Topography, cell response, and nerve regeneration

Annual Review of Biomedical Engineering

Volumn 12, Issue , 2010, Pages 203-231

  Hoffman Kim, Diane ^a   Mitchel, Jennifer A ^a   Bellamkonda, Ravi V ^b  

^a BROWN UNIVERSITY   (United States)

^b Emory University   (United States)

Author keywords

axon; cell tension; contact guidance; lithography; neuron

Indexed keywords

AXON; CELL RESPONSE; CELL TYPES; CELLULAR MECHANISMS; CELLULAR ORGANIZATION; CONTACT GUIDANCE; LOOKING TOWARD; MORPHOLOGICAL CHANGES; NERVE INJURIES; NERVE REGENERATION; NEURAL RESPONSE; PHYSICAL FEATURES; SURROUNDING ENVIRONMENT; TOPOGRAPHICAL CUES;

GENE EXPRESSION; TOPOGRAPHY;

PRECISION ENGINEERING;

FIBRONECTIN; FOCAL ADHESION KINASE; LAMININ; NERVE GROWTH FACTOR; POLYLACTIC ACID; BIOMATERIAL;

ANISOTROPY; BIOMIMETICS; CELL ACTIVATION; CELL FUNCTION; CENTRAL NERVOUS SYSTEM; DORSAL ROOT; EXTRACELLULAR MATRIX; IN VITRO STUDY; MICROFILAMENT; MICROTUBULE; MULTICHANNEL RECORDER; NERVE FIBER GROWTH; NERVE INJURY; NERVE REGENERATION; NEURAL STEM CELL; PERIPHERAL NERVOUS SYSTEM; REVIEW; SCHWANN CELL; SPINAL GANGLION; TOPOGRAPHY; ANIMAL; ANIMAL MODEL; GROWTH CONE; NERVE CELL; NERVE FIBER; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; AXONS; COATED MATERIALS, BIOCOMPATIBLE; GROWTH CONES; MODELS, ANIMAL; NERVE REGENERATION; NEURONS;

EID: 77955640328     PISSN: 15239829     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-bioeng-070909-105351     Document Type: Review

References (180)

