Extrinsic and intrinsic factors controlling axonal regeneration after spinal cord injury

Expert Reviews in Molecular Medicine

Volumn 11, Issue , 2009, Pages

  Afshari, Fardad T ^a   Kappagantula, Sunil ^a   Fawcett, James W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTRINSIC FACTOR; NERVE PROTEIN;

ANIMAL; ARTICLE; CELL MOTION; CENTRAL NERVOUS SYSTEM; CONVALESCENCE; FEMALE; FIBROSIS; HUMAN; MALE; MYELIN SHEATH; NERVE CELL; NERVE FIBER; NERVE REGENERATION; PATHOLOGY; PHYSIOLOGY; REGENERATION; SPINAL CORD; SPINAL CORD INJURY; STEM CELL TRANSPLANTATION;

ANIMALS; AXONS; CELL MOVEMENT; CENTRAL NERVOUS SYSTEM; FEMALE; FIBROSIS; HUMANS; INTRINSIC FACTOR; MALE; MYELIN SHEATH; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEURONS; RECOVERY OF FUNCTION; REGENERATION; SPINAL CORD; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION;

EID: 77951642506     PISSN: 14623994     EISSN: None     Source Type: Journal    
DOI: 10.1017/S1462399409001288     Document Type: Review

References (173)

1. Oudega, M. (2007) Schwann cell and olfactory ensheathing cell implantation for repair of the contused spinal cord. Acta Physiologica 189, 181-189
2. Kwon, B.K., Borisoff, J.F. and Tetzlaff, W. (2002) Molecular targets for therapeutic intervention after spinal cord injury. Molecular Interventions 2, 244-258
3. Silver, J. and Miller, J.H. (2004) Regeneration beyond the glial scar. Nature Reviews Neuroscience 5, 146-156 (Pubitemid 38160289)
4. Fawcett, J.W. and Asher, R.A. (1999) The glial scar and central nervous system repair. Brain Research Bulletin 49, 377-391 (Pubitemid 29385505)
5. Okada, S. et al. (2004) Blockade of interleukin-6 receptor suppresses reactive astrogliosis and ameliorates functional recovery in experimental spinal cord injury. Journal of Neuroscience Research 76, 265-276 (Pubitemid 38451214)
6. Nakamura, M. et al. (2005) Role of IL-6 in spinal cord injury in a mouse model. Clinical Reviews in Allergy and Immunology 28, 197-204
7. Faulkner, J.R. et al. (2004) Reactive astrocytes protect tissue and preserve function after spinal cord injury. Journal of Neuroscience 24, 2143-2155 (Pubitemid 38314546)
8. Bundesen, L.Q. et al. (2003) Ephrin-B2 and EphB2 regulation of astrocyte-meningeal fibroblast interactions in response to spinal cord lesions in adult rats. Journal of Neuroscience 23, 7789-7800 (Pubitemid 37052347)
9. Abnet, K., Fawcett, J.W. and Dunnett, S.B. (1991) Interactions between meningeal cells and astrocytes in vivo and in vitro. Brain Research Developmental Brain Research 59, 187-196
10. Windle, W.F., Clemente, C.D. and Chambers, W.W. (1952) Inhibition of formation of a glial barrier as a means of permitting a peripheral nerve to grow into the brain. Journal of Comparative Neurology 96, 359-369
11. Kwok, J.C. et al. (2008) Proteoglycans in the central nervous system: Plasticity, regeneration and their stimulation with chondroitinase ABC. Restorative Neurology and Neuroscience 26, 131-145
12. Niclou, S.P., Ehlert, E.M. and Verhaagen, J. (2006) Chemorepellent axon guidance molecules in spinal cord injury. Journal of Neurotrauma 23, 409-421 (Pubitemid 43726318)
13. Asher, R.A. et al. (2000) Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. Journal of Neuroscience 20, 2427-2438 (Pubitemid 30220330)
14. Yong, V.W. et al. (1991) Gamma-interferon promotes proliferation of adult human astrocytes in vitro and reactive gliosis in the adult mouse brain in vivo. Proceedings of the National Academy of Sciences of the United States of America 88, 7016-7020 (Pubitemid 21915080)
15. Giulian, D. et al. (1988) Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization. Journal of Neuroscience 8, 2485-2490
16. Grados-Munro, E.M. and Fournier, A.E. (2003) Myelin-associated inhibitors of axon regeneration. Journal of Neuroscience Research 74, 479-485 (Pubitemid 37352069)
