Sensory axon regeneration: Rebuilding functional connections in the spinal cord

Trends in Neurosciences

Volumn 35, Issue 3, 2012, Pages 156-163

  Smith, George M ^a,c   Falone, Anthony E ^b   Frank, Eric ^b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TEMPLE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHONDROITIN SULFATE; NERVE GROWTH FACTOR; NEURITE PROMOTING FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN 3; PROTEIN NOGO; PROTEOGLYCAN;

ASTROCYTE; CELL TYPE; DORSAL ROOT; GANGLION; MYELINATED NERVE; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SCHWANN CELL; SENSORY NERVE; SPINAL CORD; SPINAL GANGLION; SPINE INJURY; SYNAPSE; UPREGULATION;

ANIMALS; AXONS; GANGLIA, SPINAL; HUMANS; NERVE CRUSH; NERVE REGENERATION; NEURAL PATHWAYS; SENSORY RECEPTOR CELLS; SPINAL CORD; SPINAL CORD INJURIES; UP-REGULATION;

EID: 84857686109     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2011.10.006     Document Type: Review

References (82)

1. Schwab J.M., et al. Experimental strategies to promote spinal cord regeneration: an integrative perspective. Prog. Neurobiol. 2006, 78:91-116.
2. Rossignol S., et al. Spinal cord injury: time to move?. J. Neurosci. 2007, 27:11782-11792.
3. Cafferty W.B., et al. Axonal growth therapeutics: regeneration or sprouting or plasticity?. Trends Neurosci. 2008, 31:215-220.
4. Blesch A., Tuszynski M.H. Spinal cord injury: plasticity, regeneration and the challenge of translational drug development. Trends Neurosci. 2009, 32:41-47.
5. Basso D.M. Neuroanatomical substrates of functional recovery after experimental spinal cord injury: implications of basic science research for human spinal cord injury. Phys. Ther. 2000, 80:808-817.
6. Sipski M.L., Richards J.S. Spinal cord injury rehabilitation: state of the science. Am. J. Phys. Med. Rehabil. 2006, 85:310-342.
7. Aguayo A.J., et al. Influences of the glial environment on the elongation of axons after injury: transplantation studies in adult rodents. J. Exp. Biol. 1981, 95:231-240.
8. David S., Aguayo A.J. Axonal elongation into peripheral nervous system 'bridges' after central nervous system injury in adult rats. Science 1981, 214:931-933.
9. Ramón y Cajal, S. (1928) Degeneration and Regeneration of the Nervous System, translations by DeFelipe, J. and E.G. Jones, Oxford University Press, London.
10. Di Maio A., et al. In vivo imaging of dorsal root regeneration: rapid immobilization and presynaptic differentiation at the CNS/PNS border. J. Neurosci. 2011, 31:4569-4582.
11. Carlstedt T. Regenerating axons form nerve terminals at astrocytes. Brain Res. 1985, 347:188-191.
12. Liuzzi F.J., Lasek R.J. Astrocytes block axonal regeneration in mammals by activating the physiological stop pathway. Science 1987, 237:642-645.
13. Reier P.J., et al. Development of embryonic spinal cord transplants in the rat. Brain Res. 1983, 312:201-219.
14. George R., Griffin J.W. Delayed macrophage responses and myelin clearance during Wallerian degeneration in the central nervous system: the dorsal radiculotomy model. Exp. Neurol. 1994, 129:225-236.
15. Avellino A.M., et al. Differential macrophage responses in the peripheral and central nervous system during wallerian degeneration of axons. Exp. Neurol. 1995, 136:183-198.
16. Liu L., et al. Glial cell proliferation in the spinal cord after dorsal rhizotomy or sciatic nerve transection in the adult rat. Exp. Brain Res. 2000, 131:64-73.
17. Aldskogius H., Kozlova E.N. Central neuron-glial and glial-glial interactions following axon injury. Prog. Neurobiol. 1998, 55:1-26.
18. Filous A.R., et al. Immature astrocytes promote CNS axonal regeneration when combined with chondroitinase ABC. Dev Neurobiol 2010, 70:826-841.
19. Lee J.K., et al. Assessing spinal axon regeneration and sprouting in Nogo-, MAG-, and OMgp-deficient mice. Neuron 2010, 66:663-670.
20. Giger R.J., et al. Mechanisms of CNS myelin inhibition: evidence for distinct and neuronal cell type specific receptor systems. Restor. Neurol. Neurosci. 2008, 26:97-115.
21. Atwal J.K., et al. PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 2008, 322:967-970.
22. Filbin M.T. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 2003, 4:703-713.
23. Caroni P., Schwab M.E. Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1988, 1:85-96.
24. Li S., et al. Blockade of Nogo-66, myelin-associated glycoprotein, and oligodendrocyte myelin glycoprotein by soluble Nogo-66 receptor promotes axonal sprouting and recovery after spinal injury. J. Neurosci. 2004, 24:10511-10520.
