Neural regeneration: Lessons from regenerating and non-regenerating systems

Molecular Neurobiology

Volumn 46, Issue 2, 2012, Pages 227-241

  Ferreira, Leonardo M R ^a   Floriddia, Elisa M ^b   Quadrato, Giorgia ^b   Di Giovanni, Simone ^b  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Axonal regeneration; Biocurrents; Therapies

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN PROTEIN; NEU DIFFERENTIATION FACTOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; TRIPHOSPHOINOSITIDE;

ANIMAL MODEL; ARTICLE; BIOENERGY; CELL MIGRATION; CELL PROLIFERATION; CELL THERAPY; CENTRAL NERVOUS SYSTEM; GLIA CELL; HIPPOCAMPUS; HUMAN; MOLECULAR THERAPY; MOUSE; NERVE CELL PLASTICITY; NERVE FIBER REGENERATION; NERVE REGENERATION; NEURAL STEM CELL; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; SCHWANN CELL; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; SPINAL CORD REGENERATION; SUBVENTRICULAR ZONE;

EID: 84868112209     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-012-8290-9     Document Type: Article

References (152)

1. Brockes JP, Kumar A (2008) Comparative aspects of animal regeneration. Annu Rev Cell Dev Biol 24:525-549
2. Birnbaum KD, Sanchez Alvarado A (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132:697-710 (Pubitemid 351253692)
3. Ferretti P, Zhang F, O'Neill P (2003) Changes in spinal cord regenerative ability through phylogenesis and development: lessons to be learnt. Dev Dyn 226:245-256 (Pubitemid 36158169)
4. Endo T, Yoshino J, Kado K, Tochinai S (2007) Brain regeneration in anuran amphibians. Dev Growth Differ 49:121-129
5. Fields RD, Stevens-Graham B (2002) New insights into neuronglia communication. Science 298:556-562
6. Doetsch F (2003) The glial identity of neural stem cells. Nat Neurosci 6:1127-1134 (Pubitemid 37346029)
7. Keirstead HS, Hasan SJ, Muir GD, Steeves JD (1992) Suppression of the onset of myelination extends the permissive period for the functional repair of embryonic spinal cord. Proc Natl Acad Sci USA 89:11664-11668 (Pubitemid 23004703)
8. Yoshino J, Tochinai S (2004) Successful reconstitution of the non-regenerating adult telencephalon by cell transplantation in Xenopus laevis. Dev Growth Differ 46:523-534
9. Kumar A, Delgado JP, Gates PB, Neville G, Forge A, Brockes JP (2011) The aneurogenic limb identifies developmental cell interactions underlying vertebrate limb regeneration. Proc Natl Acad Sci U S A 108:13588-13593
10. Yoshino J, Tochinai S (2006) Functional regeneration of the olfactory bulb requires reconnection to the olfactory nerve in Xenopus larvae. Dev Growth Differ 48:15-24
11. Gong Q, Shipley MT (1995) Evidence that pioneer olfactory axons regulate telencephalon cell cycle kinetics to induce the formation of the olfactory bulb. Neuron 14:91-101
12. Iten LE, Bryant SV (1976) Stages of tail regeneration in the adult newt, Notophthalmus viridescens. J Exp Zool 196:283-292
13. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335
14. Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137:433-457
15. Gross CG (2009) Three before their time: neuroscientists whose ideas were ignored by their contemporaries. Exp Brain Res 192:321-334
16. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317 (Pubitemid 28512114)
17. Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch DH, Alvarez-Buylla A (2011) Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478:382-386
18. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716 (Pubitemid 29278045)
19. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25-34 (Pubitemid 29044150)
