Advances in peripheral nerve regeneration

Nature Reviews Neurology

Volumn 9, Issue 12, 2013, Pages 668-676

  Scheib, Jami ^a   Höke, Ahmet ^a  

^a JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; LEVACECARNINE; NEUROTROPHIC FACTOR; PROTEIN C JUN; PROTEOCHONDROITIN SULFATE; TRANSCRIPTION FACTOR;

APOPTOSIS; BASEMENT MEMBRANE; EXTRACELLULAR MATRIX; HUMAN; IMMUNOMODULATION; MACROPHAGE; MUSCLE DENERVATION; NERVE FIBER DEGENERATION; NERVE FIBER GROWTH; NERVE REGENERATION; NERVE SPROUTING; NERVE TRANSECTION; NEURAL STEM CELL TRANSPLANTATION; NEUROPROTECTION; NONHUMAN; PERIPHERAL NERVE INJURY; PHENOTYPIC VARIATION; PRIORITY JOURNAL; RETROGRADE NERVE FIBER TRANSPORT; REVIEW; SCHWANN CELL; SPINAL GANGLION;

ANIMALS; AXONS; DISEASE MODELS, ANIMAL; HUMANS; MICE; NERVE REGENERATION; PERIPHERAL NERVE INJURIES; PERIPHERAL NERVES; RATS; SCHWANN CELLS;

EID: 84890121474     PISSN: 17594758     EISSN: 17594766     Source Type: Journal    
DOI: 10.1038/nrneurol.2013.227     Document Type: Review

References (118)

1. Sunderland, S. Factors influencing the course of regeneration and quality of recovery after nerve suture. Brain 75, 19-54 (1952)
2. Sunderland, S. Nerves and Nerve Injuries (Churchill Livingstone, 1978)
3. Brushart, T. M. Nerve Repair (Oxford University Press, 2011)
4. Woodhall, B. & Beebe, G. W. Peripheral nerve regeneration: A follow-up study of 3,656 World War II injuries (U.S. Government Printing Office, 1956)
5. Wujek, J. R. & Lasek, R. J. Correlation of axonal regeneration and slow component B in two branches of a single axon. J. Neurosci. 2, 243-251 (1983) (Pubitemid 13125703)
6. Buchthal, F. & Kühl, V. Nerve conduction, tactile sensibility, and the electromyogram after suture or compression of peripheral nerve: A longitudinal study in man. J. Neurol. Neurosurg. Psychiatry 42, 436-451 (1979) (Pubitemid 9158949)
7. Dolenc, V. & Janko, M. Nerve regeneration following primary repair. Acta Neurochir. 34, 223-234 (1976)
8. Fu, S. Y. & Gordon, T. Contributing factors to poor functional recovery after delayed nerve repair: Prolonged axotomy. J. Neurosci. 15, 3876-3885 (1995)
9. Sulaiman, O. A. & Gordon, T. Effects of short-and long-term Schwann cell denervation on peripheral nerve regeneration, myelination, and size. Glia 32, 234-246 (2000)
10. Ide, C. Peripheral nerve regeneration. Neurosci. Res. 25, 101-121 (1996) (Pubitemid 26232009)
11. Hoke, A. Mechanisms of disease: what factors limit the success of peripheral nerve regeneration in humans Nat. Clin. Pract. Neurol. 2, 448-454 (2006) (Pubitemid 44137946)
12. Anzil, A. P. & Wernig, A. Muscle fibre loss and reinnervation after long-term denervation. J. Neurocytol. 18, 833-845 (1989) (Pubitemid 20011385)
13. Ma, C. H. et al. Accelerating axonal growth promotes motor recovery after peripheral nerve injury in mice. J. Clin. Invest. 121, 4332-4347 (2011)
14. Richardson, P. M., McGuinness, U. M. & Aguayo, A. J. Axons from CNS neurons regenerate into PNS grafts. Nature 284, 264-265 (1980) (Pubitemid 10112047)
15. David, S. & Aguayo, A. J. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214, 931-933 (1981) (Pubitemid 12220099)
16. Filbin, M. T. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 4, 703-713 (2003) (Pubitemid 37280150)
17. Huebner, E. A. & Strittmatter, S. M. Axon regeneration in the peripheral and central nervous systems. Results Probl. Cell Differ. 48, 339-351 (2009)
