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Electrospun Fibers as Substrates for Peripheral Nerve Regeneration

  • Jörg MeyEmail author
  • Gary Brook
  • Dorothée Hodde
  • Andreas Kriebel
Chapter
Part of the Advances in Polymer Science book series (POLYMER, volume 246)

Abstract

Since axonal regeneration is possible in the peripheral nervous system, lesions can be treated by suturing disconnected nerve stumps or, when a lesion-induced gap must be bridged, by grafting an autologous nerve. However, nerve transplantations require multiple operations and cause a sensory deficit at the donor site. It is therefore desirable to develop artificial conduits for nerve regeneration as alternatives to the autograft. A core concept for the design of such implants is the incorporation of orientated nanofibers.

Artificial implants have to promote and guide axonal growth, the migration of Schwann cells, and they must not cause excessive inflammatory reactions. With hollow tubes, which are already used as nerve bridges in clinical studies, it is not possible to achieve regeneration over distances much larger than 30 mm. For this purpose, biocompatible tubes are being developed that contain orientated electrospun fibers consisting of a range of natural or synthetic materials. More recently, artificial guidance materials have been endowed with biologically active molecules. Extracellular matrix proteins or synthetic peptides that activate integrin receptors have been coupled to electrospun fibers. Other approaches adopted gradients of neurotrophins or incorporate living cells. One of the long-term goals of this research is to develop cell-free artificial implants that become integrated at the lesion site to the extent that they become populated by migrating host glia and allow a similar degree of regeneration that is supported by the autologous nerve.

Keywords

Artificial implants Biomaterials Electrospinning Extracellular matrix Growth factors Peripheral nerve Regeneration 

Abbreviations

BDNF

Brain-derived neurotrophic factor

CAM

Cell adhesion molecule

CNS

Central nervous system

CNTF

Ciliary neurotrophic factor

DRG

Dorsal root ganglion

ECM

Extracellular matrix

ePTFE

Extended poly(tetrafluoroethylene)

ErbB

Erythroblastic leukemia viral oncogen (epidermal growth factor receptor family)

FGF

Fibroblast growth factor

GDNF

Glial-derived neurotrophic factor

GFR

Receptor of GDNF-family ligands

GGF

Glial growth factor

IGF

Insulin-like growth factor

IL

Interleukin

LIF

Leukemia inhibitory factor

NGF

Nerve growth factor

NT

Neurotrophin

PAN-MA

Poly(acrylonitrile-co-methacrylate)

PCL

Poly(ε-caprolactone)

PCLEEP

Poly(caprolactone-co-ethyl ethylene phosphate)

PGA

Poly(glycolic acid)

PHB

Poly(hydroxybutyric acid)

pHEMA

Poly(2-hydroxyethyl methacrylate)

pHEMA-MMA

Poly(2-hydroxyethyl methacrylate-co-methyl methacrylate)

PLA

Poly(lactic acid); the d- and l-isomers are often referred to as PDLA, PLLA, respectively

PLGA

Poly(lactic-co-glycolic acid)

PN

Peripheral nerve

PNS

Peripheral nervous system

PPE

Polyphosphoester

PPy

Poly(pyrrole)

sPEG

Star-shaped poly(ethylene glycol)

STAT

Signal transducer and activator of transcription

TGF

Transforming growth factor

trk

Tyrosine kinase/tropomyosin receptor kinase (neurotrophin receptor)

VEGF

Vascular endothelial growth factor

Notes

Acknowledgment

A research project to develop an artificial nerve implant, conducted by JM and GB, is supported by the Deutsche Forschungsgemeinschaft (ME 1261/11-1).