20. Decimo I, Bifari F, Francisco JR, Malpeli G, Dolci S, Lavarini V, Pretto S, Vasquez S, Sciancalepore M, Montalbano A, Berton V, Krampera M, Fumagalli G (2011) Nestin- and DCX-positive cells reside in adult spinal cord meninges and participate to injury-induced parenchymal reaction. Stem Cells 29:2062-76
21. Conti L, Cattaneo E (2010) Neural stem cell systems: physiological players or in vitro entities? Nat Rev Neurosci 11:176-187
22. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123-1133 (Pubitemid 26389268)
23. Mason I (2007) Initiation to end point: the multiple roles of fibroblast growth factors in neural development. Nat Rev Neurosci 8:583-596 (Pubitemid 47093932)
24. Hu X, Cai J, Yang J, Smith GM (2010) Sensory axon targeting is increased by NGF gene therapy within the lesioned adult femoral nerve. Exp Neurol 223:153-165
25. Richardson PM, Issa VM (1984) Peripheral injury enhances central regeneration of primary sensory neurones. Nature 309:791-793 (Pubitemid 14119428)
26. Neumann S, Woolf CJ (1999) Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23:83-91 (Pubitemid 29262466)
27. Neumann S, Skinner K, Basbaum AI (2005) Sustaining intrinsic growth capacity of adult neurons promotes spinal cord regeneration. Proc Natl Acad Sci U S A 102:16848-16852 (Pubitemid 41688865)
28. Ylera B, Erturk A, Hellal F, Nadrigny F, Hurtado A, Tahirovic S, Oudega M, Kirchhoff F, Bradke F (2009) Chronically CNS-injured adult sensory neurons gain regenerative competence upon a lesion of their peripheral axon. Curr Biol 19:930-936
29. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI (2002) Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34:885-893 (Pubitemid 34722279)
30. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT (2002) Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34:895-903 (Pubitemid 34722280)
31. Hannila SS, Filbin MT (2008) The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Exp Neurol 209:321-332 (Pubitemid 351174133)
32. Costigan M, Befort K, Karchewski L, Griffin RS, D'Urso D, Allchorne A, Sitarski J, Mannion JW, Pratt RE, Woolf CJ (2002) Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci 3:16
33. Goldberg JL (2003) How does an axon grow? Genes Dev 17:941-958 (Pubitemid 36459447)
34. Hanz S, Perlson E, Willis D, Zheng JQ, Massarwa R, Huerta JJ, Koltzenburg M, Kohler M, van Minnen J, Twiss JL, Fainzilber M (2003) Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40:1095-1104 (Pubitemid 38032787)
35. Perlson E, Hanz S, Medzihradszky KF, Burlingame AL, Fainzilber M (2004) From snails to sciatic nerve: retrograde injury signaling from axon to soma in lesioned neurons. J Neurobiol 58:287-294 (Pubitemid 38173725)
36. Perlson E, Hanz S, Ben-Yaakov K, Segal-Ruder Y, Seger R, Fainzilber M (2005) Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 45:715-726 (Pubitemid 40320706)
37. Di Giovanni S, Knights CD, Rao M, Yakovlev A, Beers J, Catania J, Avantaggiati ML, Faden AI (2006) The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration. EMBO J 25:4084-4096 (Pubitemid 44338749)
38. Floriddia E, Nguyen T, Di Giovanni S (2012) Chromatin immunoprecipitation from dorsal root ganglia tissue following axonal injury. J Vis Exp (in press)
39. Moore DL, Goldberg JL (2011) Multiple transcription factor families regulate axon growth and regeneration. Dev Neurobiol 71:1186-1211
40. Filbin MT (2006) Recapitulate development to promote axonal regeneration: good or bad approach? Philos Trans R Soc Lond B Biol Sci 361:1565-1574 (Pubitemid 44450211)
41. Richardson PM (1991) Neurotrophic factors in regeneration. Curr Opin Neurobiol 1:401-406