25. Ji B., et al. Effect of combined treatment with methylprednisolone and soluble Nogo-66 receptor after rat spinal cord injury. Eur. J. Neurosci. 2005, 22:587-594.
26. Li S., et al. Transgenic inhibition of Nogo-66 receptor function allows axonal sprouting and improved locomotion after spinal injury. Mol. Cell. Neurosci. 2005, 29:26-39.
27. Wang X., et al. Delayed Nogo receptor therapy improves recovery from spinal cord contusion. Ann. Neurol. 2006, 60:540-549.
28. Harvey P.A., et al. Blockade of Nogo receptor ligands promotes functional regeneration of sensory axons after dorsal root crush. J. Neurosci. 2009, 29:6285-6295.
29. Peng X., et al. Soluble Nogo receptor down-regulates expression of neuronal Nogo-A to enhance axonal regeneration. J. Biol. Chem. 2010, 285:2783-2795.
30. Pindzola R.R., et al. Putative inhibitory extracellular matrix molecules at the dorsal root entry zone of the spinal cord during development and after root and sciatic nerve lesions. Dev. Biol. 1993, 156:34-48.
31. Zhang Y., et al. Correlation between putative inhibitory molecules at the dorsal root entry zone and failure of dorsal root axonal regeneration. Mol. Cell. Neurosci. 2001, 17:444-459.
32. Beggah A.T., et al. Lesion-induced differential expression and cell association of Neurocan, Brevican, Versican V1 and V2 in the mouse dorsal root entry zone. Neuroscience 2005, 133:749-762.
33. McPhail L.T., et al. The astrocytic barrier to axonal regeneration at the dorsal root entry zone is induced by rhizotomy. Eur. J. Neurosci. 2005, 21:267-270.
34. Cafferty W.B., et al. Chondroitinase ABC-mediated plasticity of spinal sensory function. J. Neurosci. 2008, 28:11998-12009.
35. Smith G.M., Hale J.H. Macrophage/microglia regulation of astrocytic tenascin: synergistic action of transforming growth factor-beta and basic fibroblast growth factor. J. Neurosci. 1997, 17:9624-9633.
36. Asher R.A., et al. Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells. J. Neurosci. 2002, 22:2225-2236.
37. Smith G.M., Strunz C. Growth factor and cytokine regulation of chondroitin sulfate proteoglycans by astrocytes. Glia 2005, 52:209-218.
38. Masuda T., et al. Netrin-1 signaling for sensory axons: Involvement in sensory axonal development and regeneration. Cell Adhes. Migr. 2009, 3:171-173.
39. Yiu G., He Z. Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 2006, 7:617-627.
40. Shen Y., et al. PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 2009, 326:592-596.
41. Tan C.L., et al. Integrin activation promotes axon growth on inhibitory chondroitin sulfate proteoglycans by enhancing integrin signaling. J. Neurosci. 2011, 31:6289-6295.
42. Bradbury E.J., et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002, 416:636-640.
43. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 2004, 5:146-156.
44. Steinmetz M.P., et al. Chronic enhancement of the intrinsic growth capacity of sensory neurons combined with the degradation of inhibitory proteoglycans allows functional regeneration of sensory axons through the dorsal root entry zone in the mammalian spinal cord. J. Neurosci. 2005, 25:8066-8076.
45. Quaglia X., et al. Delayed priming promotes CNS regeneration post-rhizotomy in Neurocan and Brevican-deficient mice. Brain 2008, 131:240-249.
46. Chong M.S., et al. Axonal regeneration from injured dorsal roots into the spinal cord of adult rats. J. Comp. Neurol. 1999, 410:42-54.
47. Ramer M.S., et al. Functional regeneration of sensory axons into the adult spinal cord. Nature 2000, 403:312-316.
48. Ramer M.S., et al. Two-tiered inhibition of axon regeneration at the dorsal root entry zone. J. Neurosci. 2001, 21:2651-2660.
49. Busch S.A., et al. Overcoming macrophage-mediated axonal dieback following CNS injury. J. Neurosci. 2009, 29:9967-9976.
50. Wang R., et al. Persistent restoration of sensory function by immediate or delayed systemic artemin after dorsal root injury. Nat. Neurosci. 2008, 11:488-496.
51. Zhang Y., et al. NT-3 delivered by an adenoviral vector induces injured dorsal root axons to regenerate into the spinal cord of adult rats. J. Neurosci. Res. 1998, 54:554-562.
52. Romero M.I., et al. Functional regeneration of chronically injured sensory afferents into adult spinal cord after neurotrophin gene therapy. J. Neurosci. 2001, 21:8408-8416.
53. Tang X.Q., et al. Targeting sensory axon regeneration in adult spinal cord. J. Neurosci. 2007, 27:6068-6078.
