. 2011, 7:2401-2409.
109. Shen Q., Wang Y., Kokovay E., Lin G., Chuang S.M., Goderie S.K., Roysam B., Temple S. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008, 3:289-300.
110. Silva G.A., Czeisler C., Niece K.L., Beniash E., Harrington D.A., Kessler J.A., Stupp S.I. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science 2004, 303:1352-1355.
111. Smeal R.M., Tresco P.A. The influence of substrate curvature on neurite outgrowth is cell type dependent. Exp. Neurol. 2008, 213:281-292.
112. Smeal R.M., Rabbitt R., Biran R., Tresco P.A. Substrate curvature influences the direction of nerve outgrowth. Ann. Biomed. Eng. 2005, 33:376-382.
113. Song B.N., Li Y.X., Han D.M. Delayed electrical stimulation and BDNF application following induced deafness in rats. Acta Otolaryngol. 2009, 129:142-154.
114. Song S., Kim M., Shin J.H. Upstream mechanotaxis behavior of endothelial cells. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 2009:2106-2110.
115. 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.
116. Suri S., Schmidt C.E. Photopatterned collagen-hyaluronic acid interpenetrating polymer network hydrogels. Acta Biomater. 2009, 5:2385-2397.
117. Suri S., Schmidt C.E. Cell-laden hydrogel constructs of hyaluronic acid, collagen, and laminin for neural tissue engineering. Tissue Eng. A 2010, 16:1703-1716.
118. Talbott J.F., Cao Q., Bertram J., Nkansah M., Benton R.L., Lavik E., Whittemore S.R. CNTF promotes the survival and differentiation of adult spinal cord-derived oligodendrocyte precursor cells in vitro but fails to promote remyelination in vivo. Exp. Neurol. 2007, 204:485-489.
119. 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.
120. Thomopoulos S., Das R., Sakiyama-Elbert S., Silva M.J., Charlton N., Gelberman R.H. bFGF and PDGF-BB for tendon repair: controlled release and biologic activity by tendon fibroblasts in vitro. Ann. Biomed. Eng. 2009, 38:225-234.
121. Tomita H., Sugano E., Isago H., Hiroi T., Wang Z., Ohta E., Tamai M. Channelrhodopsin-2 gene transduced into retinal ganglion cells restores functional vision in genetically blind rats. Exp. Eye Res. 2010, 90:429-436.
122. Tresco P.A., Winslow B.D. The challenge of integrating devices into the central nervous system. Crit. Rev. Biomed. Eng. 2011, 39:29-44.
123. Tsai E.C., Dalton P.D., Shoichet M.S., Tator C.H. Synthetic hydrogel guidance channels facilitate regeneration of adult rat brainstem motor axons after complete spinal cord transection. J. Neurotrauma 2004, 21:789-804.
124. Tysseling-Mattiace V.M., Sahni V., Niece K.L., Birch D., Czeisler C., Fehlings M.G., Stupp S.I., Kessler J.A. Self-assembling nanofibers inhibit glial scar formation and promote axon elongation after spinal cord injury. J. Neuroscience 2008, 28:3814-3823.
125. 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.
126. Webber D.J., Bradbury E.J., McMahon S.B., Minger S.L. Transplanted neural progenitor cells survive and differentiate but achieve limited functional recovery in the lesioned adult rat spinal cord. Regen. Med. 2007, 2:929-945.
127. Wen X., Tresco P.A. Effect of filament diameter and extracellular matrix molecule precoating on neurite outgrowth and Schwann cell behavior on multifilament entubulation bridging device in vitro. J. Biomed. Mater. Res. A 2006, 76:626-637.
128. 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.
129. 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.
130. Woerly S., Doan V.D., Evans-Martin F., Paramore C.G., Peduzzi J.D. Spinal cord reconstruction using NeuroGel implants and functional recovery after chronic injury. J. Neurosci. Res. 2001, 66:1187-1197.
131. Wood M.D., Hunter D., Mackinnon S.E., Sakiyama-Elbert S.E. Heparin-binding-affinity-based delivery systems releasing nerve growth factor enhance sciatic nerve regeneration. J. Biomater. Sci. Polym. Ed. 2010, 21:771-787.
132. Wood M.D., MacEwan M.R., French A.R., Moore A.M., Hunter D.A., Mackinnon S.E., Moran D.W., Borschel G.H., Sakiyama-Elbert S.E. Fibrin matrices with affinity-based delivery systems and neurotrophic factors promote functional nerve regeneration. Biotechnol. Bioeng. 2010, 106:970-979.
133. Wood-Dauphinee S., Exner G. Quality of life in patients with spinal cord injury - basic issues, assessment, and recommendations - results of a consensus meeting. Restor. Neurol. Neurosci. 2002, 20:135-149.
134. Xu W., Russo G.S., Hashimoto T., Zhang J., Vitek J.L. Subthalamic nucleus stimulation modulates thalamic neuronal activity. J. Neurosci. 2008, 28:11916-11924.
135. Xu X., Zhang S.-X., Li H., Aebischer P., Bunge M. Regrowth of axons into the distal spinal cord through a Schwann-cell-seeded mini-channel implanted into hemisected adult rat spinal cord. Eur. J. Neurosci. 1999, 11:1723-1740.
136. Xu X.M., Chen A., Guénard V., Kleitman N., Bunge M.B. Bridging Schwann cell transplants promote axonal regeneration from both the rostral and caudal stumps of the transected adult rat spinal cord. J. Neurocytol. 1997, 26:1-16.
137. Xu X.M., Guénard V., Kleitman N., Aebischer P., Bunge M.B. A Combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann Cell grafts in adult rat thoracic spinal cord. Exp. Neurol. 1995, 134:261-272.
138. Xu X.M., Guénard V., Kleitman N., Bunge M.B. Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J. Comp. Neurol. 1995, 351:145-160.
139. Yucel D., Kose G.T., Hasirci V. Polyester based nerve guidance conduit design. Biomaterials 2010, 31:1596-1603.
140. Zhang F., Aravanis A.M., Adamantidis A., de Lecea L., Deisseroth K. Circuit-breakers: optical technologies for probing neural signals and systems. Nat. Rev. Neurosci. 2007, 8:577-581.
141. Zhang X.Q., Tang H., Hoshi R., De Laporte L., Qiu H., Xu X., Shea L.D., Ameer G.A. Sustained transgene expression via citric acid-based polyester elastomers. Biomaterials 2009, 30:2632-2641.