42. Gordon T (2009) The role of neurotrophic factors in nerve regeneration. Neurosurg Focus 26:E3
43. Hollis ER 2nd, Jamshidi P, Low K, Blesch A, Tuszynski MH (2009) Induction of corticospinal regeneration by lentiviral trkBinduced Erk activation. Proc Natl Acad Sci USA 106:7215-7220
44. Aguayo AJ, Epps J, Charron L, Bray GM (1976) Multipotentiality of Schwann cells in cross-anastomosed and grafted myelinated and unmyelinated nerves: quantitative microscopy and radioautography. Brain Res 104:1-20
45. Ide C, Tohyama K, Yokota R, Nitatori T, Onodera S (1983) Schwann cell basal lamina and nerve regeneration. Brain Res 288:61-75 (Pubitemid 14212694)
46. Ide C (1983) Nerve regeneration and Schwann cell basal lamina: observations of the long-term regeneration. Arch Histol Jpn 46:243-257 (Pubitemid 13056130)
47. Nave KA, Trapp BD (2008) Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci 31:535-561
48. Jessen KR, Mirsky R (2008) Negative regulation of myelination: relevance for development, injury, and demyelinating disease. Glia 56:1552-1565
49. Levy D, Hoke A, Zochodne DW (1999) Local expression of inducible nitric oxide synthase in an animal model of neuropathic pain. Neurosci Lett 260:207-209 (Pubitemid 29089197)
50. Levy D, Kubes P, Zochodne DW (2001) Delayed peripheral nerve degeneration, regeneration, and pain inmice lacking inducible nitric oxide synthase. J Neuropathol Exp Neurol 60:411-421 (Pubitemid 32467098)
51. Parkinson DB, Bhaskaran A, Arthur-Farraj P, Noon LA, Woodhoo A, Lloyd AC, Feltri ML, Wrabetz L, Behrens A, Mirsky R, Jessen KR (2008) c-Jun is a negative regulator of myelination. J Cell Biol 181:625-637 (Pubitemid 351717510)
52. Schotte OE, Butler EG (1941) Morphological effects of denervation and amputation of limbs in urodele larvae. J Exp Zool 87:279-322
53. Satoh A, Gardiner DM, Bryant SV, Endo T (2007) Nerve-induced ectopic limb blastemas in the axolotl are equivalent to amputation-induced blastemas. Dev Biol 312:231-244 (Pubitemid 350186157)
54. Satoh A, Bryant SV, Gardiner DM (2008) Regulation of dermal fibroblast dedifferentiation and redifferentiation during wound healing and limb regeneration in the axolotl. Dev Growth Differ 50:743-754
55. Stocum DL (1984) The urodele limb regeneration blastema. Determination and organization of the morphogenetic field. Differentiation 27:13-28 (Pubitemid 14058813)
56. da Silva SM, Gates PB, Brockes JP (2002) The newt ortholog of CD59 is implicated in proximodistal identity during amphibian limb regeneration. Dev Cell 3:547-555 (Pubitemid 35252263)
57. Kumar A, Godwin JW, Gates PB, Garza-Garcia AA, Brockes JP (2007) Molecular basis for the nerve dependence of limb regeneration in an adult vertebrate. Science 318:772-777 (Pubitemid 351411765)
58. Blassberg RA, Garza-Garcia A, Janmohamed A, Gates PB, Brockes JP (2011) Functional convergence of signalling by GPI-anchored and anchorless forms of a salamander protein implicated in limb regeneration. J Cell Sci 124:47-56
59. Garza-Garcia AA, Driscoll PC, Brockes JP (2010) Evidence for the local evolution of mechanisms underlying limb regeneration in salamanders. Integr Comp Biol 50:528-535
60. Yntema CL (1959) Regeneration in sparsely innervated and aneurogenic forelimbs of Amblystoma larvae. J Exp Zool 140:101-123
61. Becker RO (1960) The bioelectric field pattern in the salamander and its simulation by an electronic analog. IRE Trans Med Electron ME-7:202-207
62. Levin M (2007) Large-scale biophysics: ion flows and regeneration. Trends Cell Biol 17:261-270 (Pubitemid 46829851)
