Axonal degeneration and regeneration: A mechanistic tug-of-war

Journal of Neurochemistry

Volumn 108, Issue 1, 2009, Pages 23-32

  Hilliard, Massimo A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Axonal regeneration; Neurodegenerative diseases; Pruning; Spinal cord injury; Wallerian degeneration; WldS

Indexed keywords

CYCLIC AMP; NICOTINAMIDE NUCLEOTIDE ADENYLYLTRANSFERASE; OXIDOPAMINE; PACLITAXEL; UBIQUITIN; VINCRISTINE;

ALZHEIMER DISEASE; DEGENERATIVE DISEASE; GENE MUTATION; GLAUCOMA; HUMAN; HUNTINGTON CHOREA; MOTOR NEURON DISEASE; NERVE CELL NECROSIS; NERVE FIBER DEGENERATION; NERVE FIBER REGENERATION; NERVE INJURY; NEUROPATHY; NEUROPHYSIOLOGY; NONHUMAN; OLFACTORY RECEPTOR; PARKINSON DISEASE; PATHOGENESIS; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; REVIEW;

ANIMALS; AXONS; HUMANS; NERVE DEGENERATION; NERVE REGENERATION; NEURODEGENERATIVE DISEASES;

INVERTEBRATA; VERTEBRATA; WALLERIA;

EID: 57249111802     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05754.x     Document Type: Review

References (107)

1. S) with improved preservation of neuromuscular synapses. Eur. J. Neurosci. 21, 271 277.
2. Araki T., Sasaki Y. Milbrandt J. (2004) Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305, 1010 1013.
3. Awasaki T., Tatsumi R., Takahashi K., Arai K., Nakanishi Y., Ueda R. Ito K. (2006) Essential role of the apoptotic cell engulfment genes draper and ced-6 in programmed axon pruning during Drosophila metamorphosis. Neuron 50, 855 867.
4. Bareyre F. M., Kerschensteiner M., Misgeld T. Sanes J. R. (2005) Transgenic labeling of the corticospinal tract for monitoring axonal responses to spinal cord injury. Nat. Med. 11, 1355 1360.
5. Bennett V. Baines A. J. (2001) Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 81, 1353 1392.
6. Benson M. D., Romero M. I., Lush M. E., Lu Q. R., Henkemeyer M. Parada L. F. (2005) Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proc. Natl Acad. Sci. USA 102, 10694 10699.
7. Bhatt D. H., Otto S. J., Depoister B. Fetcho J. R. (2004) Cyclic AMP-induced repair of zebrafish spinal circuits. Science 305, 254 258.
8. Bisby M. A. Chen S. (1990) Delayed Wallerian degeneration in sciatic nerves of C57BL/Ola mice is associated with impaired regeneration of sensory axons. Brain Res. 530, 117 120.
9. Blackmore M. Letourneau P. C. (2006a) Changes within maturing neurons limit axonal regeneration in the developing spinal cord. J. Neurobiol. 66, 348 360.
10. Blackmore M. Letourneau P. C. (2006b) L1, b1 integrin, and cadherins mediate axonal regeneration in the embryonic spinal cord. J. Neurobiol. 66, 1564 1583.
11. Bradbury E. J. McMahon S. B. (2006) Spinal cord repair strategies: why do they work? Nat. Rev. Neurosci. 7, 644 653.
12. Brown M. C., Lunn E. R. Perry V. H. (1992) Consequences of slow Wallerian degeneration for regenerating motor and sensory axons. J. Neurobiol. 23, 521 536.
13. Brown M. C., Perry V. H., Hunt S. P. Lapper S. R. (1994) Further studies on motor and sensory nerve regeneration in mice with delayed Wallerian degeneration. Eur. J. Neurosci. 6, 420 428.
14. Carbonetto S. Muller K. J. (1977) A regenerating neuron in the leech can form an electrical synapse on its severed axon segment. Nature 267, 450 452.
15. Carulli D., Laabs T., Geller H. M. Fawcett J. W. (2005) Chondroitin sulfate proteoglycans in neural development and regeneration. Curr. Opin. Neurobiol. 15, 116 120.
16. Cavanagh J. B. (1964) The significance of the "dying back" process in experimental and human neurological disease. Int. Rev. Exp. Pathol. 3, 219 267.
17. Chen M. S., Huber A. B., van der Haar M. E., Frank M., Schnell L., Spillmann A. A., Christ F. Schwab M. E. (2000) Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403, 434 439.
18. Cifuentes-Diaz C., Nicole S., Velasco M. E., Borra-Cebrian C., Panozzo C., Frugier T., Millet G., Roblot N., Joshi V. Melki J. (2002) Neurofilament accumulation at the motor endplate and lack of axonal sprouting in a spinal muscular atrophy mouse model. Hum. Mol. Genet. 11, 1439 1447.
19. Coleman M. (2005) Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 6, 889 898.
20. S) mouse. Proc. Natl Acad. Sci. USA 95, 9985 9990.
21. S) mouse. Proc. Natl Acad. Sci. USA 97, 11377 11382.
22. Conforti L., Adalbert R. Coleman M. P. (2007a) Neuronal death: where does the end begin? Trends Neurosci. 30, 159 166.
23. S to delay Wallerian degeneration. Cell Death Differ. 14, 116 127.
24. Deriemer S. A., Elliott E. J., Macagno E. R. Muller K. J. (1983) Morphological evidence that regenerating axons can fuse with severed axon segments. Brain Res. 272, 157 161.
25. Domeniconi M., Cao Z., Spencer T. et al. (2002) Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 35, 283 290.
26. Domeniconi M., Zampieri N., Spencer T., Hilaire M., Mellado W., Chao M. V. Filbin M. T. (2005) MAG induces regulated intramembrane proteolysis of the p75 neurotrophin receptor to inhibit neurite outgrowth. Neuron 46, 849 855.
27. Edgar J. M., McLaughlin M., Yool D. et al. (2004) Oligodendroglial modulation of fast axonal transport in a mouse model of hereditary spastic paraplegia. J. Cell Biol. 166, 121 131.
28. Ferri A., Sanes J. R., Coleman M. P., Cunningham J. M. Kato A. C. (2003) Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease. Curr. Biol. 13, 669 673.
29. Fischer L. R., Culver D. G., Tennant P., Davis A. A., Wang M., Castellano-Sanchez A., Khan J., Polak M. A. Glass J. D. (2004) Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol. 185, 232 240.
30. G93A fALS mouse. Neurobiol. Dis. 19, 293 300.
31. Fournier A. E., GrandPre T. Strittmatter S. M. (2001) Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409, 341 346.
32. Freeman M. R., Delrow J., Kim J., Johnson E. Doe C. Q. (2003) Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function. Neuron 38, 567 580.
33. Gabel C. V., Antonie F., Chuang C. F., Samuel A. D. Chang C. (2008) Distinct cellular and molecular mechanisms mediate initial axon development and adult-stage axon regeneration in C. elegans. Development 135, 1129 1136.
34. S mice after cortical lesion. Brain 129, 1546 1556.
35. Gould T. W., Buss R. R., Vinsant S., Prevette D., Sun W., Knudson C. M., Milligan C. E. Oppenheim R. W. (2006) Complete dissociation of motor neuron death from motor dysfunction by Bax deletion in a mouse model of ALS. J. Neurosci. 26, 8774 8786.
36. GrandPre T., Nakamura F., Vartanian T. Strittmatter S. M. (2000) Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature 403, 439 444.
37. Guo S. X., Bourgeois F., Chokshi T., Durr N. J., Hilliard M. A., Chronis N. Ben-Yakar A. (2008) Femtosecond laser nanoaxotomy lab-on-a-chip for in vivo nerve regeneration studies. Nat. Methods 5, 531 533.
38. Hammarlund M., Davis W. S. Jorgensen E. M. (2000) Mutations in β-spectrin disrupt axon outgrowth and sarcomere structure. J. Cell Biol. 149, 931 942.
39. Hammarlund M., Jorgensen E. M. Bastiani M. J. (2007) Axons break in animals lacking β-spectrin. J. Cell Biol. 176, 269 275.
40. Harel N. Y. Strittmatter S. M. (2006) Can regenerating axons recapitulate developmental guidance during recovery from spinal cord injury? Nat. Rev. Neurosci. 7, 603 616.
41. S protection distinguishes axon degeneration following injury from naturally occurring developmental pruning. Neuron 50, 883 895.
42. Hoy R. R., Bittner G. D. Kennedy D. (1967) Regeneration in crustacean motoneurons: evidence for axonal fusion. Science 156, 251 252.
43. Kage E., Hayashi Y., Takeuchi H., Hirotsu T., Kunitomo H., Inoue T., Arai H., Iino Y. Kubo T. (2005) MBR-1, a novel helix-turn-helix transcription factor, is required for pruning excessive neurites in Caenorhabditis elegans. Curr. Biol. 15, 1554 1559.
44. Kerschensteiner M., Schwab M. E., Lichtman J. W. Misgeld T. (2005) In vivo imaging of axonal degeneration and regeneration in the injured spinal cord. Nat. Med. 11, 572 577.
45. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., Yokochi M., Mizuno Y. Shimizu N. (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605 608.
46. Korhonen L. Lindholm D. (2004) The ubiquitin proteasome system in synaptic and axonal degeneration: a new twist to an old cycle. J. Cell Biol. 165, 27 30.
47. S, binds directly to VCP/p97 and partially redistributes it within the nucleus. Mol. Biol. Cell 17, 1075 1084.
48. Lee T., Lee A. Luo L. (1999) Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126, 4065 4076.
49. Liu Q. A. Hengartner M. O. (1998) Candidate adaptor protein CED-6 promotes the engulfment of apoptotic cells in C. elegans. Cell 93, 961 972.
50. Liu B. P., Fournier A., GrandPre T. Strittmatter S. M. (2002) Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science 297, 1190 1193.
51. Ludwin S. K. Bisby M. A. (1992) Delayed Wallerian degeneration in the central nervous system of Ola mice: an ultrastructural study. J. Neurol. Sci. 109, 140 147.
52. Lunn E. R., Perry V. H., Brown M. C., Rosen H. Gordon S. (1989) Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve. Eur. J. Neurosci. 1, 27 33.
53. Luo L. O'Leary D. D. (2005) Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 28, 127 156.
54. Lyon M. F., Ogunkolade B. W., Brown M. C., Atherton D. J. Perry V. H. (1993) A gene affecting Wallerian nerve degeneration maps distally on mouse chromosome 4. Proc. Natl Acad. Sci. USA 90, 9717 9720.
55. MacDonald J. M., Beach M. G., Porpiglia E., Sheehan A. E., Watts R. J. Freeman M. R. (2006) The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 50, 869 881.
56. Mack T. G., Reiner M., Beirowski B. et al. (2001) Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 4, 1199 1206.
57. McKerracher L., David S., Jackson D. L., Kottis V., Dunn R. J. Braun P. E. (1994) Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13, 805 811.
58. McQuarrie I. G. Grafstein B. (1973) Axon outgrowth enhanced by a previous nerve injury. Arch. Neurol. 29, 53 55.
59. Mi S., Lee X., Shao Z. et al. (2004) LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat. Neurosci. 7, 221 228.
60. S, inhibits axonal spheroid pathology in gracile axonal dystrophy mice. Brain 128, 405 416.
61. Moorthy S., Chen L. Bennett V. (2000) Caenorhabditis elegansβ-G spectrin is dispensable for establishment of epithelial polarity, but essential for muscular and neuronal function. J. Cell Biol. 149, 915 930.
62. Moreau-Fauvarque C., Kumanogoh A., Camand E. et al. (2003) The transmembrane semaphorin Sema4D/CD100, an inhibitor of axonal growth, is expressed on oligodendrocytes and upregulated after CNS lesion. J. Neurosci. 23, 9229 9239.
63. Mukhopadhyay G., Doherty P., Walsh F. S., Crocker P. R. Filbin M. T. (1994) A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13, 757 767.
64. Neumann S. Woolf C. J. (1999) Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23, 83 91.
65. Neumann S., Bradke F., Tessier-Lavigne M. Basbaum A. I. (2002) Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34, 885 893.
66. O'Leary D. D. Koester S. E. (1993) Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex. Neuron 10, 991 1006.
67. Park J. B., Yiu G., Kaneko S., Wang J., Chang J., He X. L., Garcia K. C. 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.
68. Prineas J. (1969) The pathogenesis of dying-back polyneuropathies. II. An ultrastructural study of experimental acrylamide intoxication in the cat. J. Neuropath. Exper. Neurol. 28, 598 621.
69. Prinjha R., Moore S. E., Vinson M., Blake S., Morrow R., Christie G., Michalovich D., Simmons D. L. Walsh F. S. (2000) Inhibitor of neurite outgrowth in humans. Nature 403, 383 384.
70. Raff M. C., Whitmore A. V. Finn J. T. (2002) Axonal self-destruction and neurodegeneration. Science 296, 868 871.
71. Rohde C. B., Zeng F., Gonzalez-Rubio R., Angel M. Yanik M. F. (2007) Microfluidic system for on-chip high-throughput whole-animal sorting and screening at subcellular resolution. Proc. Natl Acad. Sci. USA 104, 13891 13895.
72. Rubens O., Logina I., Kravale I., Eglite M. Donaghy M. (2001) Peripheral neuropathy in chronic occupational inorganic lead exposure: a clinical and electrophysiological study. J. Neurol. Neurosurg. Psychiatr. 71, 200 204.
73. Sagot Y., Dubois-Dauphin M., Tan S. A., de Bilbao F., Aebischer P., Martinou J. C. Kato A. C. (1995) Bcl-2 overexpression prevents motoneuron cell body loss but not axonal degeneration in a mouse model of a neurodegenerative disease. J. Neurosci. 15, 7727 7733.
74. Saigoh K., Wang Y. L., Suh J. G. et al. (1999) Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Nat. Genet. 23, 47 51.
75. S-mediated protection of dopaminergic fibers in an animal model of Parkinson disease. Curr. Biol. 14, 326 330.
76. S mutation delays robust loss of motor and sensory axons in a genetic model for myelin-related axonopathy. J. Neurosci. 23, 2833 2839.
77. Sasaki Y., Araki T. Milbrandt J. (2006) Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. J. Neurosci. 26, 8484 8491.
78. Schlaepfer W. W. (1971) Vincristine-induced axonal alterations in rat peripheral nerve. J. Neuropath. Exper. Neurol. 30, 488 505.
79. Schlamp C. L., Li Y., Dietz J. A., Janssen K. T. Nickells R. W. (2006) Progressive ganglion cell loss and optic nerve degeneration in DBA/2J mice is variable and asymmetric. BMC Neurosci. 7, 66.
80. Shao Z., Browning J. L., Lee X. et al. (2005) TAJ/TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron 45, 353 359.
81. Shimura H., Hattori N., Kubo S. et al. (2000) Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat. Genet. 25, 302 305.
82. Silva A., Wang Q., Wang M., Ravula S. K. Glass J. D. (2006) Evidence for direct axonal toxicity in vincristine neuropathy. J. Peripher. Nerv. Syst. 11, 211 216.
83. Silver J. Miller J. H. (2004) Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5, 146 156.
84. Spencer P. S. Schaumburg H. H. (1974) A review of acrylamide neurotoxicity. Part II. Experimental animal neurotoxicity and pathologic mechanisms. Can. J. Neurol. Sci. 1, 152 169.
85. Stokin G. B., Lillo C., Falzone T. L. et al. (2005) Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307, 1282 1288.
86. Trapp B. D., Peterson J., Ransohoff R. M., Rudick R., Mork S. Bo L. (1998) Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 338, 278 285.
87. S does not attenuate mutant SOD1-mediated motor neuron disease. Neuromol. Med. 5, 193 203.
88. Waller A. (1850) Experiments on the section of glossopharingeal and hypoglossal nerves of the frog and observations of the alternatives produced thereby in the structure of their primitive fibers. Phil. Trans. R. Soc. Lond. 140, 423 429.
89. Wang M. S., Wu Y., