Retrograde signaling in injured nerve - The axon reaction revisited

Journal of Neurochemistry

Volumn 99, Issue 1, 2006, Pages 13-19

  Hanz, Shlomit ^a,b   Fainzilber, Mike ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Axon; Injury; Retrograde; Signal

Indexed keywords

CARRIER PROTEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; KARYOPHERIN; MITOGEN ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; VIMENTIN;

BINDING SITE; FACILITATION; LINKAGE ANALYSIS; MOLECULE; MOTOR NERVE CONDUCTION; NERVE CONDUCTION; NERVE DEGENERATION; NERVE FIBER; NERVE FIBER REGENERATION; NERVE INJURY; NERVE POTENTIAL; NERVE REGENERATION; NERVE TRANSECTION; NEUROFILAMENT; NONHUMAN; OPTIC NERVE; PERIKARYON; PERIPHERAL NERVE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RETROGRADE NERVE FIBER TRANSPORT; REVIEW; SENSORY NERVE CONDUCTION; SIGNAL TRANSDUCTION;

ANIMALS; AXONAL TRANSPORT; AXONS; HUMANS; MODELS, NEUROLOGICAL; NERVE REGENERATION; SIGNAL TRANSDUCTION; TRAUMA, NERVOUS SYSTEM;

EID: 33748714938     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04089.x     Document Type: Review

References (74)

1. Ambron R. T. and Walters E. T. (1996) Priming events and retrograde injury signals. A new perspective on the cellular and molecular biology of nerve regeneration. Mol Neurobiol. 13, 61-79.
2. Bassell G. J. and Twiss J. L. (2006) RNA exodus to Israel: RNA controlling function in the far reaches of the neuron. Workshop on RNA control on neuronal function. EMBO Rep 7, 31-35.
3. Berdan R. C., Easaw J. C. and Wang R. (1993) Alterations in membrane potential after axotomy at different distances from the soma of an identified neuron and the effect of depolarization on neurite outgrowth and calcium channel expression. J. Neurophysiol. 69, 151-164.
4. Blackmore M. and Letourneau P. C. (2006) Changes within maturing neurons limit axonal regeneration in the developing spinal cord. J. Neurobiol. 66, 348-360.
5. Bonilla I. E., Tanabe K. and Strittmatter S. M. (2002) Small proline-rich repeat protein 1A is expressed by axotomized neurons and promotes axonal outgrowth. J. Neurosci. 22, 1303-1315.
6. Bowman A. B., Kamal A., Ritchings B. W., Philp A. V., McGrail M., Gindhart J. G. and Goldstein L. S. (2000) Kinesin-dependent axonal transport is mediated by the sunday driver (SYD) protein. Cell 103, 583-594.
7. Bronfman F. C. and Fainzilber M. (2004) Multi-tasking by the p75 receptor: sortilin things out? EMBO Reports 5, 867-871.
8. Cao Z., Gao Y., Bryson J. B. et al. (2006) The cytokine interleukin-6 is sufficient but not necessary to mimic the peripheral conditioning lesion effect on axonal growth. J. Neurosci. 26, 5565-5573.
9. Caroni P. (1998) Neuro-regeneration: plasticity for repair and adaptation. Essays Biochem. 33, 53-64.
10. Carulli D., Laabs T., Geller H. M. and Fawcett J. W. (2005) Chondroitin sulfate proteoglycans in neural development and regeneration. Curr. Opin. Neurobiol. 15, 116-120.
11. Cavalli V., Kujala P., Klumperman J. and Goldstein L. S. (2005) Sunday Driver links axonal transport to damage signaling. J. Cell Biol. 168, 775-787.
12. Chierzi S., Ratto G. M., Verma P. and Fawcett J. W. (2005) The ability of axons to regenerate their growth cones depends on axonal type and age, and is regulated by calcium, cAMP and ERK. Eur J. Neurosci. 21, 2051-2062.
13. Cragg B. G. (1970) What is the signal for chromatolysis? Brain Res. 23, 1-21.
14. Curtis R., Tonra J. R., Stark J. L., Adryan K. M., Park J. S., Cliffer K. D., Lindsay R. M. and DiStefano P. S. (1998) Neuronal injury increases retrograde axonal transport of the neurotrophins to spinal sensory neurons and motor neurons via multiple receptor mechanisms. Mol Cell Neurosci. 12, 105-118.
15. Dusart I., Ghoumari A., Wehrle R., Morel M. P., Bouslama-Oueghlani L., Camand E. and Sotelo C. (2005) Cell death and axon regeneration of Purkinje cells after axotomy: challenges of classical hypotheses of axon regeneration. Brain Res. Brain Res. Rev. 49, 300-316.
16. Fawcett J. W. and Keynes R. J. (1990) Peripheral nerve regeneration. Annu. Rev. Neurosci. 13, 43-60.
17. Fischer D., He Z. and Benowitz. L. I. (2004a) Counteracting the Nogo receptor enhances optic nerve regeneration if retinal ganglion cells are in an active growth state. J. Neurosci. 24, 1646-1651.
18. Fischer D., Petkova V., Thanos S. and Benowitz. L. I. (2004b) Switching mature retinal ganglion cells to a robust growth state in vivo: gene expression and synergy with RhoA inactivation. J. Neurosci. 24, 8726-8740.
19. Gold B. G. (1997) Axonal regeneration of sensory nerves is delayed by continuous intrathecal infusion of nerve growth factor. Neuroscience 76, 1153-1158.
20. Goldberg J. L. (2003) How does an axon grow? Genes Dev 17, 941-958.
21. Goldberg J. L. (2004) Intrinsic neuronal regulation of axon and dendrite growth. Curr. Opin. Neurobiol. 14, 551-557.
22. Hanz S. and Fainzilber M. (2004) Integration of retrograde axonal and nuclear transport mechanisms in neurons: implications for therapeutics. Neuroscientist 10, 404-408.
23. Hanz S., Perlson E., Willis D. et al. (2003) Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40, 1095-1104.
24. Kenney A. M. and Kocsis J. D. (1998) Peripheral axotomy induces long-term c-Jun amino-terminal kinase-1 activation and activator protein-1 binding activity by c-Jun and junD in adult rat dorsal root ganglia In vivo. J. Neurosci. 18, 1318-1328.
25. Lee N., Neitzel K. L., Devlin B. K. and MacLennan A. J. (2004) STAT3 phosphorylation in injured axons before sensory and motor neuron nuclei: potential role for STAT3 as a retrograde signaling transcription factor. J. Comp Neurol. 474, 535-545.
26. Levy J. R. and Holzbaur E. L. (2006) Cytoplasmic dynein/dynactin function and dysfunction in motor neurons. Int. J. Dev Neurosci. 24, 103-111.
27. Lieberman A. R. (1971) The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int. Rev. Neurobiol. 14, 49-124.
28. Lindwall C., Dahlin L., Lundborg G. and Kanje M. (2004) Inhibition of c-Jun phosphorylation reduces axonal outgrowth of adult rat no-dose ganglia and dorsal root ganglia sensory neurons. Mol Cell Neurosci. 27, 267-279.
29. Lindwall C. and Kanje M. (2005) Retrograde axonal transport of JNK signaling molecules influence injury induced nuclear changes in p-c-Jun and ATF3 in adult rat sensory neurons. Mol Cell Neurosci. 29, 269-282.
30. Lu P., Jones L. L. and Tuszynski M. H. (2005) BDNF-expressing marrow stromal cells support extensive axonal growth at sites of spinal cord injury. Exp Neurol. 191, 344-360.
31. Mandolesi G., Madeddu F., Bozzi Y., Maffei L. and Ratto G. M. (2004) Acute physiological response of mammalian central neurons to axotomy: ionic regulation and electrical activity. Faseb J. 18, 1934-1936.
32. Mesika A., Kiss V., Brumfeld V., Ghosh G. and Reich Z. (2005) Enhanced intracellular mobility and nuclear accumulation of DNA plasmids associated with a karyophilic protein. Hum Gene Ther 16, 200-208.
33. Moffett S. B. (2000) Regeneration as an application of gastropod neural plasticity. Microsc Res. Tech 49, 579-588.
34. Nadeau S., Hein P., Fernandes K. J., Peterson A. C. and Miller F. D. (2005) A transcriptional role for C/EBP beta in the neuronal response to axonal injury. Mol Cell Neurosci. 29, 525-535.
35. Neumann S., Bradke F., Tessier-Lavigne M. and Basbaum A. I. (2002) Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34, 885-893.
36. Obata K., Yamanaka H., Dai Y., Mizushima T., Fukuoka T., Tokunaga A. and Noguchi K. (2004) Differential activation of MAPK in injured and uninjured DRG neurons following chronic constriction injury of the sciatic nerve in rats. Eur J. Neurosci. 20, 2881-2895.
37. Otis K. O., Thompson K. R. and Martin K. C. (2006) Importin-mediated nuclear transport in neurons. Curr. Opin. Neurobiol., 16, 329-335.
38. Perlson E., Hanz. S., Ben-Yaakov K., Segal-Ruder Y., Seger R. and Fainzilber M. (2005) Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 45, 715-726.
39. Perlson E., Hanz. S., Medzihradszky K. F., Burlingame A. L. and Fainzilber M. (2004a) From snails to sciatic nerve: Retrograde injury signaling from axon to soma in lesioned neurons. J. Neurobiol. 58, 287-294.
40. Perlson E., Medzihradszky K. F., Darula Z., Munno D. W., Syed N. I., Burlingame A. L. and Fainzilber M. (2004b) Differential Proteomics Reveals Multiple Components in Retrogradely Transported Axoplasm After Nerve Injury. Mol Cell Proteomics 3, 510-520.
41. Pfister K. K., Shah P. R., Hummerich H., Russ A., Cotton J., Annuar A. A., King S. M. and Fisher E. M. (2006) Genetic Analysis of the Cytoplasmic Dynein Subunit Families. PLoS Genet 2, e1.
42. Povelones M., Tran K., Thanos D. and Ambron R. T. (1997) An NF-kappaB-like transcription factor in axoplasm is rapidly inactivated after nerve injury in Aplysia. J. Neurosci. 17, 4915-4920.
43. Qiu J., Cafferty W. B., McMahon S. B. and Thompson S. W. (2005) Conditioning injury-induced spinal axon regeneration requires signal transducer and activator of transcription 3 activation. J. Neurosci. 25, 1645-1653.
44. Qiu J., Cai D., Dai H., McAtee M., Hoffman P. N., Bregman B. S. and Filbin M. T. (2002) Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34, 895-903.
45. Raivich G., Hellweg R. and Kreutzberg G. W. (1991) NGF receptor-mediated reduction in axonal NGF uptake and retrograde transport following sciatic nerve injury and during regeneration. Neuron 7, 151-164.
46. Rajan P., Stewart C. L. and Fink J. S. (1995) LIF-mediated activation of STAT proteins after neuronal injury in vivo. Neuroreport 6, 2240-2244.
47. Reynolds A. J., Hendry I. A. and Bartlett S. E. (2001) Anterograde and retrograde transport of active extracellular signal-related kinase 1 (ERK1) in the ligated rat sciatic nerve. Neuroscience 105, 761-771.
48. Salata M. W., Dillman J. F.3rd, Lye R. J. and Pfister K. K. (2001) Growth factor regulation of cytoplasmic dynein intermediate chain subunit expression preceding neurite extension. J. Neurosci. Res. 65, 408-416.
49. Salman H., Abu-Arish A., Oliel S., Loyter A., Klafter J., Granek R. and Elbaum M. (2005) Nuclear localization signal peptides induce molecular delivery along microtubules. Biophys. J. 89, 2134-2145.
50. Schmied R. and Ambron R. T. (1997) A nuclear localization signal targets proteins to the retrograde transport system, thereby evading uptake into organelles in aplysia axons. J. Neurobiol. 33, 151-160.
51. Schmied R., Huang C. C., Zhang X. P., Ambron D. A. and Ambron R. T. (1993) Endogenous axoplasmic proteins and proteins containing nuclear localization signal sequences use the retrograde axonal transport/nuclear import pathway in Aplysia neurons. J. Neurosci. 13, 4064-4071.
52. Schwaiger F. W., Hager G., Schmitt A. B. et al. (2000) Peripheral but not central axotomy induces changes in Janus kinases (JAK) and signal transducers and activators of transcription (STAT). Eur J. Neurosci. 12, 1165-1176.
53. Seijffers R., Allchorne A. J. and Woolf C. J. (2006) The transcription factor ATF-3 promotes neurite outgrowth. Mol Cell Neurosci. 32, 143-154.
54. Shadiack A. M., Sun Y. and Zigmond R. E. (2001) Nerve growth factor antiserum induces axotomy-like changes in neuropeptide expression in intact sympathetic and sensory neurons. J. Neurosci. 21, 363-371.
55. Smith D. S. and Skene J. H. (1997) A transcription-dependent switch controls competence of adult neurons for distinct modes of axon growth. J. Neurosci. 17, 646-658.
56. Snider W. D., Zhou F. Q., Zhong J. and Markus A. (2002) Signaling the pathway to regeneration. Neuron 35, 13-16.
57. Steinmetz. M. P., Horn K. P., Tom V. J., Miller J. H., Busch S. A., Nair D., Silver D. J. and Silver J. (2005) 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. 25, 8066-8076.
58. Sung Y. J., Povelones M. and Ambron R. T. (2001) RISK-1: a novel MAPK homologue in axoplasm that is activated and retrogradely transported after nerve injury. J. Neurobiol. 47, 67-79.
59. Sung Y. J., Walters E. T. and Ambron R. T. (2004) A neuronal isoform of protein kinase G couples mitogen-activated protein kinase nuclear import to axotomy-induced long-term hyperexcitability in Aplysia sensory neurons. J. Neurosci. 24, 7583-7595.
60. Teng F. Y. and Tang B. L. (2005) Why do Nogo/Nogo-66 receptor gene knockouts result in inferior regeneration compared to treatment with neutralizing agents? J. Neurochem. 94, 865-874.
61. Thompson K. R., Otis K. O., Chen D. Y., Zhao Y., O'Dell T. J. and Martin K. C. (2004) Synapse to nucleus signaling during long-term synaptic plasticity; a role for the classical active nuclear import pathway. Neuron 44, 997-1009.
62. Tuszynski M. H., Grill R., Jones L. L., Brant A., Blesch A., Low K., Lacroix S. and Lu P. (2003) NT-3 gene delivery elicits growth of chronically injured corticospinal axons and modestly improves functional deficits after chronic scar resection. Exp Neurol. 181, 47-56.
63. Verhey K. J., Meyer D., Deehan R., Blenis J., Schnapp B. J., Rapoport T. A. and Margolis B. (2001) Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J. Cell Biol. 152, 959-970.
64. Weis K. (2003) Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell 112, 441-451.
65. Wellmann H., Kaltschmidt B. and Kaltschmidt C. (2001) Retrograde Transport of Transcription Factor NF-kappa B in Living Neurons. J. Biol. Chem. 276, 11 821-11 829.
66. Willis D. E. and Twiss J. L. (2006) The evolving roles of axonally synthesized proteins in regeneration. Curr. Opin. Neurobiol. 16, 111-118.
67. Yamashita T., Fujitani M., Yamagishi S., Hata K. and Mimura F. (2005) Multiple signals regulate axon regeneration through the nogo receptor complex. Mol Neurobiol. 32, 105-111.
68. Yano H. and Chao M. V. (2004) Mechanisms of neurotrophin receptor vesicular transport. J. Neurobiol. 58, 244-257.
69. Yao G. L., Kato H., Khalil M., Kiryu S. and Kiyama H. (1997) Selective upregulation of cytokine receptor subchain and their intracellular signalling molecules after peripheral nerve injury. Eur J. Neurosci. 9, 1047-1054.
70. Yin Y., Henzl M. T., Lorber B., Nakazawa T., Thomas T. T., Jiang F., Langer R. and Benowitz. L. I. (2006) Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat Neurosci. 9, 843-852.
71. Zhang X. P. and Ambron R. T. (2000) Positive injury signals induce growth and prolong survival in Aplysia neurons. J. Neurobiol. 45, 84-94.
72. Ziv N. E. and Spira M. E. (1993) Spatiotemporal distribution of Ca2+ following axotomy and throughout the recovery process of cultured Aplysia neurons. Eur J. Neurosci. 5, 657-668.
73. Ziv N. E. and Spira M. E. (1995) Axotomy induces a transient and localized elevation of the free intracellular calcium concentration to the millimolar range. J. Neurophysiol. 74, 2625-2637.
74. Zrouri H., Le Goascogne C., Li W. W., Pierre M. and Courtin F. (2004) The role of MAP kinases in rapid gene induction after lesioning of the rat sciatic nerve. Eur J. Neurosci. 20, 1811-1818.