63. Messerli MA, Graham DM (2011) Extracellular electrical fields direct wound healing and regeneration. Biol Bull 221:79-92
64. Zhao M, Song B, Pu J, Wada T, Reid B, Tai G, Wang F, Guo A, Walczysko P, Gu Y, Sasaki T, Suzuki A, Forrester JV, Bourne HR, Devreotes PN, McCaig CD, Penninger JM (2006) Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature 442:457-460 (Pubitemid 44264795)
65. Britland S, McCaig C (1996) Embryonic Xenopus neurites integrate and respond to simultaneous electrical and adhesive guidance cues. Exp Cell Res 226:31-38 (Pubitemid 26238924)
66. Yao L, Shanley L, McCaig C, Zhao M (2008) Small applied electric fields guide migration of hippocampal neurons. J Cell Physiol 216:527-535 (Pubitemid 351898481)
67. Becker RO (1961) The bioelectric factors in amphibian-limb regeneration. J Bone Joint Surg Am 43-A:643-656
68. Borgens RB (1984) Are limb development and limb regeneration both initiated by an integumentary wounding? A hypothesis. Differentiation 28:87-93 (Pubitemid 15167871)
69. Becker RO (1972) Stimulation of partial limb regeneration in rats. Nature 235:109-111
70. Becker RO, Spadaro JA (1972) Electrical stimulation of partial limb regeneration in mammals. Bull N Y Acad Med 48:627-641
71. Feng Z, Levine AJ (2010) The regulation of energy metabolism and the IGF-1/mTOR pathways by the p53 protein. Trends Cell Biol 20:427-434
72. Stambolic V, Suzuki A, de la Pompa JL, Brothers GM, Mirtsos C, Sasaki T, Ruland J, Penninger JM, Siderovski DP, Mak TW (1998) Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 95:29-39 (Pubitemid 28458022)
73. Park KK, Liu K, Hu Y, Smith PD, Wang C, Cai B, Xu B, Connolly L, Kramvis I, Sahin M, He Z (2008) Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 322:963-966
74. Liu K, Lu Y, Lee JK, Samara R, Willenberg R, Sears-Kraxberger I, Tedeschi A, Park KK, Jin D, Cai B, Xu B, Connolly L, Steward O, Zheng B, He Z (2010) PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat Neurosci 13:1075-1081
75. Ma XM, Blenis J (2009) Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10:307-318
76. Sun F, Park KK, Belin S, Wang D, Lu T, Chen G, Zhang K, Yeung C, Feng G, Yankner BA, He Z (2011) Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 480:372-375
77. Gu J, Tamura M, Pankov R, Danen EH, Takino T, Matsumoto K, Yamada KM (1999) Shc and FAK differentially regulate cell motility and directionality modulated by PTEN. J Cell Biol 146:389-403 (Pubitemid 29369775)
78. Denker SP, Barber DL (2002) Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J Cell Biol 159:1087-1096 (Pubitemid 36055762)
79. Lee JO, Yang H, Georgescu MM, Di Cristofano A, Maehama T, Shi Y, Dixon JE, Pandolfi P, Pavletich NP (1999) Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 99:323-334 (Pubitemid 29519911)
80. Murata Y, Iwasaki H, Sasaki M, Inaba K, Okamura Y (2005) Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435:1239-1243 (Pubitemid 40943089)
81. Kohout SC, Bell SC, Liu L, Xu Q, Minor DL Jr, Isacoff EY (2010) Electrochemical coupling in the voltage-dependent phosphatase Ci-VSP. Nat Chem Biol 6:369-375
82. Ratzan WJ, Evsikov AV, Okamura Y, Jaffe LA (2011) Voltage sensitive phosphoinositide phosphatases of Xenopus: their tissue distribution and voltage dependence. J Cell Physiol 226:2740-2746
83. Wu Y, Dowbenko D, Pisabarro MT, Dillard-Telm L, Koeppen H, Lasky LA (2001) PTEN 2, a Golgi-associated testis-specific homologue of the PTEN tumor suppressor lipid phosphatase. J Biol Chem 276:21745-21753
84. Walker SM, Downes CP, Leslie NR (2001) TPIP: a novel phosphoinositide 3-phosphatase. Biochem J 360:277-283 (Pubitemid 33151322)