18. Vargas, M. E. & Barres, B. A. Why is Wallerian degeneration in the CNS so slow Annu. Rev. Neurosci. 30, 153-179 (2007) (Pubitemid 47218754)
19. Ludwin, S. K. Oligodendrocyte survival in Wallerian degeneration. Acta Neuropathol. 80, 184-191 (1990) (Pubitemid 20196809)
20. He, Z. & Koprivica, V. The Nogo signaling pathway for regeneration block. Annu. Rev. Neurosci. 27, 341-368 (2004) (Pubitemid 39050407)
21. Lu, P. et al. Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell 150, 1264-1273 (2012)
22. Hanz, S. et al. Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40, 1095-1104 (2003) (Pubitemid 38032787)
23. Ben-Yaakov, K. et al. Axonal transcription factors signal retrogradely in lesioned peripheral nerve. EMBO J. 31, 1350-1363 (2012)
24. Perry, R. B. et al. Subcellular knockout of importin 1 perturbs axonal retrograde signaling. Neuron 75, 294-305 (2012)
25. Rosenberg, A. F., Wolman, M. A., Franzini-Armstrong, C. & Granato, M. In vivo nerve-macrophage interactions following peripheral nerve injury. J. Neurosci. 32, 3898-3909 (2012)
26. Conforti, L. et al. A Ufd2/D4Cole1e chimeric protein and overexpression of Rbp7 in the slow Wallerian degeneration (WldS) mouse. Proc. Natl Acad. Sci. USA 97, 11377-11382 (2000)
27. Lunn, E. R., Perry, V. H., Brown, M. C., Rosen, H. & Gordon, S. Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve. Eur. J. Neurosci. 1, 27-33 (1989) (Pubitemid 19142026)
28. Perry, V. H., Brown, M. C., Lunn, E. R., Tree, P. & Gordon, S. Evidence that very slow Wallerian degeneration in C57BL/Ola mice is an intrinsic property of the peripheral nerve. Eur. J. Neurosci. 2, 802-808 (1990) (Pubitemid 20314475)
29. Glass, J. D., Brushart, T. M., George, E. B. & Griffin, J. W. Prolonged survival of transected nerve fibres in C57BL/Ola mice is an intrinsic characteristic of the axon. J. Neurocytol. 22, 311-321 (1993) (Pubitemid 23162784)
30. Gillingwater, T. H. et al. Delayed synaptic degeneration in the CNS of WldS mice after cortical lesion. Brain 129, 1546-1556 (2006) (Pubitemid 43999386)
31. Benavides, E. & Alvarez, J. Peripheral axons of WldS mice, which regenerate after a delay of several weeks, do so readily when transcription is inhibited in the distal stump. Neurosci. Lett. 258, 77-80 (1998) (Pubitemid 28566178)
32. Bisby, M. A. & Chen, S. Delayed Wallerian degeneration in sciatic nerves of C57BL/Ola mice is associated with impaired regeneration of sensory axons. Brain Res. 530, 117-120 (1990) (Pubitemid 20348586)
33. Mack, T. G. et al. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 4, 1199-1206 (2001) (Pubitemid 33135625)
34. Avery, M. A. et al. WldS prevents axon degeneration through increased mitochondrial flux and enhanced mitochondrial Ca2+ buffering. Curr. Biol. 22, 596-600 (2012)
35. George, E. B., Glass, J. D. & Griffin, J. W. Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels. J. Neurosci. 15, 6445-6452 (1995)
36. Adalbert, R. et al. Intra-axonal calcium changes after axotomy in wild-type and slow Wallerian degeneration axons. Neuroscience 225, 44-54 (2012)
37. Wang, X. et al. The role of abnormal mitochondrial dynamics in the pathogenesis of Alzheimer's disease. J. Neurochem. 109 (Suppl. 1), 153-159 (2009)
38. Yi, M., Weaver, D. & Hajnoczky, G. Control of mitochondrial motility and distribution by the calcium signal: A homeostatic circuit. J. Cell Biol. 167, 661-672 (2004) (Pubitemid 39565147)