1. Harrison RG. 1912. The cultivation of tissues in extraneous medium as a method of morphogenetic study. Anat. Rec. 6:181-193
2. Weiss P. 1947. The problem of specificity in growth and development. Yale J. Biol. Med. 19(3):235-278
3. Curtis AS, Varde M. 1964. Control of cell behavior: topological factors. J. Natl. Cancer Inst. 33:15-26
4. Voldman J, Gray ML, Schmidt MA. 1999. Microfabrication in biology and medicine. Annu. Rev. Biomed. Eng. 1:401-425
5. Curtis A, Wilkinson C. 1997. Topographical control of cells. Biomaterials 18(24):1573-1583
6. Lim JY, Donahue HJ. 2007. Cell sensing and response to micro-and nanostructured surfaces produced by chemical and topographic patterning. Tissue Eng. 13(8):1879-1891
7. Rakic P. 1972. Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145(1):61-83
8. O'Rourke NA, Sullivan DP, Kaznowski CE, Jacobs AA, McConnell SK. 1995. Tangential migration of neurons in the developing cerebral cortex. Development 121(7):2165-2176
9. Nadarajah B, Alifragis P, Wong RO, Parnavelas JG. 2002. Ventricle-directed migration in the developing cerebral cortex. Nat. Neurosci. 5(3):218-224 (Pubitemid 34171134)
10. Malatesta P, Appolloni I, Calzolari F. 2008. Radial glia and neural stem cells. Cell Tissue Res. 331(1):165-178
11. Hynes RO, Patel R, Miller RH. 1986. Migration of neuroblasts along preexisting axonal tracts during prenatal cerebellar development. J. Neurosci. 6(3):867-876
12. Jacobs JR, Goodman CS. 1989. Embryonic development of axon pathways in the Drosophila CNS. I. A glial scaffold appears before the first growth cones. J. Neurosci. 9(7):2402-2411
13. Hatten ME. 1990. Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci. 13(5):179-184
14. Ono K, Kawamura K. 1989. Migration of immature neurons along tangentially oriented fibers in the subpial part of the fetal mouse medulla oblongata. Exp. Brain Res. 78(2):290-300
15. Silver J, Lorenz SE, Wahlsten D, Coughlin J. 1982. Axonal guidance during development of the great cerebral commissures: descriptive and experimental studies, in vivo, on the role of preformed glial pathways. J. Comp. Neurol. 210(1):10-29
16. Nagata I, Nakatsuji N. 1991. Rodent CNS neuroblasts exhibit both perpendicular and parallel contact guidance on the aligned parallel neurite bundle. Development 112(2):581-590
17. Sabry JH, O'Connor TP, Evans L, Toroian-Raymond A, Kirschner M, Bentley D. 1991. Microtubule behavior during guidance of pioneer neuron growth cones in situ. J. Cell Biol. 115(2):381-395 (Pubitemid 21926034)
18. Auld V. 1999. Glia as mediators of growth cone guidance: studies from insect nervous systems. Cell Mol. Life Sci. 55(11):1377-1385
19. Hidalgo A. 2003. Neuron-glia interactions during axon guidance in Drosophila. Biochem. Soc. Trans. 31(Pt. 1):50-55
20. Whitington PM, Quilkey C, Sink H. 2004. Necessity and redundancy of guidepost cells in the embryonic Drosophila CNS. Int. J. Dev. Neurosci. 22(3):157-163
21. Palka J, Whitlock KE, Murray MA. 1992. Guidepost cells. Curr. Opin. Neurobiol. 2(1):48-54
22. O'Conner T. 1999. Intermediate targets and segmental pathfinding. Cell Mol. Life Sci. 55(11):1358-1364
23. Dahlin L, Johansson F, Lindwall C, Kanje M. 2009. Chapter 28: future perspective in peripheral nerve reconstruction. Int. Rev. Neurobiol. 87:507-530
24. Mladinic M, Muller KJ, Nicholls JG. 2009. Central nervous system regeneration: from leech to opossum. J. Physiol. 587(Pt. 12):2775-2782
25. Saxena S, Caroni P. 2007. Mechanisms of axon degeneration: from development to disease. Prog. Neu-robiol. 83(3):174-191
26. Bunge RP. 1994. The role of the Schwann cell in trophic support and regeneration. J. Neurol. 242(1 Suppl. 1):S19-21
27. Griffin JW, Thompson WJ. 2008. Biology and pathology of nonmyelinating Schwann cells. Glia 56(14):1518-1531
28. Torigoe K, Tanaka HF, Takahashi A, Awaya A, Hashimoto K. 1996. Basic behavior of migratory Schwann cells in peripheral nerve regeneration. Exp. Neurol. 137(2):301-308
29. Chen YY, McDonald D, Cheng C, Magnowski B, Durand J, Zochodne DW. 2005. Axon and Schwann cell partnership during nerve regrowth. J. Neuropathol. Exp. Neurol. 64(7):613-622
30. Stoll G, Muller HW. 1999. Nerve injury, axonal degeneration and neural regeneration: basic insights. Brain Pathol. 9(2):313-325