85. Aguayo AJ, Dickson R, Trecarten J, Attiwell M, Bray GM, Richardson P (1978) Ensheathment and myelination of regenerating PNS fibres by transplanted optic nerve glia. Neurosci Lett 9:97-104 (Pubitemid 9028286)
86. David S, Aguayo AJ (1981) Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214:931-933 (Pubitemid 12220099)
87. David S, Aguayo AJ (1985) Axonal regeneration after crush injury of rat central nervous system fibres innervating peripheral nerve grafts. J Neurocytol 14:1-12 (Pubitemid 15075833)
88. Savio T, Schwab ME (1990) Lesioned corticospinal tract axons regenerate in myelin-free rat spinal cord. Proc Natl Acad Sci U S A 87:4130-4133
89. Caroni P, Schwab ME (1988) Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J Cell Biol 106:1281-1288
90. Schnell L, Schwab ME (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343:269-272 (Pubitemid 20030644)
91. Chen MS, Huber AB, van der Haar ME, Frank M, Schnell L, Spillmann AA, Christ F, Schwab ME (2000) Nogo-A is a myelinassociated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403:434-439 (Pubitemid 30073093)
92. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, Braun PE (1994) Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13:805-811
93. Mukhopadhyay G, Doherty P, Walsh FS, Crocker PR, Filbin MT (1994) A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13:757-767 (Pubitemid 24300179)
94. Bartsch U (1996) Myelination and axonal regeneration in the central nervous system of mice deficient in the myelin-associated glycoprotein. J Neurocytol 25:303-313 (Pubitemid 26225017)
95. Yin X, Crawford TO, Griffin JW, Tu P, Lee VM, Li C, Roder J, Trapp BD (1998) Myelin-associated glycoprotein is a myelin signal that modulates the caliber of myelinated axons. J Neurosci 18:1953-1962 (Pubitemid 28141401)
96. Nguyen T, Mehta NR, Conant K, Kim KJ, Jones M, Calabresi PA, Melli G, Hoke A, Schnaar RL, Ming GL, Song H, Keswani SC, Griffin JW (2009) Axonal protective effects of the myelin-associated glycoprotein. J Neurosci 29:630-637
97. Fournier AE, GrandPre T, Strittmatter SM (2001) Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409:341-346 (Pubitemid 32151238)
98. Wang KC, Kim JA, Sivasankaran R, Segal R, He Z (2002) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420:74-78 (Pubitemid 35291442)
99. Yamashita T, Tohyama M (2003) The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat Neurosci 6:461-467 (Pubitemid 36514693)
100. Mi S, Lee X, Shao Z, Thill G, Ji B, Relton J, Levesque M, Allaire N, Perrin S, Sands B, Crowell T, Cate RL, McCoy JM, Pepinsky RB (2004) LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat Neurosci 7:221-228 (Pubitemid 38280445)
101. Park JB, Yiu G, Kaneko S, Wang J, Chang J, He XL, Garcia KC, He Z (2005) A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 45:345-351 (Pubitemid 40188202)
102. Bartsch U, Bandtlow CE, Schnell L, Bartsch S, Spillmann AA, Rubin BP, Hillenbrand R, Montag D, Schwab ME, Schachner M (1995) Lack of evidence that myelin-associated glycoprotein is a major inhibitor of axonal regeneration in the CNS. Neuron 15:1375-1381 (Pubitemid 26005374)
103. Bregman BS, Kunkel-Bagden E, Schnell L, Dai HN, Gao D, Schwab ME (1995) Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378:498-501
104. Kottis V, Thibault P, Mikol D, Xiao ZC, Zhang R, Dergham P, Braun PE (2002) Oligodendrocyte-myelin glycoprotein (OMgp) is an inhibitor of neurite outgrowth. J Neurochem 82:1566-1569