17. McGee, A.W. and Strittmatter, S.M. (2003) The Nogo-66 receptor: focusing myelin inhibition of axon regeneration. Trends in Neurosciences 26, 193-198 (Pubitemid 36412001)
18. Caroni, P. and Schwab, M.E. (1988) Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. Journal of Cell Biology 106, 1281-1288
19. Caroni, P. and Schwab, M.E. (1988) Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1, 85-96
20. Schnell, L. and Schwab, M.E. (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343, 269-272 (Pubitemid 20030644)
21. Fouad, K., Klusman, I. and Schwab, M.E. (2004) Regenerating corticospinal fibers in the Marmoset (Callitrix jacchus) after spinal cord lesion and treatment with the anti-Nogo-A antibody IN-1. European Journal of Neuroscience 20, 2479-2482 (Pubitemid 39472410)
22. Freund, P. et al. (2006) Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nature Medicine 12, 790-792 (Pubitemid 44050068)
23. Blight, A.R. and Tuszynski, M.H. (2006) Clinical trials in spinal cord injury. Journal of Neurotrauma 23, 586-593 (Pubitemid 43726331)
24. Chen, M.S. et al. (2000) Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403, 434-439 (Pubitemid 30073093)
25. Hu, F. and Strittmatter, S.M. (2008) The N-terminal domain of Nogo-A inhibits cell adhesion and axonal outgrowth by an integrin-specific mechanism. Journal of Neuroscience 28, 1262-1269 (Pubitemid 351186346)
26. Fournier, A.E., GrandPre, T. and Strittmatter, S.M. (2001) Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409, 341-346 (Pubitemid 32151238)
27. Wang, K.C. et al. (2002) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420, 74-78 (Pubitemid 35291442)
28. Mosyak, L. et al. (2006) The structure of the Lingo-1 ectodomain, a module implicated in central nervous system repair inhibition. Journal of Biological Chemistry 281, 36378-36390 (Pubitemid 46041372)
29. GrandPre, T., Li, S. and Strittmatter, S.M. (2002) Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 417, 547-551 (Pubitemid 34595921)
30. Zheng, B. et al. (2003) Lack of enhanced spinal regeneration in Nogo-deficient mice. Neuron 38, 213-224 (Pubitemid 36555648)
31. Simonen, M. et al. (2003) Systemic deletion of the myelin-associated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 38, 201-211 (Pubitemid 36555647)
32. Kim, J.E. et al. (2003) Axon regeneration in young adult mice lacking Nogo-A/B. Neuron 38, 187-199
33. Lee, J.K. et al. (2009) Reassessment of corticospinal tract regeneration in Nogo-deficient mice. Journal of Neuroscience 29, 8649-8654
34. Martini, R. (1994) Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. Journal of Neurocytology 23, 1-28
35. Mukhopadhyay, G. et al. (1994) A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13, 757-767 (Pubitemid 24300179)
36. McKerracher, L. et al. (1994) Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13, 805-811
37. Schnaar, R.L. and Lopez, P.H. (2009) Myelin-associated glycoprotein and its axonal receptors. Journal of Neuroscience Research 87, 3267-3276
38. Mehta, N.R. et al. (2007) Gangliosides and Nogo receptors independently mediate myelinassociated glycoprotein inhibition of neurite outgrowth in different nerve cells. Journal of Biological Chemistry 282, 27875-27886 (Pubitemid 47529534)
39. Domeniconi, M. et al. (2002) Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 35, 283-290 (Pubitemid 34876731)
40. Mikol, D.D. and Stefansson, K. (1988) A phosphatidylinositol-linked peanut agglutinin-binding glycoprotein in central nervous system myelin and on oligodendrocytes. Journal of Cell Biology 106, 1273-1279
41. Kottis, V. et al. (2002) Oligodendrocyte-myelin glycoprotein (OMgp) is an inhibitor of neurite outgrowth. Journal of Neurochemistry 82, 1566-1569
42. Wang, K.C. et al. (2002) Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417, 941-944 (Pubitemid 34716869)
43. Niederost, B. et al. (2002) Nogo-A and myelin-associated glycoprotein mediate neurite growth inhibition by antagonistic regulation of RhoA and Rac1. Journal of Neuroscience 22, 10368-10376 (Pubitemid 35416874)