References

  1. 1.
    Sunderland S (1951) Brain 74:491Google Scholar
  2. 2.
    Pabari A, Yang SY, Seifalian AM, Mosahebi A (2010) J Plast Reconstr Aesthet Surg 63:1941Google Scholar
  3. 3.
    Brenner MJ, Hess JR, Myckatyn TM, Hayashi A, Hunter DA, Mackinnon SE (2006) Laryngoscope 116:1685Google Scholar
  4. 4.
    Meek MF, Varejao AS, Geuna S (2004) Tissue Eng 10:1027Google Scholar
  5. 5.
    Deumens R, Bozkurt A, Meek MF, Marcus MAE, Joosten EAJ, Weis J, Brook GA (2010) Prog Neurobiol 92:245Google Scholar
  6. 6.
    Gu X, Ding F, Yang Y, Liu J (2011) Prog Neurobiol 93:204Google Scholar
  7. 7.
    Sulaiman OAR, Boyd JG, Gordon T (2005) Axonal regeneration in the peripheral nervous system of mammals. In: Kettenmann H, Ransom BR (eds) Neuroglia. Oxford University Press, Oxford, pp 454–466Google Scholar
  8. 8.
    Boyd JG, Gordon T (2003) Mol Neurobiol 27:277Google Scholar
  9. 9.
    Makwana M, Raivich G (2005) FEBS J 272:2628Google Scholar
  10. 10.
    Sendtner M, Stöckli KA, Thoenen H (1992) J Cell Biol 118:139Google Scholar
  11. 11.
    Heumann R, Korsching S, Bandtlow C, Thoenen H (1987) J Cell Biol 104:1623Google Scholar
  12. 12.
    Shadiack AM, Sun Y, Zigmond RE (2001) J Neurosci 21:363Google Scholar
  13. 13.
    Kanje M, Skottner A, Lundborg G, Sjoberg J (1991) Brain Res 563:285Google Scholar
  14. 14.
    Huang EJ, Reichardt LF (2001) Annu Rev Neurosci 24:677Google Scholar
  15. 15.
    Sendtner M, Kreutzberg GW, Thoenen H (1990) Nature 345:440Google Scholar
  16. 16.
    Glazner GW, Lupien S, Miller JA, Ishii DN (1993) Neuroscience 54:791Google Scholar
  17. 17.
    Emel E, Ergun SS, Kotan D, Gursoy EB, Parman Y, Zengin A, Nurten A (2011) J Neurosurg 114:522Google Scholar
  18. 18.
    Gordon T (2010) J Commun Disord 43:265Google Scholar
  19. 19.
    Hoyle GW, Mercer EH, Palmiter RD, Brinster RL (1993) Neuron 10:1019Google Scholar
  20. 20.
    Trupp M, Rydén M, Jörnvall H, Funakoshi H, Timmusk T, Arenas E, Ibánez CF (1995) J Cell Biol 130:137Google Scholar
  21. 21.
    Keast JR, Forrest SL, Osborne PB (2010) J Comp Neurol 518:3024Google Scholar
  22. 22.
    Nave KA, Salzer JL (2006) Curr Opin Neurobiol 16:492Google Scholar
  23. 23.
    Citri A, Skaria KB, Yarden Y (2003) Exp Cell Res 284:54Google Scholar
  24. 24.
    Carroll SL, Miller ML, Frohnert PW, Kim SS, Corbett JA (1997) J Neurosci 17:1642Google Scholar
  25. 25.
    Panaite PA, Barakat-Walter I (2010) J Neurosci Res 88:1751Google Scholar
  26. 26.
    Zhelyaznik N, Schrage K, McCaffery P, Mey J (2003) Eur J Neurosci 18:1033Google Scholar
  27. 27.
    Zhelyaznik N, Mey J (2006) Neuroscience 141:1761Google Scholar
  28. 28.
    Taha MO, Rosseto M, Fraga MM, Mueller SF, Fagundes DJ, Novo NF, Caricati-Neto A (2004) Transpl Proc 36:404Google Scholar
  29. 29.
    Corcoran J, Maden M (1999) Nat Neurosci 2:307Google Scholar
  30. 30.
    Corcoran J, Shroot B, Pizzey J, Maden M (2000) J Cell Sci 113:2567Google Scholar
