Surface Microstructures on Planar Substrates and Textile Fibers Guide Neurite Outgrowth: A Scaffold Solution to Push Limits of Critical Nerve Defect Regeneration?

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Weigel, Stefan ^a,b   Osterwalder, Thomas ^a   Tobler, Ursina ^a   Yao, Li ^c,d   Wiesli, Manuel ^a   Lehnert, Thomas ^e   Pandit, Abhay ^c   Bruinink, Arie ^a  

^a SWISS FEDERAL LABORATORIES FOR MATERIALS SCIENCE AND TECHNOLOGY   (Switzerland)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^d WICHITA STATE UNIVERSITY   (United States)

^e EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMATERIAL; CARBON; POLYIMIDE; SILICON;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOCOMPATIBILITY; CHICKEN; CONTROLLED STUDY; CRITICAL SIZE PERIPHERAL NERVE DEFECT; EMBRYO; EXCIMER LASER; GEOMETRY; GROWTH CONE; HEALING; MATERIAL COATING; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; PERIPHERAL NEUROPATHY; POSITRON EMISSION TOMOGRAPHY; SPINAL CORD NERVE CELL; SURFACE MICROSTRUCTURE; SURFACE PROPERTY; TEXTILE FIBER; VELOCITY; WOUND HEALING;

ANIMALS; BIOCOMPATIBLE MATERIALS; CHICK EMBRYO; NERVE REGENERATION; NEURITES; NEURONS; SPINAL CORD; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84871203094     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050714     Document Type: Article

References (71)

1. Ming GL, Wong ST, Henley J, Yuan XB, Song HJ, et al. (2002) Adaptation in the chemotactic guidance of nerve growth cones. Nature 417: 411-418.
2. Song HJ, Ming GL, Poo MM, (1997) cAMP-induced switching in turning direction of nerve growth cones. Nature 388: 276-279.
3. Cao X, Shoichet MS, (2001) Defining the concentration gradient of nerve growth factor for guided neurite outgrowth. Neurosci 103: 831-840.
4. Adams DN, Kao EYC, Hypolite CL, Distefano MD, Hu WS, et al. (2005) Growth cones turn and migrate up an immobolized gradient of the laminin IKVAV peptide. J Neurobiol 62: 134-147.
5. Torimitsu K, Kawana A, (1990) Selective growth of sensory nerve fibers on metal oxide pattern in culture. Devl Brain Res 51: 128-131.
6. Bernard A, Fitzli D, Sonderegger P, Delamarche E, Michel B, et al. (2001) Affinity capture of proteins from solution and their dissociation by contact printing. Nat Biotechnol 19: 866-869.
7. Dowell-Mesfin NM, Abdul-Karim MA, Turner AMP, Schanz S, Craighead HG, et al. (2004) Topgraphically modified surfaces affect orientation and growth of hippocampal neurons. J Neural Eng 1: 78-90.
8. Clark P, Connolly P, Curtis AS, Dow JA, Wilkinson CD, (1987) Topographical control of cell behaviour: I. Simple step cues. Development 99: 439-448.
9. Rajnicek AM, Britland S, McCaig CD, (1997) Contact guidance of CNS neurites on grooved quartz: influence of groove dimensions, neuronal age and cell type. J Cell Sci 110: 2905-2913.
10. Stier H, Schlosshauer B, (1995) Axonal guidance in the chicken retina. Development 121: 1443-1454.
11. Sun M, Kingham PJ, Reid AJ, Armstrong SJ, Terenghi G, et al. (2010) In vitro and in vivo testing of novel ultrathin PCL and PCL/PLA blend films as peripheral nerve conduit. J Biomed Mater Res A 93: 1470-1481.
12. Morelli S, Salerno S, Piscioneri A, Papenburg BJ, Di Vito A, et al. (2010) Influence of micro-patterned PLLA membranes on outgrowth and orientation of hippocampal neurites. Biomaterials 31: 7000-7011.