44. Yamashita, T. et al. (2005) Multiple signals regulate axon regeneration through the Nogo receptor complex. Molecular Neurobiology 32, 105-111 (Pubitemid 41397179)
45. Gallo, V., Bertolotto, A. and Levi, G. (1987) The proteoglycan chondroitin sulfate is present in a subpopulation of cultured astrocytes and in their precursors. Developmental Biology 123, 282-285
46. Johnson-Green, P.C., Dow, K.E. and Riopelle, R.J. (1991) Characterization of glycosaminoglycans produced by primary astrocytes in vitro. Glia 4, 314-321
47. Crespo, D. et al. (2007) How does chondroitinase promote functional recovery in the damaged CNS? Experimental Neurology 206, 159-171 (Pubitemid 47094767)
48. Dou, C.L. and Levine, J.M. (1994) Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. Journal of Neuroscience 14, 7616-7628
49. McKeon, R.J., Hoke, A. and Silver, J. (1995) Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Experimental Neurology 136, 32-43
50. Moon, L.D. et al. (2001) Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nature Neuroscience 4, 465-466 (Pubitemid 32397182)
51. Caggiano, A.O. et al. (2005) Chondroitinase ABCI improves locomotion and bladder function following contusion injury of the rat spinal cord. Journal of Neurotrauma 22, 226-239 (Pubitemid 40333517)
52. Bradbury, E.J. et al. (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640 (Pubitemid 34406764)
53. Cafferty, W.B. et al. (2007) Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. Journal of Neuroscience 27, 2176-2185 (Pubitemid 46340954)
54. Yada, T. et al. (2003) Chondroitin sulfate synthase-2. Molecular cloning and characterization of a novel human glycosyltransferase homologous to chondroitin sulfate glucuronyltransferase, which has dual enzymatic activities. Journal of Biological Chemistry 278, 30235-30247 (Pubitemid 36962418)
55. Kitagawa, H. et al. (1997) Regulation of chondroitin sulfate biosynthesis by specific sulfation: acceptor specificity of serum beta-GalNAc transferase revealed by structurally defined oligosaccharides. Glycobiology 7, 531-537 (Pubitemid 27246727)
56. Laabs, T.L. et al. (2007) Inhibiting glycosaminoglycan chain polymerization decreases the inhibitory activity of astrocyte-derived chondroitin sulfate proteoglycans. Journal of Neuroscience 27, 14494-14501
57. Zhou, F.Q. et al. (2006) Neurotrophins support regenerative axon assembly over CSPGs by an ECM-integrin-independent mechanism. Journal of Cell Science 119, 2787-2796
58. Smith-Thomas, L.C. et al. (1994) An inhibitor of neurite outgrowth produced by astrocytes. Journal of Cell Science 107, 1687-1695 (Pubitemid 24198487)
59. Yamaguchi, Y., Mann, D.M. and Ruoslahti, E. (1990) Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature 346, 281-284
60. Davies, J.E. et al. (2004) Decorin suppresses neurocan, brevican, phosphacan and NG2 expression and promotes axon growth across adult rat spinal cord injuries. European Journal of Neuroscience 19, 1226-1242 (Pubitemid 38387200)
61. Santra, M., Reed, C.C. and Iozzo, R.V. (2002) Decorin binds to a narrow region of the epidermal growth factor (EGF) receptor, partially overlapping but distinct from the EGF-binding epitope. Journal of Biological Chemistry 277, 35671-35681
62. Minor, K. et al. (2008) Decorin promotes robust axon growth on inhibitory CSPGs and myelin via a direct effect on neurons. Neurobiology of Disease 32, 88-95
63. Zou, Y. et al. (2000) Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 102, 363-375
64. Raper, J.A. (2000) Semaphorins and their receptors in vertebrates and invertebrates. Current Opinion in Neurobiology 10, 88-94
65. Pasterkamp, R.J., Anderson, P.N. and Verhaagen, J. (2001) Peripheral nerve injury fails to induce growth of lesioned ascending dorsal column axons into spinal cord scar tissue expressing the axon repellent Semaphorin3A. European Journal of Neuroscience 13, 457-471 (Pubitemid 32158777)