39. Osterloh, J. M. et al. dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science 337, 481-484 (2012)
40. Akhouayri, I., Turc, C., Royet, J. & Charroux, B. Toll8/Tollo negatively regulates antimicrobial response in the Drosophila respiratory epithelium. PLoS Pathog. 7, e1002319 (2011)
41. Hoke, A., Gordon, T., Zochodne, D. W. & Sulaiman, O. A. A decline in glial celllinederived neurotrophic factor expression is associated with impaired regeneration after long-term Schwann cell denervation. Exp. Neurol. 173, 77-85 (2002) (Pubitemid 34081727)
42. You, S., Petrov, T., Chung, P. H. & Gordon, T. The expression of the low affinity nerve growth factor receptor in long-term denervated Schwann cells. Glia 20, 87-100 (1997) (Pubitemid 27253202)
43. Rahmatullah, M. et al. Synergistic regulation of Schwann cell proliferation by heregulin and forskolin. Mol. Cell Biol. 18, 6245-6252 (1998) (Pubitemid 28500515)
44. Chen, Z. L., Yu, W. M. & Strickland, S. Peripheral regeneration. Annu. Rev. Neurosci. 30, 209-233 (2007) (Pubitemid 47218756)
45. Murinson, B. B., Archer, D. R., Li, Y. & Griffin, J. W. Degeneration of myelinated efferent fibers prompts mitosis in Remak Schwann cells of uninjured Cfiber afferents. J. Neurosci. 25, 1179-1187 (2005) (Pubitemid 40268959)
46. Hu, X. et al. Bace1 modulates myelination in the central and peripheral nervous system. Nat. Neurosci. 9, 1520-1525 (2006) (Pubitemid 44862660)
47. Willem, M. et al. Control of peripheral nerve myelination by the secretase BACE1. Science 314, 664-666 (2006) (Pubitemid 44646394)
48. Mei, L. & Xiong, W. C. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat. Rev. Neurosci. 9, 437-452 (2008) (Pubitemid 351704944)
49. Woodhoo, A. et al. Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat. Neurosci. 12, 839-847 (2009)
50. Jessen, K. R. & Mirsky, R. Negative regulation of myelination: Relevance for development, injury, and demyelinating disease. Glia 56, 1552-1565 (2008)
51. Arthur-Farraj, P. J. et al. cJun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron 75, 633-647 (2012)
52. Viader, A., Chang, L. W., Fahrner, T., Nagarajan, R. & Milbrandt, J. MicroRNAs modulate Schwann cell response to nerve injury by reinforcing transcriptional silencing of dedifferentiation-related genes. J. Neurosci. 31, 17358-17369 (2011)
53. Kim, H. A., Ratner, N., Roberts, T. M. & Stiles, C. D. Schwann cell proliferative responses to cAMP and Nf1 are mediated by cyclin D1. J. Neurosci. 21, 1110-1116 (2001) (Pubitemid 32128756)
54. Weinberg, H. J. & Spencer, P. S. The fate of Schwann cells isolated from axonal contact. J. Neurocytol. 7, 555-569 (1978) (Pubitemid 9040730)
55. Bain, J. R., Veltri, K. L., Chamberlain, D. & Fahnestock, M. Improved functional recovery of denervated skeletal muscle after temporary sensory nerve innervation. Neuroscience 103, 503-510 (2001) (Pubitemid 32201936)
56. Aird, R. B. & Naffziger, H. C. The pathology of human striated muscle following denervation. J. Neurosurg. 10, 216-227 (1953)
57. Eberstein, A. & Eberstein, S. Electrical stimulation of denervated muscle: Is it worthwhile Med. Sci. Sports Exerc. 28, 1463-1469 (1996) (Pubitemid 26424669)
58. Gordon, T., Tyreman, N. & Raji, M. A. The basis for diminished functional recovery after delayed peripheral nerve repair. J. Neurosci. 31, 5325-5334 (2011)