31. Busch SA, Silver J. 2007. The role of extracellular matrix in CNS regeneration. Curr. Opin. Neurobiol. 17(1):120-127
32. Pekny M, Nilsson M. 2005. Astrocyte activation and reactive gliosis. Glia 50(4):427-434
33. Avellino AM, Hart D, Dailey AT, MacKinnon M, Ellegala D, Kliot M. 1995. Differential macrophage responses in the peripheral and central nervous system during Wallerian degeneration of axons. Exp. Neurol. 136(2):183-198
34. Schmidt CE, Leach JB. 2003. Neural tissue engineering: strategies for repair and regeneration. Annu. Rev. Biomed. Eng. 5:293-347
35. O'Donnell M, Chance RK, Bashaw GJ. 2009. Axon growth and guidance: receptor regulation and signal transduction. Annu. Rev. Neurosci. 32:383-412
36. Bernhardt RR. 1999. Cellular and molecular bases of axonal pathfinding during embryogenesis of the fish central nervous system. J. Neurobiol. 38(1):137-160
37. Becker CG, Becker T. 2007. Growth and pathfinding of regenerating axons in the optic projection of adult fish. J. Neurosci. Res. 85(12):2793-2799
38. Kalil K, Dent EW. 2005. Touch and go: guidance cues signal to the growth cone cytoskeleton. Curr. Opin. Neurobiol. 15(5):521-526
39. Wen Z, Zheng JQ. 2006. Directional guidance of nerve growth cones. Curr. Opin. Neurobiol. 16(1):52-58
40. Geller HM, Fawcett JW. 2002. Buildingabridge: engineering spinal cord repair.Exp. Neurol. 174(2):125-136
41. Foley JD, Grunwald EW, Nealey PF, Murphy CJ. 2005. Cooperative modulation of neuritogenesis by PC12 cells by topography and nerve growth factor. Biomaterials 26(17):3639-3644
42. Gomez N, Lu Y, Chen S, Schmidt CE. 2007. Immobilized nerve growth factor and microtopography have distinct effects on polarization versus axon elongation in hippocampal cells in culture. Biomaterials 28(2):271-284
43. Mahoney MJ, Chen RR, Tan J, Saltzman WM. 2005. The influence of microchannels on neurite growth and architecture. Biomaterials 26(7):771-778
44. Haq F, Venkatramani A, Keith C, Zhang G. 2007. Neurite development in PC12 cells cultured on nanopillars and nanopores with sizes comparable with filopodia. Int. J. Nanomed. 2(1):107-115
45. Houchin-Ray T, Swift LA, Jang JH, Shea LD. 2007. Patterned PLG substrates for localized DNA delivery and directed neurite extension. Biomaterials 28(16):2603-2611 (Pubitemid 46367211)
46. Koh HS, Yong T, Chan CK, Ramakrishna S. 2008. Enhancement of neurite outgrowth using nano-structured scaffolds coupled with laminin. Biomaterials 29(26):3574-3582
47. Rangappa N, Romero A, Nelson KD, Eberhart RC, Smith GM. 2000. Laminin-coated poly(L-lactide) filaments induce robust neurite growth while providing directional orientation. J. Biomed. Mater. Res. 51(4):625-634
48. Miller C, Jeftinija S, Mallapragada S. 2002. Synergistic effects of physical and chemical guidance cues on neurite alignment and outgrowth on biodegradable polymer substrates. Tissue Eng. 8(3):367-378
49. Miller C, Jeftinija S, Mallapragada S. 2001. Micropatterned Schwann cell-seeded biodegradable polymer substrates significantly enhance neurite alignment and outgrowth. Tissue Eng. 7(6):705-715
50. Kofron C, Hoffman-Kim D. 2009. Optimization by response surface methodology of confluent aligned monolayers of glial and non-glial cells. Cell. Mol. Eng. 2(4):554-572
51. Dowell-Mesfin NM, Abdul-Karim MA, Turner AM, Schanz S,Craighead HG, et al. 2004. Topographically modified surfaces affect orientation and growth of hippocampal neurons. J. Neural. Eng. 1(2):78-90
52. Walsh JF, Manwaring ME, Tresco PA. 2005. Directional neurite outgrowth is enhanced by engineered meningeal cell-coated substrates. Tissue Eng. 11(7-8):1085-1094
53. Hanson JN, Motala MJ, Heien ML, Gillette M, Sweedler J, Nuzzo RG. 2009. Textural guidance cues for controlling process outgrowth of mammalian neurons. Lab Chip 9(1):122-131
54. Li GN, Hoffman-Kim D. 2008. Evaluation of neurite outgrowth anisotropy using a novel application of circular analysis. J. Neurosci. Methods 174:202-214
55. Johansson F, Carlberg P, Danielsen N, Montelius L, Kanje M. 2006. Axonal outgrowth on nano-imprinted patterns. Biomaterials 27(8):1251-1258
56. Corey JM, Lin DY, Mycek KB, Chen Q, Samuel S, et al. 2007. Aligned electrospun nanofibers specify the direction of dorsal root ganglia neurite growth. J. Biomed. Mater. Res. A 83(3):636-645