66. Pasterkamp, R.J., Giger, R.J. and Verhaagen, J. (1998) Regulation of semaphorin III/collapsin-1 gene expression during peripheral nerve regeneration. Experimental Neurology 153, 313-327 (Pubitemid 28489897)
67. Kikuchi, K. et al. (2003) In vitro and in vivo characterization of a novel semaphorin 3A inhibitor, SM-216289 or xanthofulvin. Journal of Biological Chemistry 278, 42985-42991 (Pubitemid 37345911)
68. Kaneko, S. et al. (2006) A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nature Medicine 12, 1380-1389 (Pubitemid 44924496)
69. Klein, R. (2004) Eph/ephrin signaling in morphogenesis, neural development and plasticity. Current Opinion in Cell Biology 16, 580-589
70. Goldshmit, Y., McLenachan, S. and Turnley, A. (2006) Roles of Eph receptors and ephrins in the normal and damaged adult CNS. Brain Research Reviews 52, 327-345 (Pubitemid 44291808)
71. Gale, N.W. et al. (1996) Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17, 9-19 (Pubitemid 26251587)
72. Torres, R. et al. (1998) PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron 21, 1453-1463 (Pubitemid 29022546)
73. Kullander, K. and Klein, R. (2002) Mechanisms and functions of Eph and ephrin signalling. Nature Reviews Molecular Cell Biology 3, 475-486 (Pubitemid 34733429)
74. Gao, P.P. et al. (1998) Regulation of thalamic neurite outgrowth by the Eph ligand ephrin-A5: implications in the development of thalamocortical projections. Proceedings of the National Academy of Sciences of the United States of America 95, 5329-5334
75. Kullander, K. et al. (2001) Ephrin-B3 is the midline barrier that prevents corticospinal tract axons from recrossing, allowing for unilateral motor control. Genes and Development 15, 877-888 (Pubitemid 32295068)
76. Benson, M.D. et al. (2005) Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proceedings of the National Academy of Sciences of the United States of America 102, 10694-10699 (Pubitemid 41061616)
77. Willson, C.A. et al. (2002) Upregulation of EphA receptor expression in the injured adult rat spinal cord. Cell Transplantation 11, 229-239 (Pubitemid 34665823)
78. Miranda, J.D. et al. (1999) Induction of Eph B3 after spinal cord injury. Experimental Neurology 156, 218-222 (Pubitemid 29153000)
79. Fabes, J. et al. (2006) Accumulation of the inhibitory receptor EphA4 may prevent regeneration of corticospinal tract axons following lesion. European Journal of Neuroscience 23, 1721-1730
80. Kliffen, M. et al. (1997) Increased expression of angiogenic growth factors in age-related maculopathy. British Journal of Ophthalmology 81, 154-162 (Pubitemid 27092496)
81. Goldshmit, Y. et al. (2004) Axonal regeneration and lack of astrocytic gliosis in EphA4-deficient mice. Journal of Neuroscience 24, 10064-10073 (Pubitemid 39492030)
82. Fabes, J. et al. (2007) Regeneration-enhancing effects of EphA4 blocking peptide following corticospinal tract injury in adult rat spinal cord. European Journal of Neuroscience 26, 2496-2505 (Pubitemid 350064163)
83. Lawrenson, I.D. et al. (2002) Ephrin-A5 induces rounding, blebbing and de-adhesion of EphA3-expressing 293T and melanoma cells by CrkII and Rho-mediated signalling. Journal of Cell Science 115, 1059-1072 (Pubitemid 34257389)
84. Miao, H. et al. (2000) Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion-kinase dephosphorylation. Nature Cell Biology 2, 62-69
85. Yamaguchi, Y. et al. (2001) RhoA inhibits the nerve growth factor-induced Rac1 activation through Rho-associated kinase-dependent pathway. Journal of Biological Chemistry 276, 18977-18983
86. Rutishauser, U. (2008) Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nature Reviews Neuroscience 9, 26-35
87. Finne, J. et al. (1983) Occurrence of alpha 2-8 linked polysialosyl units in a neural cell adhesion molecule. Biochemical and Biophysical Research Communications 112, 482-487
88. Kiss, J.Z. et al. (2001) The role of neural cell adhesion molecules in plasticity and repair. Brain Research Reviews 36, 175-184 (Pubitemid 33020747)
89. Becker, C.G. et al. (1996) The polysialic acid modification of the neural cell adhesion molecule is involved in spatial learning and hippocampal long-term potentiation. Journal of Neuroscience Research 45, 143-152 (Pubitemid 26257315)
90. Hoyk, Z., Parducz, A. and Theodosis, D.T. (2001) The highly sialylated isoform of the neural cell adhesion molecule is required for estradiol-induced morphological synaptic plasticity in the adult arcuate nucleus. European Journal of Neuroscience 13, 649-656 (Pubitemid 32174790)
91. Hu, H. et al. (1996) The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron 16, 735-743 (Pubitemid 26124051)
92. Dusart, I. et al. (1999) Late axonal sprouting of injured Purkinje cells and its temporal correlation with permissive changes in the glial scar. Journal of Comparative Neurology 408, 399-418 (Pubitemid 29211191)
93. El Maarouf, A., Petridis, A.K. and Rutishauser, U. (2006) Use of polysialic acid in repair of the central nervous system. Proceedings of the National Academy of Sciences of the United States of America 103, 16989-16994 (Pubitemid 44737365)
94. Zhang, Y. et al. (2007) Induced expression of polysialic acid in the spinal cord promotes regeneration of sensory axons. Molecular and Cellular Neurosciences 35, 109-119 (Pubitemid 46636307)
95. Zhang, Y. et al. (2007) Lentiviral-mediated expression of polysialic acid in spinal cord and conditioning lesion promote regeneration of sensory axons into spinal cord. Molecular Therapy 15, 1796-1804 (Pubitemid 47434186)
96. Marino, P. et al. (2009) A polysialic acid mimetic peptide promotes functional recovery in a mouse model of spinal cord injury. Experimental Neurology 219, 163-174
97. Lu, P. and Tuszynski, M.H. (2008) Growth factors and combinatorial therapies for CNS regeneration. Experimental Neurology 209, 313-320 (Pubitemid 351174138)
98. Ramer, M.S., Priestley, J.V. and McMahon, S.B. (2000) Functional regeneration of sensory axons into the adult spinal cord. Nature 403, 312-316 (Pubitemid 30062387)
99. Kobayashi, N.R. et al. (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. Journal of Neuroscience 17, 9583-9595 (Pubitemid 28006402)
100. Schnell, L. et al. (1994) Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367, 170-173 (Pubitemid 24031697)
101. Blesch, A. et al. (2004) Axonal responses to cellularly delivered NT-4/5 after spinal cord injury. Molecular and Cellular Neurosciences 27, 190-201 (Pubitemid 39370100)
102. Blesch, A. and Tuszynski, M.H. (2003) Cellular GDNF delivery promotes growth of motor and dorsal column sensory axons after partial and complete spinal cord transections and induces remyelination. Journal of Comparative Neurology 467, 403-417 (Pubitemid 37421083)
103. Bennett, D.L. et al. (2006) Artemin has potent neurotrophic actions on injured C-fibres. Journal of the Peripheral Nervous System 11, 330-345 (Pubitemid 44730224)
104. Zhou, Z. et al. (2009) HSV-mediated transfer of artemin overcomes myelin inhibition to improve outcome after spinal cord injury. Molecular Therapy 17, 1173-1179
105. Park, S. and Hong, Y.W. (2006) Transcriptional regulation of artemin is related to neurite outgrowth and actin polymerization in mature DRG neurons. Neuroscience Letters 404, 61-66 (Pubitemid 44041790)
106. Paveliev, M., Airaksinen, M.S. and Saarma, M. (2004) GDNF family ligands activate multiple events during axonal growth in mature sensory neurons. Molecularand Cellular Neurosciences 25, 453-459 (Pubitemid 38366410)
107. Block, M.L., Zecca, L. and Hong, J.S. (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nature Reviews Neuroscience 8, 57-69 (Pubitemid 46011999)
108. Hashimoto, M. et al. (2005) Inflammation-induced GDNF improves locomotor function after spinal cord injury. Neuroreport 16, 99-102 (Pubitemid 40250377)