105. Ji B, Case LC, Liu K, Shao Z, Lee X, Yang Z, Wang J, Tian T, Shulga-Morskaya S, Scott M, He Z, Relton JK, Mi S (2008) Assessment of functional recovery and axonal sprouting in oligodendrocyte-myelin glycoprotein (OMgp) null mice after spinal cord injury. Mol Cell Neurosci 39:258-267
106. Cafferty WB, Duffy P, Huebner E, Strittmatter SM (2010) MAG and OMgp synergize with Nogo-A to restrict axonal growth and neurological recovery after spinal cord trauma. J Neurosci 30:6825-6837
107. Lee JK, Geoffroy CG, Chan AF, Tolentino KE, Crawford MJ, Leal MA, Kang B, Zheng B (2010) Assessing spinal axon regeneration and sprouting in Nogo-, MAG-, and OMgp-deficient mice. Neuron 66:663-670
108. Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5:146-156 (Pubitemid 38160289)
109. Yiu G, He Z (2006) Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 7:617-627 (Pubitemid 44106744)
110. Goritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Frisen J (2011) A pericyte origin of spinal cord scar tissue. Science 333:238-242
111. Frisen J, Haegerstrand A, Risling M, Fried K, Johansson CB, Hammarberg H, Elde R, Hokfelt T, Cullheim S (1995) Spinal axons in central nervous system scar tissue are closely related to laminin-immunoreactive astrocytes. Neuroscience 65:293-304
112. McKeon RJ, Hoke A, Silver J (1995) Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp Neurol 136:32-43
113. Jones LL, Sajed D, Tuszynski MH (2003) Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permissiveness and inhibition. J Neurosci 23:9276-9288 (Pubitemid 37323026)
114. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV (2004) Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 24:2143-2155 (Pubitemid 38314546)
115. Rolls A, Shechter R, Schwartz M (2009) The bright side of the glial scar in CNS repair. Nat Rev Neurosci 10:235-241
116. McKeon RJ, Schreiber RC, Rudge JS, Silver J (1991) Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 11:3398-3411
117. Davies SJ, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J (1997) Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390:680-683 (Pubitemid 28016354)
118. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640 (Pubitemid 34406764)
119. Davies SJ, Goucher DR, Doller C, Silver J (1999) Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19:5810-5822 (Pubitemid 29327918)
120. McKeon RJ, Jurynec MJ, Buck CR (1999) The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J Neurosci 19:10778-10788 (Pubitemid 30235724)
121. Jones LL, Yamaguchi Y, Stallcup WB, Tuszynski MH (2002) NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J Neurosci 22:2792-2803 (Pubitemid 37465828)
122. Jones LL, Margolis RU, Tuszynski MH (2003) The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp Neurol 182:399-411 (Pubitemid 36937092)
123. Shen Y, Tenney AP, Busch SA, Horn KP, Cuascut FX, Liu K, He Z, Silver J, Flanagan JG (2009) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326:592-596
124. Fisher D, Xing B, Dill J, Li H, Hoang HH, Zhao Z, Yang XL, Bachoo R, Cannon S, Longo FM, Sheng M, Silver J, Li S (2011) Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J Neurosci 31:14051-14066
125. Cummings BJ, Uchida N, Tamaki SJ, Salazar DL, Hooshmand M, Summers R, Gage FH, Anderson AJ (2005) Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci U S A 102:14069-14074 (Pubitemid 41377704)
126. Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH,Weissman IL (2000) Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci U S A 97:14720-14725 (Pubitemid 32016642)
127. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, Steward O (2005) Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 25:4694-4705 (Pubitemid 40664118)