  31. 31.
    Latasa J-J, Ituero M, Moran-González A, Aranda A, Cosgaya JM (2010) Glia 58:1451Google Scholar
  32. 32.
    Murakami M, Simons M (2008) Curr Opin Hematol 15:215Google Scholar
  33. 33.
    Pola R, Aprahamian TR, Bosch-Marce M, Curry C, Gaetani E, Flex A, Smith RC, Isner JM, Losordo DW (2004) Neurobiol Aging 25:1361Google Scholar
  34. 34.
    Pan HC, Wu HT, Cheng FC, Chen CH, Sheu ML, Chen CJ (2009) Biochem Biophys Res Commun 382:177Google Scholar
  35. 35.
    Koopmans G, Hasse B, Sinis N (2009) Int Rev Neurobiol 87:363Google Scholar
  36. 36.
    Geiger B, Bershadsky A, Pankov R, Yamada KM (2001) Nat Rev Mol Cell Biol 2:794Google Scholar
  37. 37.
    Hynes RO (1992) Cell 69:11Google Scholar
  38. 38.
    Martini R, Schachner M (1988) J Cell Biol 106:1735Google Scholar
  39. 39.
    Bixby JL, Lilien J, Reichardt LF (1988) J Cell Biol 107:353Google Scholar
  40. 40.
    Martini R (1994) J Neurocytol 23:1Google Scholar
  41. 41.
    Soares S, Traka M, von Boxberg Y, Bouquet C, Karagogeos D, Nothias F (2005) Eur J Neurosci 21:1169Google Scholar
  42. 42.
    Hasegawa M, Seto A, Uchiyama N, Kida S, Yamashima T, Yamashita J (1996) J Neuropathol Exp Neurol 55:424Google Scholar
  43. 43.
    Thornton MR, Mantovani C, Birchall MA, Terenghi G (2005) J Anat 206:69Google Scholar
  44. 44.
    Dahlin L, Lundborg G (2001) J Hand Surg Br 26:393Google Scholar
  45. 45.
    Meek MF, Jansen K (2009) J Biomed Mater Res A 89:734Google Scholar
  46. 46.
    Meek MF, Coert JH (2008) Ann Plast Surg 60:466Google Scholar
  47. 47.
    de Ruiter GC, Malessy MJ, Yaszemski MJ, Windebank AJ, Spinner RJ (2009) Neurosurg Focus 26:E5Google Scholar
  48. 48.
    Dalton PD, Mey J (2009) Front Biosci 14:769Google Scholar
  49. 49.
    de Ruiter GC, Spinner RJ, Malessy MJ, Moore MJ, Sorenson EJ, Currier BL, Yaszemski MJ, Windebank AJ (2008) Neurosurgery 63:144Google Scholar
  50. 50.
    Yao L, de Ruiter GC, Wang H, Knight AM, Spinner RJ, Yaszemski MJ, Windebank AJ, Pandit A (2010) Biomaterials 31:5789Google Scholar
  51. 51.
    Yao L, Windebank AJ, Pandit A (2010) J Biomater Sci Polym Ed 21:1081Google Scholar
  52. 52.
    Kim YT, Haftel VK, Kumar S, Bellamkonda RV (2008) Biomaterials 29:3117Google Scholar
  53. 53.
    Ribeiro-Resende VT, Koenig B, Nichterwitz S, Oberhoffner S, Schlosshauer B (2009) Biomaterials 30:5251Google Scholar
  54. 54.
    Labrador RO, Buti M, Navarro X (1998) Exp Neurol 149:243Google Scholar
  55. 55.
    Inada Y, Morimoto S, Takakura Y, Nakamura T (2004) Neurosurgery 55:640Google Scholar
  56. 56.
    Toba T, Nakamura T, Shimizu Y, Matsumoto K, Ohnishi K, Fukuda S, Yoshitani M, Ueda H, Hori Y, Endo K (2001) J Biomed Mater Res 58:622Google Scholar
  57. 57.
    Ceballos D, Navarro X, Dubey N, Wendelschafer-Crabb G, Kennedy WR, Tranquillo RT (1999) Exp Neurol 158:290Google Scholar
  58. 58.