13. Reich U, Fadeeva E, Warnecke A, Paasche G, Muller P, et al. (2012) Directing neuronal cell growth on implant material surfaces by microstructuring. J Biomed Mater Res B Appl Biomater 100: 940-947.
14. Mahoney MJ, Chen RR, Tan J, Saltzman WM, (2005) The influence of microchannels on neurite growth and architecture. Biomaterials 26: 771-778.
15. Wieringa PA, Wiertz RW, de Weerd E, Rutten WL, (2010) Bifurcating microchannels as a scaffold to induce separation of regenerating neurites. J Neural Eng 7: 16001.
16. Clark P, Connolly P, Curtis ASG, Dow JAT, Wilkinson CDW, (1991) Cell guidance by ultrafine topography in vitro. J Cell Sci 99: 73-77.
17. Kaehr B, Allen R, KJavier DJ, Currie J, Shear JB, (2004) Guiding neuronal development with in situ microfabrication. PNAS 101: 16104-16108.
18. Nagata I, Kawana A, Nakatsuji N, (1993) Perpendicular contact guidance of CNS neuroblasts on artificial microstructures. Development 117: 401-408.
19. Yucel D, Kose GT, Hasirci V, (2010) Polyester based nerve guidance conduit design. Biomaterials 31: 1596-1603.
20. Klinkhammer K, Bockelmann J, Simitzis C, Brook GA, Grafahrend D, et al. (2010) Functionalization of electrospun fibers of poly(epsilon-caprolactone) with star shaped NCO-poly(ethylene glycol)-stat-poly(propylene glycol) for neuronal cell guidance. J Mater Sci Mater Med 21: 2637-2651.
21. Schnell E, Klinkhammer K, Balzer S, Brook G, Klee D, et al. (2007) Guidance of glial cell migration and axonal growth on electrospun nanofibers of poly-epsilon-caprolactone and a collagen/poly-epsilon-caprolactone blend. Biomaterials 28: 3012-3025.
22. 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: 3117-3127.
23. Madduri S, Papaloizos M, Gander B, (2010) Trophically and topographically functionalized silk fibroin nerve conduits for guided peripheral nerve regeneration. Biomaterials 31: 2323-2334.
24. Francz G, Schroeder A, Hauert R, (1999) Surface analysis and bioreactions to Ti and V conatining a-C:H. Surf Interface Anal 28: 3-7.
25. Wagner F, Hoffmann P, (2000) The angle dependence of structure formation on excimer laser ablated ramps in stretched poly(ethylene terephthalate). Applied Surface Science 168: 158-161.
26. Pekarik V, Bourikas D, Miglino N, Joset P, Preiswerk S, et al. (2003) Screening for gene function in chicken embryo using RNAi and electroporation. Nat Biotechnol 21: 93-96.
27. Hamburger V, Hamilton HL, (1951) A Series of Normal Stages in the Development of the Chick Embryo. Journal of Morphology 88: 49-&.
28. Kuhn TB, (2003) Growing and working with spinal motor neurons. Meth Cell Biol 71: 67-87.
29. Sonderegger P, Lemkin PF, Lipkin LE, Nelson PG, (1985) Differential modulation of the expression of axonal proteins by non-neuronal cells of the peripheral and central nervous system. EMBO J 4: 1395-1401.
30. Kaiser JP, Reinmann A, Bruinink A, (2006) The effect of topographic characteristics on cell migration velocity. Biomaterials 27: 5230-5241.
31. Katz MJ, (1985) How Straight Do Axons Grow. Journal of Neuroscience 5: 589-595.
32. Stepien E, Stanisz J, Korohoda W, (1999) Contact guidance of chick embryo neurons on single scratches in glass and on underlying aligned human skin fibroblasts. Cell Biol Int 23: 105-116.