57. Tranquillo RT. 1999. Self-organization of tissue-equivalents: the nature and role of contact guidance. Biochem. Soc. Symp. 65:27-42
58. Bellamkonda RV. 2006. Peripheral nerve regeneration: an opinion on channels, scaffolds and anisotropy. Biomaterials 27(19):3515-3518
59. Yao L, Wang S, Cui W, Sherlock R, O'Connell C, et al. 2009. Effect of functionalized micropatterned PLGA on guided neurite growth. Acta Biomater. 5(2):580-588
60. Cecchini M, Ferrari A, Beltram F. 2008. PC12 polarity on biopolymer nanogratings. J. Phys. Conf. Ser. 100:012003
61. Li J, McNally H, Shi R. 2008. Enhanced neurite alignment on micro-patterned poly-L-lactic acid films. J. Biomed. Mater. Res. A 87(2):392-404
62. Lietz M, Dreesmann L, Hoss M, Oberhoffner S, Schlosshauer B. 2006. Neuro tissue engineering of glial nerve guides and the impact of different cell types. Biomaterials 27(8):1425-1436
63. Hirono T, Torimitsu K, Kawana A, Fukuda J. 1988. Recognition of artificial microstructures by sensory nerve fibers in culture. Brain Res. 446(1):189-194
64. Clark P, Connolly P, Curtis AS, Dow JA, Wilkinson CD. 1990. Topographical control of cell behaviour: II. Multiple grooved substrata. Development 108(4):635-644
65. Li N, Folch A. 2005. Integration of topographical and biochemical cues by axons during growth on microfabricated 3-D substrates. Exp. Cell Res. 311(2):307-316
66. Nagata I, Kawana A, Nakatsuji N. 1993. Perpendicular contact guidance of CNS neuroblasts on artificial microstructures. Development 117(1):401-408
67. Rajnicek A, Britland S, McCaig C. 1997. Contact guidance of CNS neurites on grooved quartz: influence of groove dimensions, neuronal age and cell type. J. Cell Sci. 110(Pt. 23):2905-2913
68. Martinez E, Engel E, Planell JA, Samitier J. 2009. Effects of artificial micro-and nano-structured surfaces on cell behaviour. Ann. Anat. 191(1):126-135
69. Ono K, Shokunbi T, Nagata I, Tokunaga A, Yasui Y, Nakatsuji N. 1997. Filopodia and growth cones in the vertically migrating granule cells of the postnatal mouse cerebellum. Exp. Brain Res. 117(1):17-29
70. Nagata I, Ono K, Kawana A, Kimura-Kuroda J. 2006. Aligned neurite bundles of granule cells regulate orientation of Purkinje cell dendrites by perpendicular contact guidance in two-dimensional and three-dimensional mouse cerebellar cultures. J. Comp. Neurol. 499(2):274-289
71. Goldner JS, Bruder JM, Li G, Gazzola D, Hoffman-Kim D. 2006. Neurite bridging across micropat-terned grooves. Biomaterials 27(3):460-472
72. Vasita R, Katti DS. 2006. Nanofibers and their applications in tissue engineering. Int. J. Nanomed. 1(1):15-30
73. Yu TT, Shoichet MS. 2005. Guided cell adhesion and outgrowth in peptide-modified channels for neural tissue engineering. Biomaterials 26(13):1507-1514
74. Wen X, Tresco PA. 2006. 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 76(3):626-637
75. Murugan R, Ramakrishna S. 2007. Design strategies of tissue engineering scaffolds with controlled fiber orientation. Tissue Eng. 13(8):1845-1866
76. Kumbar SG, James R, Nukavarapu SP, Laurencin CT. 2008. Electrospun nanofiber scaffolds: engineering soft tissues. Biomed. Mater. 3(3):034002
77. Kim YT, Haftel VK, Kumar S, Bellamkonda RV. 2008. The role of aligned polymer fiber-based constructs in the bridging of long peripheral nerve gaps. Biomaterials 29(21):3117-3127
78. Yang F, Murugan R, Wang S, Ramakrishna S. 2005. Electrospinning of nano/micro scale poly(L-lactic acid) aligned fibers and their potential in neural tissue engineering. Biomaterials 26(15):2603-2610
79. Kriparamanan R, Aswath P, Zhou A, Tang L, Nguyen KT. 2006. Nanotopography: cellular responses to nanostructured materials. J. Nanosci. Nanotechnol. 6(7):1905-1919
80. Papadopoulou E, Samara A, Barberoglou M, Manousaki A, Pagakis S, et al. 2009. Silicon scaffolds promoting 3D neuronal web of cytoplasmic processes. Tissue Eng. Part C. In press
81. Hallstrom W, Martensson T, Prinz C, Gustavsson P, Montelius L, et al. 2007. Gallium phosphide nanowires as a substrate for cultured neurons. Nano Lett. 7(10):2960-2965
82. Cyster LA, Parker KG, Parker TL, Grant DM. 2004. The effect of surface chemistry and nanotopography of titanium nitride (TiN) films on primary hippocampal neurones. Biomaterials 25(1):97-107