    Möllers S, Heschel I, Damink LH, Schugner F, Deumens R, Muller B, Bozkurt A, Nava JG, Noth J, Brook GA (2009) Tissue Eng A 15:461Google Scholar
  59. 59.
    Shen H, Shen ZL, Zhang PH, Chen NL, Wang YC, Zhang ZF, Jin YQ (2010) J Biomed Mater Res B Appl Biomater 95:161Google Scholar
  60. 60.
    Chew SY, Mi R, Hoke A, Leong KW (2007) Adv Funct Mat 17:1288Google Scholar
  61. 61.
    Chiono V, Vozzi G, Vozzi F, Salvadori C, Dini F, Carlucci F, Arispici M, Burchielli S, Di SF, Geuna S, Fornaro M, Tos P, Nicolino S, Audisio C, Perroteau I, Chiaravalloti A, Domenici C, Giusti P, Ciardelli G (2009) Biomed Microdevices 11:1037Google Scholar
  62. 62.
    Bian YZ, Wang Y, Aibaidoula G, Chen GQ, Wu Q (2009) Biomaterials 30:217Google Scholar
  63. 63.
    Panseri S, Cunha C, Lowery J, Del Carro U, Taraballi F, Amadio S, Vescovi A, Gelain F (2008) BMC Biotechnol 8:39Google Scholar
  64. 64.
    Whitlock EL, Tuffaha SH, Luciano JP, Yan Y, Hunter DA, Magill CK, Moore AM, Tong AY, Mackinnon SE, Borschel GH (2009) Muscle Nerve 39:787Google Scholar
  65. 65.
    Nakamura T, Inada Y, Fukuda S, Yoshitani M, Nakada A, Itoi S, Kanemaru S, Endo K, Shimizu Y (2004) Brain Res 1027:18Google Scholar
  66. 66.
    Fan W, Gu J, Hu W, Deng A, Ma Y, Liu J, Ding F, Gu X (2008) Microsurgery 28:238Google Scholar
  67. 67.
    Inada Y, Hosoi H, Yamashita A, Morimoto S, Tatsumi H, Notazawa S, Kanemaru S, Nakamura T (2007) Neurosurgery 61:E1105–E1107Google Scholar
  68. 68.
    Lundborg G, Rosen B, Dahlin L, Danielsen N, Holmberg J (1997) J Hand Surg Am 22:99Google Scholar
  69. 69.
    Lundborg G, Rosen B, Dahlin L, Holmberg J, Rosen I (2004) J Hand Surg Br 29:100Google Scholar
  70. 70.
    Pitta MC, Wolford LM, Mehra P, Hopkin J (2001) J Oral Maxillofac Surg 59:493Google Scholar
  71. 71.
    Stanec S, Stanec Z (1998) Br J Plast Surg 51:637Google Scholar
  72. 72.
    Braga-Silva J (1999) J Hand Surg Br 24:703Google Scholar
  73. 73.
    Wangensteen KJ, Kalliainen LK (2009) J Hand NY 5:273Google Scholar
  74. 74.
    Ashley WW Jr, Weatherly T, Park TS (2006) J Neurosurg 105:452Google Scholar
  75. 75.
    Farole A, Jamal BT (2008) J Oral Maxillofac Surg 66:2058Google Scholar
  76. 76.
    Taras JS, Jacoby SM (2008) Tech Hand Up Extrem Surg 12:100Google Scholar
  77. 77.
    Lohmeyer J, Zimmermann S, Sommer B, Machens HG, Lange T, Mailänder P (2007) Chirurg 78:142Google Scholar
  78. 78.
    Moore AM, Kasukurthi R, Magill CK, Farhadi HF, Borschel GH, Mackinnon SE (2009) Hand NY 4:180Google Scholar
  79. 79.
    Weber RA, Breidenbach WC, Brown RE, Jabaley ME, Mass DP (2000) Plast Reconstr Surg 106:1036Google Scholar
  80. 80.
    Agnew SP, Dumanian GA (2010) J Hand Surg Am 35:838Google Scholar
  81. 81.
    Donoghoe N, Rosson GD, Dellon AL (2007) Microsurgery 27:595Google Scholar
  82. 82.
    Navissano M, Malan F, Carnino R, Battiston B (2005) Microsurgery 25:268Google Scholar
  83. 83.
    Bertleff MJ, Meek MF, Nicolai JP (2005) J Hand Surg Am 30:513Google Scholar
  84. 84.
    Meek MF, Nicolai JP, Robinson PH (2006) J Reconstr Microsurg 22:149Google Scholar
  85. 85.
    Clements IP, Kim Y-T, English AW, Lu X, Chung A, Bellamkonda RV (2009) Biomaterials 30:3834Google Scholar
  86. 86.
    Brown RE, Erdmann D, Lyons SF, Suchy H (1996) J Reconstr Microsurg 12:149Google Scholar
  87. 87.
    Matsumoto K, Ohnishi K, Kiyotani T, Sekine T, Eng HUM, Nakamura T, Endo K, Shimizu Y (2000) Brain Res 868:315Google Scholar
  88. 88.
    Ding F, Wu J, Yang Y, Hu W, Zhu Q, Tang X, Liu J, Gu X (2010) Tissue Eng A 16:3779Google Scholar
  89. 89.
    Siemionow M, Bozkurt M, Zor F (2010) Microsurgery 30:574Google Scholar
  90. 90.
    Lundborg G, Dahlin L, Dohi D, Kanje M, Terada N (1997) J Hand Surg Br 22:299Google Scholar
  91. 91.
    Smeal RM, Rabbitt R, Biran R, Tresco PA (2005) Ann Biomed Eng 33:376Google Scholar
  92. 92.
    Teo WE, Ramakrishna S (2006) Nanotechnology 17:R89–R106Google Scholar
  93. 93.
    Schnell E, Klinkhammer K, Balzer S, Brook GA, Klee D, Dalton PD, Mey J (2007) Biomaterials 28:3012Google Scholar
  94. 94.
    Klinkhammer K, Seiler N, Grafahrend D, Mey J, Brook GA, Möller M, Dalton PD, Klee D (2009) Tissue Eng 15:77Google Scholar
  95. 95.
    Matthews JA, Wnek GE, Simpson DG, Bowlin GL (2002) Biomacromolecules 3:232Google Scholar
  96. 96.
    Chew SY, Wen J, Yim EK, Leong KW (2005) Biomacromolecules 6:2017Google Scholar
  97. 97.
    Gerardo-Nava J, Führmann T, Klinkhammer K, Seiler N, Mey J, Klee D, Möller M, Dalton PD, Brook GA (2008) Nanomedicine 4:11Google Scholar
  98. 98.
    Bockelmann J, Klinkhammer K, von Holst A, Seiler N, Faissner A, Brook GA, Klee D, Mey J (2011) Tissue Eng A 17:475Google Scholar
  99. 99.
    Lietz M, Dreesmann L, Hoss M, Oberhoffner S, Schlosshauer B (2006) Biomaterials 27:1425Google Scholar
  100. 100.
    Wang X, Hu W, Cao Y, Yao J, Hu J, Gu X (2005) Brain 128:1897Google Scholar
  101. 101.
    Cao H, Liu T, Chew SY (2009) Adv Drug Deliv Rev 61:1055Google Scholar
  102. 102.
    Gelain F, Horii A, Zhang S (2007) Macromol Biosci 7:544Google Scholar
  103. 103.
    Gelain F, Unsworth LD, Zhang S (2010) J Control Release 145:231Google Scholar
  104. 104.
    Holmes TC, de Lacalle S, Su X, Liu G, Rich A, Zhang S (2000) Proc Natl Acad Sci USA 97:6728Google Scholar
  105. 105.
    Silva GA, Czeisler C, Niece KL, Beniash E, Harrington DA, Kessler JA, Stupp SI (2004) Science 203:1352Google Scholar
  106. 106.
    Ellis-Behnke RG, Liang YX, You SW, Tay DK, Zhang S, So KF, Schneider GE (2006) Proc Natl Acad Sci USA 103:5054Google Scholar
  107. 107.
    McGrath AM, Novikova LN, Novikov LN, Wiberg M (2010) Brain Res Bull 83:207Google Scholar
  108. 108.
    Guo J, Su H, Zeng Y, Liang YX, Wong WM, Ellis-Behnke RG, So KF, Wu W (2007) Nanomedicine 3:311Google Scholar
  109. 109.
    Verdu E, Labrador RO, Rodriguez FJ, Ceballos D, Fores J, Navarro X (2002) Restor Neurol Neurosci 20:169Google Scholar