59. Hoke, A. A (heat) shock to the system promotes peripheral nerve regeneration. J. Clin. Invest. 121, 4231-4234 (2011)
60. Park, K. K. et al. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 322, 963-966 (2008)
61. Smith, P. D. et al. SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron 64, 617-623 (2009)
62. Sun, F. et al. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 480, 372-375 (2011)
63. Christie, K. J., Webber, C. A., Martinez, J. A., Singh, B. & Zochodne, D. W. PTEN inhibition to facilitate intrinsic regenerative outgrowth of adult peripheral axons. J. Neurosci. 7, 9306-9315 (2010)
64. Patodia, S. & Raivich, G. Role of transcription factors in peripheral nerve regeneration. Front. Mol. Neurosci. 5, 8 (2012)
65. Tsujino, H. et al. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: A novel neuronal marker of nerve injury. Mol. Cell. Neurosci. 15, 170-182 (2000) (Pubitemid 30109120)
66. Bloechlinger, S., Karchewski, L. A. & Woolf, C. J. Dynamic changes in glypican1 expression in dorsal root ganglion neurons after peripheral and central axonal injury. Eur. J. Neurosci. 19, 1119-1132 (2004) (Pubitemid 38387190)
67. Seijffers, R., Mills, C. D. & Woolf, C. J. ATF3 increases the intrinsic growth state of DRG neurons to enhance peripheral nerve regeneration. J. Neurosci. 27, 7911-7920 (2007) (Pubitemid 47173306)
68. Benn, S. C. et al. Hsp27 upregulation and phosphorylation is required for injured sensory and motor neuron survival. Neuron 36, 45-56 (2002)
69. Nakagomi, S., Suzuki, Y., Namikawa, K., Kiryu-Seo, S. & Kiyama, H. Expression of the activating transcription factor 3 prevents cJun Nterminal kinase-induced neuronal death by promoting heat shock protein 27 expression and Akt activation. J. Neurosci. 23, 5187-5196 (2003) (Pubitemid 36793247)
70. Ross, A. F., Oleynikov, Y., Kislauskis, E. H., Taneja, K. L. & Singer, R. H. Characterization of a actin mRNA zipcode-binding protein. Mol. Cell. Biol. 17, 2158-2165 (1997) (Pubitemid 27133302)
71. Welshhans, K. & Bassell, G. J. Netrin1induced local actin synthesis and growth cone guidance requires zipcode binding protein J. Neurosci. 31, 9800-9813 (2011)
72. Sasaki, Y. et al. Phosphorylation of zipcode binding protein 1 is required for brain-derived neurotrophic factor signaling of local actin synthesis and growth cone turning. J. Neurosci. 30, 9349-9358 (2010)
73. Donnelly, C. J. et al. Limited availability of ZBP1 restricts axonal mRNA localization and nerve regeneration capacity. EMBO J. 30, 4665-4677 (2011)
74. Zuo, J., Hernandez, Y. J. & Muir, D. Chondroitin sulfate proteoglycan with neurite-inhibiting activity is up-regulated following peripheral nerve injury. J. Neurobiol. 34, 41-54 (1998) (Pubitemid 28032425)
75. Zuo, J. et al. Regeneration of axons after nerve transection repair is enhanced by degradation of chondroitin sulfate proteoglycan. Exp. Neurol. 176, 221-228 (2002) (Pubitemid 34762122)
76. Heine, W., Conant, K., Griffin, J. W. & Hoke, A. Transplanted neural stem cells promote axonal regeneration through chronically denervated peripheral nerves. Exp. Neurol. 189, 231-240 (2004) (Pubitemid 39221818)
77. Singh, B. et al. Accelerated axon outgrowth, guidance, and target reinnervation across nerve transection gaps following a brief electrical stimulation paradigm. J. Neurosurg. 116, 498-512 (2012)
78. Gordon, T., Sulaiman, O. A. & Ladak, A. Chapter 24: Electrical stimulation for improving nerve regeneration: where do we stand Int. Rev. Neurobiol. 87, 433-444 (2009)