83. Khan SP, Auner GG, Newaz GM. 2005. Influence of nanoscale surface roughness on neural cell attachment on silicon. Nanomedicine 1(2):125-129
84. Lamour G, Journiac N, Soues S, Bonneau S, Nassoy P, Hamraoui A. 2009. Influence of surface energy distribution on neuritogenesis. Colloids Surf. B Biointerfaces 72(2):208-218
85. Thompson DM, Buettner HM. 2006. Neurite outgrowth is directed by Schwann cell alignment in the absence of other guidance cues. Ann. Biomed. Eng. 34(1):161-168
86. Hsu SH, Chen CY, Lu PS, Lai CS, Chen CJ. 2005. Oriented Schwann cell growth on microgrooved surfaces. Biotechnol. Bioeng. 92(5):579-588
87. Fawcett JW, Asher RA. 1999. The glial scar and central nervous system repair. Brain Res. Bull. 49(6):377-391
88. Shearer MC, Fawcett JW. 2001. The astrocyte/meningeal cell interface\a barrier to successful nerve regeneration? Cell Tissue Res. 305(2):267-273
89. Silver J, Miller JH. 2004. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5(2):146-156
90. Alexander JK, Fuss B, Colello RJ. 2006. Electric field-induced astrocyte alignment directs neurite outgrowth. Neuron. Glia Biol. 2(2):93-103
91. Recknor JB, Sakaguchi DS, Mallapragada SK. 2006. Directed growth and selective differentiation of neural progenitor cells on micropatterned polymer substrates. Biomaterials 27(22):4098-4108
92. Bruder JM, Monu NC, Harrison MW, Hoffman-Kim D. 2006. Fabrication of polymeric replicas of cell surfaces with nanoscale resolution. Langmuir 22(20):8266-8270
93. Bruder JM, Lee AP, Hoffman-Kim D. 2007. Biomimetic materials replicating Schwann cell topography enhance neuronal adhesion and neurite alignment in vitro. J. Biomater. Sci. Polym. Ed. 18(8):967-982
94. Grew JC, Ricci JL, Alexander H. 2008. Connective-tissue responses to defined biomaterial surfaces. II. Behavior of rat and mouse fibroblasts cultured on microgrooved substrates. J. Biomed. Mater. Res. A 85(2):326-335 (Pubitemid 351535313)
95. Teixeira AI, Abrams GA, Bertics PJ, Murphy CJ, Nealey PF. 2003. Epithelial contact guidance on well-defined micro-and nanostructured substrates. J. Cell Sci. 116(Pt. 10):1881-1892
96. Charest JL, Eliason MT, Garcia AJ, King WP. 2006. Combined microscale mechanical topography and chemical patterns on polymer cell culture substrates. Biomaterials 27(11):2487-2494
97. Britland S, Morgan H, Wojiak-Stodart B, Riehle M, Curtis A, Wilkinson C. 1996. Synergistic and hierarchical adhesive and topographic guidance of BHK cells. Exp. Cell Res. 228(2):313-325
98. Gomez N, Chen S, Schmidt CE. 2007. Polarization of hippocampal neurons with competitive surface stimuli: contact guidance cues are preferred over chemical ligands. J. R. Soc. Interface 4(13):223-233
99. Kofron CM, Fong VJ, Hoffman-Kim D. 2009. Neurite outgrowth at the interface of 2D and 3D growth environments. J. Neural Eng. 6(1):016002
100. Kang CE, Poon PC, Tator CH, Shoichet MS. 2009. 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 15(3):595-604
101. Vavrek R, Girgis J, Tetzlaff W, Hiebert GW, Fouad K. 2006. BDNF promotes connections of corti-cospinal neurons onto spared descending interneurons in spinal cord injured rats. Brain 129(Pt. 6):1534-1545
102. Yu P, Huang L, Zou J, Zhu H, Wang X, et al. 2007. DNA vaccine against NgR promotes functional recovery after spinal cord injury in adult rats. Brain Res. 1147:66-76
103. Walmsley AR, Mir AK. 2007. Targeting the Nogo-A signalling pathway to promote recovery following acute CNS injury. Curr. Pharm. Des. 13(24):2470-2484
104. Selzer ME. 2003. Promotion of axonal regeneration in the injured CNS. Lancet Neurol. 2(3):157-166
105. Bunge MB. 2008. Novel combination strategies to repair the injured mammalian spinal cord. J. Spinal Cord Med. 31(3):262-269
106. Calancie B, Madsen PW, Wood P, Marcillo AE, Levi AD, Bunge RP. 2009. A guidance channel seeded with autologous Schwann cells for repair of cauda equina injury in a primate model. J. Spinal Cord Med. 32(4):379-388
107. Schlosshauer B, Dreesmann L, Schaller HE, Sinis N. 2006. Synthetic nerve guide implants in humans: a comprehensive survey. Neurosurgery 59(4):740-47; discussion 747-748
108. Ichihara S,Inada Y, NakamuraT.2008. Artificial nerve tubes and their application for repairof peripheral nerve injury: an update of current concepts. Injury 39(Suppl. 4):29-39