  110. 110.
    Dubey N, Letourneau PC, Tranquillo RT (1999) Exp Neurol 158:338Google Scholar
  111. 111.
    Bozkurt A, Brook GA, Moellers S, Lassner F, Sellhaus B, Weis J, Woeltje M, Tank J, Beckmann C, Fuchs P, Damink LO, Schugner F, Heschel I, Pallua N (2007) Tissue Eng 13:2971Google Scholar
  112. 112.
    Bozkurt A, Deumens R, Beckmann C, Olde Damink L, Schugner F, Heschel I, Sellhaus B, Weis J, Jahnen-Dechent W, Brook GA, Pallua N (2009) Biomaterials 30:169Google Scholar
  113. 113.
    Hood B, Levene HB, Levi AD (2009) Neurosurg Focus 26:E4Google Scholar
  114. 114.
    Radtke C, Wewetzer K, Reimers K, Vogt PM (2011) Cell Transplant 20:145–152Google Scholar
  115. 115.
    Lago N, Casas C, Muir EM, Rogers J, Navarro X (2009) Restor Neurol Neurosci 27:67Google Scholar
  116. 116.
    Schmidt CE, Baier Leach J (2003) Annu Rev Biomed Eng 5:293Google Scholar
  117. 117.
    Sørensen J, Haase G, Krarup C, Gilgenkrantz H, Kahn A, Schmalbruch H (1998) Ann Neurol 43:205Google Scholar
  118. 118.
    Radtke C, Akiyama Y, Lankford KL, Vogt PM, Krause DS, Kocsis JD (2005) Neurosci Lett 387:85Google Scholar
  119. 119.
    Guenard V, Kleitman N, Morrissey TK, Bunge RP, Aebischer P (1992) J Neurosci 12:3310Google Scholar
  120. 120.
    Kim DH, Connolly SE, Kline DG, Voorhies RM, Smith A, Posell M, Yoes T, Daniloff JK (1994) J Neurosurg 80:254Google Scholar
  121. 121.
    Lohmeyer JA, Shen ZL, Walter GF, Berger A (2007) Int J Artif Organs 30:64Google Scholar
  122. 122.
    Sinis N, Schaller HE, Becker ST, Schlosshauer B, Doser M, Roesner H, Oberhoffner S, Muller HW, Haerle M (2007) Restor Neurol Neurosci 25:131Google Scholar
  123. 123.
    May F, Weidner N, Matiasek K, Caspers C, Mrva T, Vroemen M, Henke J, Lehmer A, Schwaibold H, Erhardt W, Gänsbacher B, Hartung R (2004) J Urol 172:374Google Scholar
  124. 124.
    Kawaja MD, Boyd JG, Smithson LJ, Jahed A, Doucette R (2009) J Neurotrauma 26:155Google Scholar
  125. 125.
    Chamberlain LJ, Yannas IV, Hsu HP, Strichartz G, Spector M (1998) Exp Neurol 154:315Google Scholar
  126. 126.
    Pankov R, Yamada KM (2002) J Cell Sci 115:3861Google Scholar
  127. 127.
    Bailey SB, Eichler ME, Villadiego A, Rich KM (1993) J Neurocytol 22:176Google Scholar
  128. 128.
    Hersel U, Dahmen C, Kessler H (2003) Biomaterials 24:4385Google Scholar
  129. 129.
    Yang Y, Chen X, Ding F, Zhang P, Liu J, Gu X (2007) Biomaterials 28:1643Google Scholar
  130. 130.
    Madduri S, Papaloizos M, Gander B (2010) Biomaterials 31:2323Google Scholar
  131. 131.
    Yang Y, Ding F, Wu J, Hu W, Liu W, Liu J, Gu X (2007) Biomaterials 28:5526Google Scholar
  132. 132.
    Itoh S, Matsuda A, Kobayashi H, Ichinose S, Shinomiya K, Tanaka J (2005) J Biomed Mater Res B Appl Biomater 73:375Google Scholar
  133. 133.
    Wang W, Itoh S, Matsuda A, Aizawa T, Demura M, Ichinose S, Shinomiya K, Tanaka J (2008) J Biomed Mater Res A 85:919Google Scholar