79. Ma, J., Novikov, L. N., Wiberg, M. & Kellerth, J. O. Delayed loss of spinal motoneurons after peripheral nerve injury in adult rats: A quantitative morphological study. Exp. Brain Res. 139, 216-223 (2001) (Pubitemid 32661531)
80. Hu, P. & McLachlan, E. M. Selective reactions of cutaneous and muscle afferent neurons to peripheral nerve transection in rats. J. Neurosci. 23, 10559-10567 (2003) (Pubitemid 37485269)
81. Terenghi, G., Hart, A. & Wiberg, M. The nerve injury and the dying neurons: Diagnosis and prevention. J. Hand Surg. Eur. 36, 730-734 (2011)
82. Groves, M. J., Christopherson, T., Giometto, B. & Scaravilli, F. Axotomy-induced apoptosis in adult rat primary sensory neurons. J. Neurocytol. 26, 615-624 (1997) (Pubitemid 27431748)
83. Vestergaard, S., Tandrup, T. & Jakobsen, J. Effect of permanent axotomy on number and volume of dorsal root ganglion cell bodies. J. Comp. Neurol. 388, 307-312 (1997) (Pubitemid 27471502)
84. McKay Hart, A., Brannstrom, T., Wiberg, M. & Terenghi, G. Primary sensory neurons and satellite cells after peripheral axotomy in the adult rat: Timecourse of cell death and elimination. Exp. Brain Res. 142, 308-318 (2002) (Pubitemid 34117811)
85. Gu, Y., Spasic, Z. & Wu, W. The effects of remaining axons on motoneuron survival and NOS expression following axotomy in the adult rat. Dev. Neurosci. 19, 255-259 (1997) (Pubitemid 27230843)
86. Suzuki, H. et al. A quantitative pathological investigation of the cervical cord, roots and ganglia after long-term amputation of the unilateral upper arm. Acta Neuropathol. 85, 666-673 (1993) (Pubitemid 23212036)
87. Reid, A. J., Shawcross, S. G., Hamilton, A. E., Wiberg, M. & Terenghi, G. Nacetylcysteine alters apoptotic gene expression in axotomised primary sensory afferent subpopulations. Neurosci. Res. 65, 148-155 (2009)
88. Lin, C. R. et al. GADD45A protects against cell death in dorsal root ganglion neurons following peripheral nerve injury. J. Neurosci. Res. 89, 689-99 (2011)
89. Zhang, C. G. et al. Motorneuron protection by Nacetylcysteine after ventral root avulsion and ventral rhizotomy. Br. J. Plast. Surg. 58, 765-773 (2005)
90. Hart, A. M., Terenghi, G., Kellerth, J. O. & Wiberg, M. Sensory neuroprotection, mitochondrial preservation, and therapeutic potential of Nacetylcysteine after nerve injury. Neuroscience 125, 91-101 (2004) (Pubitemid 38402162)
91. Wilson, A. D., Hart, A., Wiberg, M. & Terenghi, G. Acetyllcarnitine increases nerve regeneration and target organ reinnervation - a morphological study. J. Plast. Reconstr. Aesthet. Surg. 63, 1186-1195 (2010)
92. Bernard, G. R. Nacetylcysteine in experimental and clinical acute lung injury. Am. J. Med. 30, S54-S59 (1991)
93. Mueller, M. et al. Rapid response of identified resident endoneurial macrophages to nerve injury. Am. J. Pathol. 159, 2187-2197 (2001) (Pubitemid 33104273)
94. Reichert, F., Saada, A. & Rotshenker, S. Peripheral nerve injury induces Schwann cells to express two macrophage phenotypes: Phagocytosis and the galactose-specific lectin MAC2. J. Neurosci. 14, 3231-3245 (1994) (Pubitemid 24139006)
95. Perry, V. H., Tsao, J. W., Fearn, S. & Brown, M. C. Radiation-induced reductions in macrophage recruitment have only slight effects on myelin degeneration in sectioned peripheral nerves of mice. Eur. J. Neurosci. 7, 271-280 (1995)