33. Schlosshauer B, Müller E, Schröder B, Planck H, Müller HW, (2003) Rat schwann cells in bioresorbabble nerve guides to promote and accelerate axonal regeneration. Brain Res 963: 321-326.
34. 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 Engineering 8: 367-378.
35. Rajnicek AM, McCaig CD, (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: 2915-2824.
36. Rajnicek AM, Foubister LE, McCaig CD, (2006) Temporally and spatially coordinated roles for Rho, Rac, Cdc42 and their effectors in growth cone guidance by a physiological electric field. J Cell Sci 119: 1723-1735.
37. 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: 367-378.
38. Shah AK, Fischer C, Knapp CF, Sisken BF, (2004) Quantitation of neurite growth parameters in explant cultures using a new image processing program. J Neurosci Meth 136: 123-131.
39. Bilsland J, Rigby M, Young L, Harper S, (1999) A rapid method for semi-quantitative analysis of neurite outgrowth from chick DRG explants using image analysis. J Neurosci Meth 92: 75-85.
40. Tai H, Buettner HM, (1998) Neurite outgrowth and growth cone morphology on micropatterned surfaces. Biotechnol Prog 14: 364-370.
41. Bouquet C, Soares S, von Boxberg Y, Ravaille-Veron M, Propst F, et al. (2004) Microtubule-associated protein 1B controls directionality of growth cone migration and axonal branching in regeneration of adult dorsal root ganglia neurons. J Neurosci 24: 7204-7213.
42. Brown MD, Cornejo BJ, Kuhn TB, Bamberg JR, (2000) Cdc42 stimulates neurite outgrowth and formation of growth cone filopodia and lamellipodia. J Neurobiol 43: 352-364.
43. Anderson M, Boström M, Pfaller K, Glueckert R, Schrott-Fischer A, et al. (2006) Structure and locomotion of adult in vitro regenerated spiral ganglian growth cones- A study using video microscopy and SEM. Hearing Res 215: 97-107.
44. Dotti CG, Sullivan CA, Banker GA, (1988) Te establishment of polarity by hippocampal neurons in culture. J Neurosci 8: 1454-1468.
45. Odde DJ, Tanaka EM, Hawkins SS, Buettner HM, (1996) Stochastic dynamics of the nerve growth cone and its microtubules during neurite outgrowth. Biotech Bioeng 50: 452-461.
46. Stepien E, Stanisz J, Korohoda W, (1999) Contact guidance of chick embryo neurons on single scratches in glass and on underlying aligned human skin fibroblasts. Cell Biology International 23: 105-116.
47. Rajnicek AM, Britland S, McCaig CD, (1997) Contact guidance of CNS neurites on grooved quartz: influence of groove dimensions, neuronal age and cell type. Journal of Cell Science 110: 2905-2913.
48. Song M, Uhrich KE, (2007) Optimal micropattern dimension enhance neurite outgrowth rates, lengths, and orientations. Annals of Biomedical Engineering.
49. Rajnicek AM, Foubister LE, McCaig CD, (2006) Temporally and spatially coordinated roles for Rho, Rac, Cdc42 and their effectors in growth cone guidance by a physiological electric field. Journal of Cell Science 119: 1723-1735.
50. Schlosshauer B, Muller E, Schroder B, Planck H, Muller HW, (2003) Rat Schwann cells in bioresorbable nerve guides to promote and accelerate axonal regeneration. Brain Research 963: 321-326.
51. Dotti CG, Sullivan CA, Banker GA, (1988) The Establishment of Polarity by Hippocampal-Neurons in Culture. Journal of Neuroscience 8: 1454-1468.
52. Odde DJ, Tanaka EM, Hawkins SS, Buettner HM, (1996) Stochastic dynamics of the nerve growth cone and its microtubules during neurite outgrowth. Biotechnology and Bioengineering 50: 452-461.