  134. 134.
    Huang J, Lu L, Hu X, Ye Z, Peng Y, Yan X, Geng D, Luo Z (2010) Neurorehabil Neural Repair 24:736Google Scholar
  135. 135.
    Yang Y, Gu X, Tan R, Hu W, Wang X, Zhang P, Zhang T (2004) Biotechnol Lett 26:1793Google Scholar
  136. 136.
    Suzuki K, Suzuki Y, Ohnishi K, Endo K, Tanihara M, Nishimura Y (1999) Neuroreport 10:2891Google Scholar
  137. 137.
    Ohta M, Suzuki Y, Chou H, Ishikawa N, Suzuki S, Tanihara M, Suzuki Y, Mizushima Y, Dezawa M, Ide C (2004) J Biomed Mater Res A 71:661Google Scholar
  138. 138.
    Suzuki K, Suzuki Y, Tanihara M, Ohnishi K, Hashimoto T, Endo K, Nishimura Y (2000) J Biomed Mater Res 49:528Google Scholar
  139. 139.
    Mohanna PN, Young RC, Wiberg M, Terenghi G (2003) J Anat 203:553Google Scholar
  140. 140.
    Mohanna PN, Terenghi G, Wiberg M (2005) Scand J Plast Reconstr Surg Hand Surg 39:129Google Scholar
  141. 141.
    Ozgenel GY (2003) Microsurgery 23:575Google Scholar
  142. 142.
    Suri S, Schmidt CE (2010) Tissue Eng A 16:1703Google Scholar
  143. 143.
    Zhang S, Holmes T, Lockshin C, Rich A (1993) Proc Natl Acad Sci USA 90:3334Google Scholar
  144. 144.
    Rafiuddin AM, Jayakumar R (2003) Brain Res 993:208Google Scholar
  145. 145.
    Lundborg G, Dahlin LB, Danielsen N, Gelberman RH, Longo FM, Powell HC, Varon S (1982) Exp Neurol 76:361Google Scholar
  146. 146.
    Dodla MC, Bellamkonda RV (2008) Biomaterials 29:33Google Scholar
  147. 147.
    Yang F, Murugan R, Wang S, Ramakrishna S (2005) Biomaterials 26:2603Google Scholar
  148. 148.
    Liu JJ, Wang CY, Wang JG, Ruan HJ, Fan CY (2011) J Biomed Mater Res A 96:13Google Scholar
  149. 149.
    Ichihara S, Inada Y, Nakada A, Endo K, Azuma T, Nakai R, Tsutsumi S, Kurosawa H, Nakamura T (2009) Tissue Eng C Meth 15:387Google Scholar
  150. 150.
    Bini TB, Gao S, Tan TC, Wang S, Lim A, Hai LB, Ramakrishna S (2004) Nanotechnology 15:1459Google Scholar
  151. 151.
    Yucel D, Kose GT, Hasirci V (2010) Biomaterials 31:1596Google Scholar
  152. 152.
    Wang S, Yaszemski MJ, Knight AM, Gruetzmacher JA, Windebank AJ, Lu L (2009) Acta Biomater 5:1531Google Scholar
  153. 153.
    Aberg M, Ljungberg C, Edin E, Millqvist H, Nordh E, Theorin A, Terenghi G, Wiberg M (2009) J Plast Reconstr Aesthet Surg 62:1503Google Scholar
  154. 154.
    Cai J, Peng X, Nelson KD, Eberhart R, Smith GM (2005) J Biomed Mater Res A 75:374Google Scholar
  155. 155.
    Oliveira JT, Almeida FM, Biancalana A, Baptista AF, Tomaz MA, Melo PA, Martinez AM (2010) Neuroscience 170:1295Google Scholar
  156. 156.
    Novikova LN, Pettersson J, Brohlin M, Wiberg M, Novikov LN (2008) Biomaterials 29:1198Google Scholar
  157. 157.
    Wang S, Wan AC, Xu X, Gao S, Mao HQ, Leong KW, Yu H (2001) Biomaterials 22:1157Google Scholar
  158. 158.
    Klinkhammer K, Bockelmann J, Simitzis C, Brook GA, Grafahrend D, Groll J, Möller M, Mey J, Klee D (2010) J Mater Sci Mater Med 21:2637Google Scholar