128. Nordqvist C (2011) Spinal cord injury stem cell trial gets $25 million award from CIRM. Med News Today.
129. Nordqvist C (2011) Geron abandons stem cell programs. Med News Today.
130. Whishaw IQ, Pellis SM, Gorny B, Kolb B, Tetzlaff W (1993) Proximal and distal impairments in rat forelimb use in reaching follow unilateral pyramidal tract lesions. Behav Brain Res 56:59-76 (Pubitemid 23272744)
131. Metz GA, Dietz V, Schwab ME, van de Meent H (1998) The effects of unilateral pyramidal tract section on hindlimb motor performance in the rat. Behav Brain Res 96:37-46 (Pubitemid 28494122)
132. Barthelemy D, Grey MJ, Nielsen JB, Bouyer L (2011) Involvement of the corticospinal tract in the control of human gait. Prog Brain Res 192:181-197
133. Schnell L, Schneider R, Kolbeck R, Barde YA, Schwab ME (1994) Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367:170-173 (Pubitemid 24031697)
134. Grill R, Murai K, Blesch A, Gage FH, Tuszynski MH (1997) Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J Neurosci 17:5560-5572
135. Kobayashi NR, Fan DP, Giehl KM, Bedard AM, Wiegand SJ, Tetzlaff W (1997) BDNF and NT-4/5 prevent atrophy of rat rubrospinal neurons after cervical axotomy, stimulate GAP-43 and Talpha1-tubulin mRNA expression, and promote axonal regeneration. J Neurosci 17:9583-9595 (Pubitemid 28006402)
136. Liu Y, Kim D, Himes BT, Chow SY, Schallert T, Murray M, Tessler A, Fischer I (1999) Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function. J Neurosci 19:4370-4387 (Pubitemid 29241090)
137. GrandPre T, Li S, Strittmatter SM (2002) Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 417:547-551 (Pubitemid 34595921)
138. Freund P, Schmidlin E, Wannier T, Bloch J, Mir A, Schwab ME, Rouiller EM (2006) Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nat Med 12:790-792 (Pubitemid 44050068)
139. Freund P, Wannier T, Schmidlin E, Bloch J, Mir A, Schwab ME, Rouiller EM (2007) Anti-Nogo-A antibody treatment enhances sprouting of corticospinal axons rostral to a unilateral cervical spinal cord lesion in adult macaque monkey. J Comp Neurol 502:644-659 (Pubitemid 46732514)
140. Freund P, Schmidlin E, Wannier T, Bloch J, Mir A, Schwab ME, Rouiller EM (2009) Anti-Nogo-A antibody treatment promotes recovery of manual dexterity after unilateral cervical lesion in adult primates-re-examination and extension of behavioral data. Eur J Neurosci 29:983-996
141. Zorner B, Schwab ME (2010) Anti-Nogo on the go: from animal models to a clinical trial. Ann N YAcad Sci 1198(Suppl 1):E22-E34
142. Usher LC, Johnstone A, Erturk A, Hu Y, Strikis D, Wanner IB, Moorman S, Lee JW,Min J, Ha HH, Duan Y, Hoffman S, Goldberg JL, Bradke F, Chang YT, Lemmon VP, Bixby JL (2010) A chemical screen identifies novel compounds that overcome glial-mediated inhibition of neuronal regeneration. J Neurosci 30:4693-4706
143. Kadoya K, Tsukada S, Lu P, Coppola G, Geschwind D, Filbin MT, Blesch A, Tuszynski MH (2009) Combined intrinsic and extrinsic neuronal mechanisms facilitate bridging axonal regeneration 1 year after spinal cord injury. Neuron 64:165-172
144. Lu P, Yang H, Jones LL, Filbin MT, Tuszynski MH (2004) Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J Neurosci 24:6402-6409 (Pubitemid 38944231)
145. Garcia-Alias G, Barkhuysen S, Buckle M, Fawcett JW (2009) Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat Neurosci 12:1145-1151
146. Wang D, Ichiyama RM, Zhao R, Andrews MR, Fawcett JW (2011) Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J Neurosci 31:9332-9344
147. Houle JD, Tom VJ, Mayes D, Wagoner G, Phillips N, Silver J (2006) Combining an autologous peripheral nervous system "bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J Neurosci 26:7405-7415 (Pubitemid 44315209)
148. Alilain WJ, Horn KP, Hu H, Dick TE, Silver J (2011) Functional regeneration of respiratory pathways after spinal cord injury. Nature 475:196-200
149. Garcia-Alias G, Petrosyan HA, Schnell L, Horner PJ, Bowers WJ, Mendell LM, Fawcett JW, Arvanian VL (2011) Chondroitinase ABC combined with neurotrophin NT-3 secretion and NR2D expression promotes axonal plasticity and functional recovery in rats with lateral hemisection of the spinal cord. J Neurosci 31:17788-17799
150. Cone CD Jr, Cone CM (1976) Induction of mitosis in mature neurons in central nervous system by sustained depolarization. Science 192:155-158
151. Shapiro S, Borgens R, Pascuzzi R, Roos K, Groff M, Purvines S, Rodgers RB, Hagy S, Nelson P (2005) Oscillating field stimulation for complete spinal cord injury in humans: a phase 1 trial. J Neurosurg Spine 2:3-10
152. Czupryn A, Zhou YD, Chen X, McNay D, Anderson MP, Flier JS, Macklis JD (2011) Transplanted hypothalamic neurons restore leptin signaling and ameliorate obesity in db/db mice. Science 334:1133-1137