109. Xu X, Yee WC, Hwang PY, Yu H, Wan AC, et al. 2003. Peripheral nerve regeneration with sustained release of poly(phosphoester) microencapsulated nerve growth factor within nerve guide conduits. Biomaterials 24(13):2405-2412
110. Pfister LA, Papaloizos M, Merkle HP, Gander B. 2007. Nerve conduits and growth factor delivery in peripheral nerve repair. J. Peripher. Nerv. Syst. 12(2):65-82
111. Kato K, Liu H, Kikuchi SI, Myers RR, Shubayev VI. 2009. Immediate anti-tumor necrosis factor-alpha (etanercept) therapy enhances axonal regeneration after sciatic nerve crush. J. Neurosci. Res. 88:360-368
112. Ruff RL, McKerracher L, Selzer ME. 2008. Repair and neurorehabilitation strategies for spinal cord injury. Ann. NY Acad. Sci. 1142:1-20
113. Blesch A, Lu P, Tuszynski MH. 2002. Neurotrophic factors, gene therapy, and neural stem cells for spinal cord repair. Brain Res. Bull. 57(6):833-838
114. de Ruiter GC, Malessy MJ, Yaszemski MJ, Windebank AJ, Spinner RJ. 2009. Designing ideal conduits for peripheral nerve repair. Neurosurg. Focus 26(2):E5
115. Brushart TM, Mathur V, Sood R, Koschorke GM. 1995. Joseph H. Boyes Award. Dispersion of regenerating axons across enclosed neural gaps. J. Hand. Surg. Am. 20(4):557-564
116. Smeal RM, Tresco PA. 2008. The influence of substrate curvature on neurite outgrowth is cell type dependent. Exp. Neurol. 213(2):281-292
117. Straley KS, Wong Po Foo C, Heilshorn S. 2009. Biomaterial design strategies for the treatment of spinal cord injuries. J. Neurotrauma 27:1-19
118. Krych AJ, Rooney GE, Chen B, Schermerhorn TC, Ameenuddin S, et al. 2009. Relationship between scaffold channel diameter and number of regenerating axons in the transected rat spinal cord. Acta Biomater. 5(7):2551-2559
119. Sundback C, Hadlock T, Cheney M, Vacanti J. 2003. Manufacture of porous polymer nerve conduits by a novel low-pressure injection molding process. Biomaterials 24(5):819-830
120. Bender MD, Bennett JM, Waddell RL, Doctor JS, Marra KG. 2004. Multi-channeled biodegradable polymer/CultiSpher composite nerve guides. Biomaterials 25(7-8):1269-1278
121. Yang Y, De Laporte L, Rives CB, Jang JH, Lin WC, et al. 2005. Neurotrophin releasing single and multiple lumen nerve conduits. J. Control Release 104(3):433-446
122. Stokols S, Tuszynski MH. 2004. The fabrication and characterization of linearly oriented nerve guidance scaffolds for spinal cord injury. Biomaterials 25(27):5839-5846
123. de Ruiter GC, Spinner RJ, Malessy MJ, Moore MJ, Sorenson EJ, et al. 2008. Accuracy of motor axon regeneration across autograft, single-lumen, and multichannel poly(lactic-co-glycolic acid) nerve tubes. Neurosurgery 63(1):144-53; discussion 153-155
124. Stokols S, Tuszynski MH. 2006. Freeze-dried agarose scaffolds with uniaxial channels stimulate and guide linear axonal growth following spinal cord injury. Biomaterials 27(3):443-451
125. Moore MJ, Friedman JA, Lewellyn EB, Mantila SM, Krych AJ, et al. 2006. Multiple-channel scaffolds to promote spinal cord axon regeneration. Biomaterials 27(3):419-429
126. Stokols S, Sakamoto J, Breckon C, Holt T, Weiss J, Tuszynski MH. 2006. Templated agarose scaffolds support linear axonal regeneration. Tissue Eng. 12(10):2777-2787
127. Smith LA, Ma PX. 2004. Nano-fibrous scaffolds for tissue engineering. Colloids Surf. B Biointerfaces 39(3):125-131
128. Hadlock T, Sundback C, Hunter D, Cheney M, Vacanti JP. 2000. A polymer foam conduit seeded with Schwann cells promotes guided peripheral nerve regeneration. Tissue Eng. 6(2):119-127
129. Rutkowski GE, Miller CA, Jeftinija S, Mallapragada SK. 2004. Synergistic effects of micropatterned biodegradable conduits and Schwann cells on sciatic nerve regeneration. J. Neural. Eng. 1(3):151-157
130. Yoshii S, Oka M, Shima M, Akagi M, Taniguchi A. 2003. Bridging a spinal cord defect using collagen filament. Spine 28(20):2346-2351 (Pubitemid 37271330)
131. Yoshii S, Oka M, Shima M, Taniguchi A, Taki Y, Akagi M. 2004. Restoration of function after spinal cord transection using a collagen bridge. J. Biomed. Mater. Res. A 70(4):569-575 (Pubitemid 39121882)
132. Yoshii S, Ito S, Shima M, Taniguchi A, Akagi M. 2009. Functional restoration of rabbit spinal cord using collagen-filament scaffold. J. Tissue Eng. Regen. Med. 3(1):19-25