  159. 159.
    Grafahrend D, Heffels KH, Beer MV, Gasteier P, Moller M, Boehm G, Dalton PD, Groll J (2011) Nat Mater 10:67Google Scholar
  160. 160.
    Tsai EC, Dalton PD, Shoichet MS, Tator CH (2004) J Neurotrauma 21:789Google Scholar
  161. 161.
    Belkas JS, Munro CA, Shoichet MS, Midha R (2005) Restor Neurol Neurosci 23:19Google Scholar
  162. 162.
    Belkas JS, Munro CA, Shoichet MS, Johnston M, Midha R (2005) Biomaterials 26:1741Google Scholar
  163. 163.
    Yu TT, Shoichet MS (2005) Biomaterials 26:1507Google Scholar
  164. 164.
    Lee JY, Bashur CA, Goldstein AS, Schmidt CE (2009) Biomaterials 30:4325Google Scholar
  165. 165.
    Gomez N, Schmidt CE (2007) J Biomed Mater Res A 81:135Google Scholar
  166. 166.
    Schmidt CE, Shastri VR, Vacanti JP, Langer R (1997) Proc Natl Acad Sci USA 94:8948Google Scholar
  167. 167.
    George PM, Saigal R, Lawlor MW, Moore MJ, LaVan DA, Marini RP, Selig M, Makhni M, Burdick JA, Langer R, Kohane DS (2009) J Biomed Mater Res A 91:519Google Scholar
  168. 168.
    Wang X, Gu X, Yuan C, Chen S, Zhang P, Zhang T, Yao J, Chen F, Chen G (2004) J Biomed Mater Res A 68:411Google Scholar
  169. 169.
    Koh HS, Yong T, Chan CK, Ramakrishna S (2008) Biomaterials 29:3574Google Scholar
  170. 170.
    Zhang YZ, Venugopal J, Huang ZM, Lim CT, Ramakrishna S (2005) Biomacromolecules 6:2583Google Scholar
  171. 171.
    Heydarkhan-Hagvall S, Schenke-Layland K, Dhanasopon AP, Rofail F, Smith H, Wu BM, Shemin R, Beygui RE, Maclellan WR (2008) Biomaterials 29:2907Google Scholar
  172. 172.
    Webb K, Budko E, Neuberger TJ, Chen S, Schachner M, Tresco PA (2001) Biomaterials 22:1017Google Scholar
  173. 173.
    Aebischer P, Salessiotis AN, Winn SR (1989) J Neurosci Res 23:282Google Scholar
  174. 174.
    Madduri S, Feldman K, Tervoort T, Papaloizos M, Gander B (2010) J Control Release 143:168Google Scholar
  175. 175.
    Moore K, MacSween M, Shoichet M (2006) Tissue Eng 12:267Google Scholar
  176. 176.
    Forsten-Williams K, Chu CL, Fannon M, Buczek-Thomas JA, Nugent MA (2008) Ann Biomed Eng 36:2134Google Scholar
  177. 177.
    Barnett MW, Fisher CE, Perona-Wright G, Davies JA (2002) J Cell Sci 115:4495Google Scholar
  178. 178.
    Kokai LE, Bourbeau D, Weber DJ, McAtee J, Marra K (2011) Tissue Eng Part A 17:1263–1275Google Scholar
  179. 179.
    Xu X, Yee WC, Hwang PY, Yu H, Wan AC, Gao S, Boon KL, Mao HQ, Leong KW, Wang S (2003) Biomaterials 24:2405Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Jörg Mey
    • 1
    • 2
    Email author
  • Gary Brook
    • 3
  • Dorothée Hodde
    • 3
  • Andreas Kriebel
    • 2
  1. 1.Hospital Nacional de Parapléjicos, SESCAMToledoSpain
  2. 2.Institut für Biologie IIRWTH Aachen UniversityAachenGermany
  3. 3.Institut für NeuropathologieRWTH Aachen UniversityAachenGermany

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