96. Barrette, B. et al. Requirement of myeloid cells for axon regeneration. J. Neurosci. 28, 9363-9376 (2008).
97. Rotshenker, S. Wallerian degeneration: The innate-immune response to traumatic nerve injury. J. Neuroinflammation 8, 109 (2011)
98. Beuche, W. & Friede, R. L. Myelin phagocytosis in Wallerian degeneration of peripheral nerves depends on silica-sensitive, bg/bg-negative and Fc-positive monocytes. Brain Res. 378, 97-106 (1986) (Pubitemid 16055804)
99. Bahr, M. & Przyrembel, C. Myelin from peripheral and central nervous system is a nonpermissive substrate for retinal ganglion cell axons. Exp. Neurol. 134, 87-93 (1995)
100. Shen, Y. J., DeBellard, M. E., Salzer, J. L., Roder, J. & Filbin, M. T. Myelin-associated glycoprotein in myelin and expressed by Schwann cells inhibits axonal regeneration and branching. Mol. Cell. Neurosci. 12, 79-91 (1998) (Pubitemid 28524292)
101. Mueller, M. et al. Macrophage response to peripheral nerve injury: The quantitative contribution of resident and hematogenous macrophages. Lab. Invest. 83, 175-185 (2003) (Pubitemid 36255363)
102. Griffin, J. W., George, R. & Ho, T. Macrophage systems in peripheral nerves. A review. J. Neuropathol. Exp. Neurol. 52, 553-560 (1993) (Pubitemid 23335730)
103. Brown, M. C., Perry, V. H., Lunn, E. R., Gordon, S. & Heumann, R. Macrophage dependence of peripheral sensory nerve regeneration: Possible involvement of nerve growth factor. Neuron 6, 359-370 (1991)
104. Heumann, R., Korsching, S., Bandtlow, C. & Thoenen, H. Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J. Cell Biol. 104, 1623-1631 (1987) (Pubitemid 17104532)
105. Mosser, D. M. & Edwards, J. P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8, 958-969 (2008)
106. Gratchev, A. et al. M1 and M2 can be re-polarized by TH2 or TH1 cytokines, respectively, and respond to exogenous danger signals. Immunobiology 211, 473-486 (2006)
107. Edwards, J. P., Zhang, X., Frauwirth, K. A. & Mosser, D. M. Biochemical and functional characterization of three activated macrophage populations. J. Leukoc. Biol. 80, 1298-1307 (2006) (Pubitemid 44904968)
108. Kigerl, K. A. et al. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 29, 13435-13444 (2009)
109. Ydens, E. et al. Acute injury in the peripheral nervous system triggers an alternative macrophage response. J. Neuroinflammation 9, 176 (2012)
110. Mokarram, N., Merchant, A., Mukhatyar, V., Patel, G. & Bellamkonda, R. V. Effect of modulating macrophage phenotype on peripheral nerve repair. Biomaterials 33, 8793-8801 (2012)
111. Rodrigues, M. C., Rodrigues, A. A. Jr, Glover, L. E., Voltarelli, J. & Borlongan, C. V. Peripheral nerve repair with cultured Schwann cells: Getting closer to the clinics. ScientificWorldJournal 2012, 413091 (2012)
112. Ren, Z., Wang, Y., Peng, J., Zhao, Q. & Lu, S. Role of stem cells in the regeneration and repair of peripheral nerves. Rev. Neurosci. 23, 135-143 (2012)
113. Bell, J. H. & Haycock, J. W. Next generation nerve guides: Materials, fabrication, growth factors, and cell delivery. Tissue Eng. Part B Rev. 18, 116-128 (2012)
114. Alsina, F. C., Ledda, F. & Paratcha, G. New insights into the control of neurotrophic growth factor receptor signaling: Implications for nervous system development and repair. J. Neurochem. 123, 652-661 (2012)
115. Madduri, S. & Gander, B. Growth factor delivery systems and repair strategies for damaged peripheral nerves. J. Control. Release 161, 274-282 (2012)
116. Cho, Y., Shi, R. & Borgens, R. B. Chitosan produces potent neuroprotection and physiological recovery following traumatic spinal cord injury. J. Exp. Biol. 213, 1513-1520 (2010)
117. Cho, Y. & Borgens, R. B. Polymer and nano-technology applications for repair and reconstruction of the central nervous system. Exp. Neurol. 233, 126-144 (2012)
118. Ebenezer, G. J. et al. Denervation of skin in neuropathies: The sequence of axonal and Schwann cell changes in skin biopsies. Brain 130, 2703-2714 (2007) (Pubitemid 47511712)