133. Reynolds LF, Bren MC, Wilson BC, Gibson GD, Shoichet MS, Murphy RJ. 2008. Transplantation of porous tubes following spinal cord transection improves hindlimb function in the rat. Spinal Cord 46(1):58-64
134. Panseri S, Cunha C, Lowery J, Del Carro U, Taraballi F, et al. 2008. Electrospun micro-and nanofiber tubes for functional nervous regeneration in sciatic nerve transections. BMC Biotechnol. 8:39
135. Cai J, Peng X, Nelson KD, Eberhart R, Smith GM. 2005. Permeable guidance channels containing microfilament scaffolds enhance axon growth and maturation. J. Biomed. Mater. Res. A 75(2):374-386
136. Lu MC, Huang YT, Lin JH, Yao CH, Lou CW, et al. 2009. Evaluation of a multi-layer microbraided polylactic acid fiber-reinforced conduit for peripheral nerve regeneration. J. Mater. Sci. Mater. Med. 20(5):1175-1180
137. Clements IP, Kim YT, English AW, LuX, Chung A,Bellamkonda RV. 2009. Thin-film enhanced nerve guidance channels for peripheral nerve repair. Biomaterials 30(23-24):3834-3846
138. Flemming RG, Murphy CJ, Abrams GA, Goodman SL, Nealey PF. 1999. Effects of synthetic micro-and nano-structured surfaces on cell behavior. Biomaterials 20(6):573-588
139. Wilson CJ, Clegg RE, Leavesley DI, Pearcy MJ. 2005. Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng. 11(1-2):1-18
140. Roach P, Farrar D, Perry CC. 2006. Surface tailoring for controlled protein adsorption: effect of topography at the nanometer scale and chemistry. J. Am. Chem. Soc. 128(12):3939-3945
141. Kane RS, Stroock AD. 2007. Nanobiotechnology: protein-nanomaterial interactions. Biotechnol. Prog. 23(2):316-319
142. Lim JY, Hansen JC, Siedlecki CA, Hengstebeck RW, Cheng J, et al. 2005. Osteoblast adhesion on poly(L-lactic acid)/polystyrene demixed thin film blends: effect of nanotopography, surface chemistry, and wettability. Biomacromolecules 6(6):3319-3327
143. Hamilton DW, Oakley C, Jaeger NA, Brunette DM. 2009. Directional change produced by perpendicularly-oriented microgrooves is microtubule-dependent for fibroblasts and epithelium. Cell Motil. Cytoskelet. 66(5):260-271
144. Walboomers XF, Croes HJ, Ginsel LA, Jansen JA. 1998. Growth behavior of fibroblasts on microgrooved polystyrene. Biomaterials 19(20):1861-1868
145. Gerecht S, Bettinger CJ, Zhang Z, Borenstein JT, Vunjak-Novakovic G, Langer R. 2007. The effect of actin disrupting agents on contact guidance of human embryonic stem cells. Biomaterials 28(28):4068-4077
146. Mai J, Sun C, Li S, Zhang X. 2007. A microfabricated platform probing cytoskeleton dynamics using multidirectional topographical cues. Biomed. Microdevices 9(4):523-531
147. Oakley C, Brunette DM. 1993. The sequence of alignment of microtubules, focal contacts and actin filaments in fibroblasts spreading on smooth and grooved titanium substrata. J. Cell Sci. 106(Pt. 1):343-354
148. Wojciak-Stothard B, Curtis AS, Monaghan W, McGrath M, Sommer I, Wilkinson CD. 1995. Role of the cytoskeleton in the reaction of fibroblasts to multiple grooved substrata. Cell Motil. Cytoskelet. 31(2):147-158
149. Rajnicek A, McCaig C. 1997. Guidance of CNS growth cones by substratum grooves and ridges: effects of inhibitors of the cytoskeleton, calcium channels and signal transduction pathways. J. Cell Sci. 110(Pt. 23):2915-2924
150. Oakes PW, Patel DC, Morin NA, Zitterbart DP, Fabry B, et al. 2009. Neutrophil morphology and migration are affected by substrate elasticity. Blood 114(7):1387-1395
151. Ali MH, Schumacker PT. 2002. Endothelial responses to mechanical stress: Where is the mechanosen-sor? Crit. Care Med. 30(5 Suppl.):S198-206
152. Katsumi A, Naoe T, Matsushita T, Kaibuchi K, Schwartz MA. 2005. Integrin activation and matrix binding mediate cellular responses to mechanical stretch. J. Biol. Chem. 280(17):16546-16549
153. Booth IR, Edwards MD, Black S, Schumann U, Miller S. 2007. Mechanosensitive channels in bacteria: signs of closure? Nat. Rev. Microbiol. 5(6):431-440
154. Kumamoto CA. 2008. Molecular mechanisms of mechanosensing and their roles in fungal contact sensing. Nat. Rev. Microbiol. 6(9):667-673
155. Monshausen GB, Gilroy S. 2009. Feeling green: mechanosensing in plants. Trends Cell Biol. 19(5):228-235