54. Romero M.I., et al. Extensive sprouting of sensory afferents and hyperalgesia induced by conditional expression of nerve growth factor in the adult spinal cord. J. Neurosci. 2000, 20:4435-4445.
55. Tang X.Q., et al. Functional repair after dorsal root rhizotomy using nerve conduits and neurotrophic molecules. Eur. J. Neurosci. 2004, 20:1211-1218.
56. Alto L.T., et al. Chemotropic guidance facilitates axonal regeneration and synapse formation after spinal cord injury. Nat. Neurosci. 2009, 12:1106-1113.
57. Kadoya K., et al. Combined intrinsic and extrinsic neuronal mechanisms facilitate bridging axonal regeneration one year after spinal cord injury. Neuron 2009, 64:165-172.
58. Harvey P., et al. Topographically specific regeneration of sensory axons in the spinal cord. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:11585-11590.
59. Liu S., et al. Neurotrophin 3 improves delayed reconstruction of sensory pathways after cervical dorsal root injury. Neurosurgery 2011, 68:450-461. discussion 461.
60. Dunlop S.A. Activity-dependent plasticity: implications for recovery after spinal cord injury. Trends Neurosci. 2008, 31:410-418.
61. Galtrey C.M., et al. Promoting plasticity in the spinal cord with chondroitinase improves functional recovery after peripheral nerve repair. Brain 2007, 130:926-939.
62. Garcia-Alias G., et al. Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat. Neurosci. 2009, 12:1145-1151.
63. Ramer M.S., et al. Neurotrophin-3-mediated regeneration and recovery of proprioception following dorsal rhizotomy. Mol. Cell. Neurosci. 2002, 19:239-249.
64. MacDermid V.E., et al. A soluble Nogo receptor differentially affects plasticity of spinally projecting axons. Eur. J. Neurosci. 2004, 20:2567-2579.
65. Wong L.F., et al. Retinoic acid receptor beta2 promotes functional regeneration of sensory axons in the spinal cord. Nat. Neurosci. 2006, 9:243-250.
66. Averill S., et al. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur. J. Neurosci. 1995, 7:1484-1494.
67. Todd A.J. Neuronal circuitry for pain processing in the dorsal horn. Nat. Rev. Neurosci. 2010, 11:823-836.
68. Molliver D.C., et al. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 1997, 19:849-861.
69. Kashiba H., et al. Distribution and colocalization of NGF and GDNF family ligand receptor mRNAs in dorsal root and nodose ganglion neurons of adult rats. Brain Res. Mol. Brain Res. 2003, 110:52-62.
70. Grant G. Primary afferent projections to the spinal cord. The Rat Nervous System 1995, 61-66. Academic Press. G. Paxinos (Ed.).
71. Klein R., et al. Disruption of the neurotrophin-3 receptor gene trkC eliminates la muscle afferents and results in abnormal movements. Nature 1994, 368:249-251.
72. Tessarollo L., et al. Targeted mutation in the neurotrophin-3 gene results in loss of muscle sensory neurons. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:11844-11848.
73. Brown A.G. Organization of the Spinal Cord 1981, Springer-Verlag.
74. Tessier-Lavigne M., Goodman C.S. The molecular biology of axon guidance. Science 1996, 274:1123-1133.
75. Cao X., Shoichet M.S. Investigating the synergistic effect of combined neurotrophic factor concentration gradients to guide axonal growth. Neuroscience 2003, 122:381-389.
76. Taylor L., et al. Neurotrophin-3 gradients established by lentiviral gene delivery promote short-distance axonal bridging beyond cellular grafts in the injured spinal cord. J. Neurosci. 2006, 26:9713-9721.
77. Oudega M., Hagg T. Nerve growth factor promotes regeneration of sensory axons into adult rat spinal cord. Exp. Neurol. 1996, 140:218-229.
78. Bamber N.I., et al. Neurotrophins BDNF and NT-3 promote axonal re-entry into the distal host spinal cord through Schwann cell-seeded mini-channels. Eur. J. Neurosci. 2001, 13:257-268.
79. Bonner J.F., et al. Grafted neural progenitors integrate and restore synaptic connectivity across the injured spinal cord. J. Neurosci. 2011, 31:4675-4686.
80. Dontchev V.D., Letourneau P.C. Nerve growth factor and semaphorin 3A signaling pathways interact in regulating sensory neuronal growth cone motility. J. Neurosci. 2002, 22:6659-6669.
81. Bennett D.L., et al. The glial cell line-derived neurotrophic factor family receptor components are differentially regulated within sensory neurons after nerve injury. J. Neurosci. 2000, 20:427-437.
82. Orozco O.E., et al. GFRalpha3 is expressed predominantly in nociceptive sensory neurons. Eur. J. Neurosci. 2001, 13:2177-2182.