109. Dougherty, K.D., Dreyfus, C.F. and Black, I.B. (2000) Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/ macrophages after spinal cord injury. Neurobiology of Disease 7, 574-585 (Pubitemid 32044283)
110. Shechter, R. et al. (2009) Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Medicine 6, e1000113
111. Rolls, A. et al. (2008) Two faces of chondroitin sulfate proteoglycan in spinal cord repair: a role in microglia/macrophage activation. PLoS Medicine 5, e171
112. Raivich, G. et al. (2004) The AP-1 transcription factor c-Jun is required for efficient axonal regeneration. Neuron 43, 57-67 (Pubitemid 38952819)
113. Skene, J.H. (1989) Axonal growth-associated proteins. Annual Review of Neuroscience 12, 127-156
114. Qiu, J. et al. (2005) Conditioning injury-induced spinal axon regeneration requires signal transducer and activator of transcription 3 activation. Journal of Neuroscience 25, 1645-1653 (Pubitemid 40279269)
115. Rossi, F., Buffo, A. and Strata, P. (2001) Regulation of intrinsic regenerative properties and axonal plasticity in cerebellar Purkinje cells. Restor Neurol Neurosci 19, 85-94
116. + induce the dedifferentiation of axonal segments into growth cones. Journal of Neuroscience 17, 3568-3579
117. Chierzi, S. et al. (2005) The ability of axons to regenerate their growth cones depends on axonal type and age, and is regulated by calcium, cAMP and ERK. European Journal of Neuroscience 21, 2051-2062 (Pubitemid 40695229)
118. +)-triggered protease activity and cytoskeletal disassembly. Journal of Neuroscience 11, 3257-3267
119. Yoo, S. et al. (2003) Plasmalemmal sealing of transected mammalian neurites is a gradual process mediated by Ca(2+)-regulated proteins. Journal of Neuroscience Research 74, 541-551 (Pubitemid 37352076)
120. Spira, M.E. et al. (2003) Critical calpain-dependent ultrastructural alterations underlie the transformation of an axonal segment into a growth cone after axotomy of cultured Aplysia neurons. Journal of Comparative Neurology 457, 293-312 (Pubitemid 36158286)
121. Chu, G.K. and Tator, C.H. (2001) Calcium influx is necessary for optimal regrowth of transected neurites of rat sympathetic ganglion neurons in vitro. Neuroscience 102, 945-957 (Pubitemid 32155889)
122. Gitler, D. and Spira, M.E. (1998) Real time imaging of calcium-induced localized proteolytic activity after axotomy and its relation to growth cone formation. Neuron 20, 1123-1135 (Pubitemid 28293130)
123. Cai, D. et al. (1999) Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron 22, 89-101 (Pubitemid 29070096)
124. Li, Y. et al. (2003) Axon regeneration in goldfish and rat retinal ganglion cells: differential responsiveness to carbohydrates and cAMP. Journal of Neuroscience 23, 7830-7838 (Pubitemid 37052350)
125. Qiu, J. et al. (2002) Spinal axonregeneration induced by elevation of cyclic AMP. Neuron 34, 895-903 (Pubitemid 34722280)
126. Qiu, J., Cai, D. and Filbin, M.T. (2002) A role for cAMP in regeneration during development and after injury. Progress in Brain Research 137, 381-387 (Pubitemid 35460957)
127. Meyer-Franke, A. et al. (1998) Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons. Neuron 21, 681-693 (Pubitemid 28498778)
128. Gao, Y. et al. (2003) Neurotrophins elevate cAMP to reach a threshold required to overcome inhibition by MAG through extracellular signal-regulated kinase-dependent inhibition of phosphodiesterase. Journal of Neuroscience 23, 11770-11777 (Pubitemid 38021304)
129. Lange, P.S. et al. (2004) Novel roles for arginase in cell survival, regeneration, and translation in the central nervous system. Journal of Nutrition 134, 2812S-2817S (Pubitemid 39315227)
130. Neumann, S. and Woolf, C.J. (1999) Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23, 83-91 (Pubitemid 29262466)
131. Cai, D. et al. (2002) Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 35, 711-719