156. Katsumi A, Orr AW, Tzima E, Schwartz MA. 2004. Integrins in mechanotransduction. J. Biol. Chem. 279(13):12001-12004
157. Makino A, Prossnitz ER, Bunemann M, Wang JM, Yao W, Schmid-Schonbein GW. 2006. G protein-coupled receptors serve as mechanosensors for fluid shear stress in neutrophils. Am. J. Physiol. Cell Physiol. 290(6):C1633-39
158. Chen CS, Tan J, Tien J. 2004. Mechanotransduction at cell-matrix and cell-cell contacts. Annu. Rev. Biomed. Eng. 6:275-302
159. Katsumi A, Milanini J, Kiosses WB, del Pozo MA, Kaunas R, et al. 2002. Effects of cell tension on the small GTPase Rac. J. Cell Biol. 158(1):153-164
160. Li S, Huang NF, Hsu S. 2005. Mechanotransduction in endothelial cell migration. J. Cell Biochem. 96(6):1110-1126
161. Wojciak-Stothard B, Ridley AJ. 2003. Shear stress-induced endothelial cell polarization is mediated by Rho and Rac but not Cdc42 or PI 3-kinases. J. Cell Biol. 161(2):429-439
162. Geiger B, Bershadsky A. 2001. Assembly and mechanosensory function of focal contacts. Curr. Opin. Cell Biol. 13(5):584-592
163. Chiquet M, Gelman L, Lutz R, Maier S. 2009. From mechanotransduction to extracellular matrix gene expression in fibroblasts. Biochim. Biophys. Acta 1793(5):911-920
164. Poole K, Khairy K, Friedrichs J, Franz C, Cisneros DA, et al. 2005. Molecular-scale topographic cues induce the orientation and directional movement of fibroblasts on two-dimensional collagen surfaces. J. Mol. Biol. 349(2):380-386
165. Arnold M, Cavalcanti-Adam EA, Glass R, Blummel J, Eck W, et al. 2004. Activation of integrin function by nanopatterned adhesive interfaces. Chemphyschem 5(3):383-388
166. Wei Y. 2008. Physical interpretation of the maximum receptor-ligand bond spacing to ensure cell adhesion in ligand-coated substrates. Langmuir 24(11):5644-5646
167. Frey MT, Tsai IY, Russell TP, Hanks SK, Wang YL. 2006. Cellular responses to substrate topography: role of myosin II and focal adhesion kinase. Biophys. J. 90(10):3774-3782
168. Wang HB, Dembo M, Hanks SK, Wang Y. 2001. Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc. Natl. Acad. Sci. USA 98(20):11295-11300
169. Dalby MJ, Giannaras D, Riehle MO, Gadegaard N, Affrossman S, Curtis AS. 2004. Rapid fibroblast adhesion to 27 nm high polymer demixed nano-topography. Biomaterials 25(1):77-83
170. Xia N, Thodeti CK, Hunt TP, Xu Q, Ho M, et al. 2008. Directional control of cell motility through focal adhesion positioning and spatial control of Rac activation. FASEB J. 22(6):1649-1659
171. Jiang X, Bruzewicz DA, Wong AP, Piel M, Whitesides GM. 2005. Directing cell migration with asymmetric micropatterns. Proc. Natl. Acad. Sci. USA 102(4):975-978
172. Parker KK, Brock AL, Brangwynne C, Mannix RJ, Wang N,et al. 2002. Directional control of lamellipo-dia extension by constraining cell shape and orienting cell tractional forces. FASEB J. 16(10):1195-1204
173. Thery M, Pepin A, Dressaire E, Chen Y, Bornens M. 2006. Cell distribution of stress fibres in response to the geometry of the adhesive environment. Cell Motil. Cytoskelet. 63(6):341-355
174. James J, Goluch ED, Hu H, Liu C, Mrksich M. 2008. Subcellular curvature at the perimeter of micropat-terned cells influences lamellipodial distribution and cell polarity. Cell Motil. Cytoskelet. 65(11):841-852
175. Dalby MJ, Riehle MO, Yarwood SJ, Wilkinson CD, Curtis AS. 2003. Nucleus alignment and cell signaling in fibroblasts: response to a micro-grooved topography. Exp. Cell Res. 284(2):274-282
176. Dalby MJ, Biggs MJ, Gadegaard N, Kalna G, Wilkinson CD, Curtis AS. 2007. Nanotopographical stimulation of mechanotransduction and changes in interphase centromere positioning. J. Cell Biochem. 100(2):326-338
177. Dalby MJ, Gadegaard N, Herzyk P, Sutherland D, Agheli H, et al. 2007. Nanomechanotransduction and interphase nuclear organization influence on genomic control. J. Cell Biochem. 102(5):1234-1244
178. Dahl KN, Ribeiro AJ, Lammerding J. 2008. Nuclear shape, mechanics, and mechanotransduction. Circ. Res. 102(11):1307-1318
179. Mateos-Langerak J, Goetze S, Leonhardt H, Cremer T, van Driel R, Lanctot C. 2007. Nuclear architecture: Is it important for genome function and can we prove it? J. Cell Biochem. 102(5):1067-1075
180. Dalby MJ. 2005. Topographically induced direct cell mechanotransduction. Med. Eng. Phys. 27(9):730-742