53. Dent EW, Callaway JL, Szebenyi G, Baas PW, Kalil K, (1999) Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches. J Neurosci 19: 8894-8908.
54. Tanaka EM, Kirschner MW, (1991) Microtubule behaviour in the growth cones of living neurons during axon elongation. J Cell Biol 115: 345-363.
55. Ignatius MJ, Sawhney N, Gupta A, Thibadeau BM, Monteiro OR, et al. (1998) Bioactive surface coatings for nanoscale instruments: Effects on CNS neurons. J Biomed Mat Res 40: 264-274.
56. Kelly S, Regan EM, Uney JB, Dick AD, McGeehan JP, et al. (2008) Patterned growth of neuronal cells on modified diamond-like carbon substrates. Biomaterials 29: 2573-2580.
57. Schroeder A, Francz G, Bruinink A, Hauert R, Mayer J, et al. (2000) Titanium containing amorphous hydrogenated carbon films (a-C: H/Ti): surface analysis and evaluation of cellular reactions using bone marrow cell cultures in vitro. Biomaterials 21: 449-456.
58. Corey JM, Brunette AL, Chen MS, Weyhenmeyer JA, Brewer GJ, et al. (1997) Differentiated B104 neuroblastoma cells are a high-resolution assay for micropatterned substrates. J Neurosci Meth 75: 91-97.
59. Kim Y-H, Hwang E-S, Kim Y-J, (2005) Polymer/metal based flexible MEMS biosensors for nerve signal monitoring and sensitive skin. J Semiconductor Technol Sci 5: 11-16.
60. Lee TH, Pan H, Kim IS, Kim JK, Cho TH, et al. (2010) Functional Regeneration of a Severed Peripheral Nerve With a 7-mm Gap in Rats Through the Use of An Implantable Electrical Stimulator and a Conduit Electrode With Collagen Coating. Neuromodulation 13: 299-305.
61. Mahoney MJ, Chen RR, Tan J, Saltzman WM, (2005) The influence of microchannels on neurite growth and architecture. Biomaterials 26: 771-778.
62. Morelli S, Salerno S, Piscioneri A, Papenburg BJ, Di Vito A, et al. (2010) Influence of micro-patterned PLLA membranes on outgrowth and orientation of hippocampal neurites. Biomaterials 31: 7000-7011.
63. Hirono T, Torimitsu K, Kawana A, Fukuda J, (1988) Recognition of artificial microstructures by sensory nerve fibers in culture. Brain Res 446: 189-194.
64. Yao L, Wang S, Cui W, Sherlock R, O'Connell C, et al. (2009) Effect of functionalized micropatterned PLGA on guided neurite growth. Acta Biomat 5: 580-588.
65. Clark P, Conolly P, Curtis A, (1990) Topographical control of cell behaviour: II. Multiple grooved substrata. Development 108: 635-644.
66. Trumble TE, Archibald S, Allan CH, (2004) Bioengineering for nerve repair in the future. J Am Soc Surg Hand 4: 134-142.
67. Torigoe K, Tanaka H, Takahashi A, Awaya A, Hashimoto K, (1996) Basic behavior of migratory Schwann cells in peripheral nerve regeneration. Exp Neruol 137: 301-308.
68. Bozkurt A, Deumens R, Beckmann C, Olde Damink L, Schügner F, et al. (2009) In vitro cell alignment obtained with a Schwann cell enriched microstructured nerve guide with longitudinal guidance channels. Biomaterials 30: 169-179.
69. Zhang Q, Zhao Y, Yan S, Yang Y, Zhao H, et al. (2012) Preparation of uniaxial multichannel silk fibroin scaffolds for guiding primary neurons. Acta Biomaterialia 8: 11.
70. 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: 1425-1436.
71. Smeal RM, Rabbitt R, Biran R, Tresco PA, (2005) Substrate curvature influences the direction of nerve outgrowth. Annals of Biomedical Engineering 33: 376-382.