132. Cao, Z. et al. (2006) The cytokine interleukin-6 is sufficient but not necessary to mimic the peripheral conditioning lesion effect on axonal growth. Journal of Neuroscience 26, 5565-5573 (Pubitemid 44318407)
133. Domowicz, M.S. et al. (2008) Aggrecan is expressed by embryonic brain glia and regulates astrocyte development. Developmental Biology 315, 114-124
134. Schreyer, D.J. and Skene, J.H. (1993) Injury-associated induction of GAP-43 expression displays axon branch specificity in rat dorsal root ganglion neurons. Journal of Neurobiology 24, 959-970 (Pubitemid 23178785)
135. Seijffers, R., Allchorne, A.J. and Woolf, C.J. (2006) The transcription factor ATF-3 promotes neurite outgrowth. Molecular and Cellular Neurosciences 32, 143-154 (Pubitemid 43868103)
136. Atwal, J.K. et al. (2000) The TrkB-Shc site signals neuronal survival and local axon growth via MEK and P13-kinase. Neuron 27, 265-277
137. Liu, R.Y. and Snider, W.D. (2001) Different signaling pathways mediate regenerative versus developmental sensory axon growth. Journal of Neuroscience 21, RC164
138. Markus, A., Zhong, J. and Snider, W.D. (2002) Raf and akt mediate distinct aspects of sensory axon growth. Neuron 35, 65-76 (Pubitemid 34804323)
139. Gallo, G. and Letourneau, P.C. (1998) Localized sources of neurotrophins initiate axon collateral sprouting. Journal of Neuroscience 18, 5403-5414 (Pubitemid 28311956)
140. Gadient, R.A. and Otten, U.H. (1997) Interleukin-6 (IL-6)-a molecule with both beneficial and destructive potentials. Progress in Neurobiology 52, 379-390 (Pubitemid 27376652)
141. Ishizaki, T. et al. (2000) Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Molecular Pharmacology 57, 976-983 (Pubitemid 30253382)
142. Dergham, P. et al. (2002) Rho signaling pathway targeted to promote spinal cord repair. Journal of Neuroscience 22, 6570-6577 (Pubitemid 35386413)
143. Monnier, P.P. et al. (2003) The Rho/ROCKpathway mediates neurite growth-inhibitory activity associated with the chondroitin sulfate proteoglycans of the CNS glial scar. Molecular and Cellular Neurosciences 22, 319-330 (Pubitemid 36407595)
144. Borisoff, J.F. et al. (2003) Suppression of Rho-kinase activity promotes axonal growth on inhibitory CNS substrates. Molecular and Cellular Neurosciences 22, 405-416 (Pubitemid 36407602)
145. Chan, C.C. et al. (2005) Dose-dependent beneficial and detrimental effects of ROCK inhibitor Y27632 on axonal sprouting and functional recovery after rat spinal cord injury. Experimental Neurology 196, 352-364 (Pubitemid 41607824)
146. Fournier, A.E., Takizawa, B.T. and Strittmatter, S.M. (2003) Rho kinase inhibition enhances axonal regeneration in the injured CNS. Journal of Neuroscience 23, 1416-1423 (Pubitemid 36258920)
147. Wahl, S. et al. (2000) Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. Journal of Cell Biology 149, 263-270 (Pubitemid 30227145)
148. Sjoberg, J. and Kanje, M. (1990) Effects of repetitive conditioning crush lesions on regeneration of the rat sciatic nerve. Brain Research 530, 167-169 (Pubitemid 20348596)
149. Gaete, J., Kameid, G. and Alvarez, J. (1998) Regenerating axons of the rat require a local source of proteins. Neuroscience Letters 251, 197-200 (Pubitemid 28381081)
150. Verma, P. et al. (2005) Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. Journal of Neuroscience 25, 331-342 (Pubitemid 40105603)
151. Twiss, J.L. and van Minnen, J. (2006) New insights into neuronal regeneration: the role of axonal protein synthesis in pathfinding and axonal extension. Journal of Neurotrauma 23, 295-308 (Pubitemid 43726311)
152. Zheng, J.Q. et al. (2001) A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. Journal of Neuroscience 21, 9291-9303
153. Hanz, S. et al. (2003) Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40, 1095-1104 (Pubitemid 38032787)
154. Guirland, C. et al. (2004) Lipid rafts mediate chemotropic guidance of nerve growth cones. Neuron 42, 51-62 (Pubitemid 38456967)
155. Ledeen, R.W. et al. (1998) The role of GM1 and other gangliosides in neuronal differentiation. Overview and new finding. Annals of the New York Academy of Sciences 845, 161-175
156. Harel, R. and Futerman, A.H. (1993) Inhibition of sphingolipid synthesis affects axonal outgrowth in cultured hippocampal neurons. Journal of Biological Chemistry 268, 14476-14481 (Pubitemid 23195578)
157. Vyas, A.A. et al. (2002) Gangliosides are functional nerve cell ligands for myelin-associated glycoprotein (MAG), an inhibitor of nerve regeneration. Proceedings of the National Academy of Sciences of the United States of America 99, 8412-8417 (Pubitemid 34651066)
158. Yang, L.J. et al. (2006) Sialidase enhances spinal axon outgrowth in vivo. Proceedings of the National Academy of Sciences of the United States of America 103, 11057-11062 (Pubitemid 44148417)
159. Wu, G., Nakamura, K. and Ledeen, R.W. (1994) Inhibition of neurite outgrowth of neuroblastoma Neuro-2a cells by cholera toxin B-subunit and anti-GM1 antibody. Molecular and Chemical Neuropathology 21, 259-271 (Pubitemid 24174525)
160. Spirman, N. et al. (1984) Regenerative capacity of the goldfish visual system is affected by antibodies specific to gangliosides injected intraocularly. Journal of Neuroimmunology 6, 197-207 (Pubitemid 14101483)
161. Ferrari, G. et al. (1995) Prevention of apoptotic neuronal death by GM1 ganglioside. Involvement of Trk neurotrophin receptors. Journal of Biological Chemistry 270, 3074-3080
162. Rybak, S., Ginzburg, I. and Yavin, E. (1983) Gangliosides stimulate neurite outgrowth and induce tubulin mRNA accumulation in neural cells. Biochemical and Biophysical Research Communications 116, 974-980 (Pubitemid 14202680)
163. Schneider, J.S., Schroeder, J.A. and Rothblat, D.S. (1998) Differential recovery of sensorimotor function in GM1 ganglioside-treated vs. spontaneously recovered MPTP-treated cats: partial striatal dopaminergic reinnervation vs. neurochemical compensation. Brain Research 813, 82-87 (Pubitemid 29012520)
164. Geisler, F.H. et al. (2001) The Sygen multicenter acute spinal cord injury study. Spine 26, S87-98
165. Riboni, L. et al. (1990) Patterns of endogenous gangliosides and metabolic processing of exogenous gangliosides in cerebellar granule cells during differentiation in culture. Neurochemical Research 15, 1175-1183
166. Neugebauer, K.M. and Reichardt, L.F. (1991) Cell-surface regulation of beta 1-integrin activity on developing retinal neurons. Nature 350, 68-71 (Pubitemid 21926123)
167. Lemons, M.L. and Condic, M.L. (2006) Combined integrin activation and intracellular cAMP cause Rho GTPase dependent growth cone collapse on laminin-1. Experimental Neurology 202, 324-335 (Pubitemid 44767756)
168. Yanagida, H., Tanaka, J. and Maruo, S. (1999) Immunocytochemical localization of a cell adhesion molecule, integrin alpha5beta1, in nerve growth cones. Journal of Orthopaedic Science 4, 353-360 (Pubitemid 29506001)
169. Wallquist, W. et al. (2004) Dorsal root ganglion neurons up-regulate the expression of laminin-associated integrins after peripheral but not central axotomy. Journal of Comparative Neurology 480, 162-169 (Pubitemid 39536623)
170. Gardiner, N.J. et al. (2005) Alpha7 integrin mediates neurite outgrowth of distinct populations of adult sensory neurons. Molecular and Cellular Neurosciences 28, 229-240 (Pubitemid 40202585)
171. Ekstrom, P.A. et al. (2003) Involvement of alpha7beta1 integrin in the conditioning-lesion effect on sensory axon regeneration. Molecular and Cellular Neurosciences 22, 383-395 (Pubitemid 36407600)
172. Plantman, S. et al. (2005) Integrin messenger RNAs in the red nucleus after axotomy and neurotrophic administration. Neuroreport 16, 709-713 (Pubitemid 40768643)
173. Andrews, M.R. et al. (2009) Alpha9 integrin promotes neurite outgrowth on tenascin-C and enhances sensory axon regeneration. Journal of Neuroscience 29, 5546-5557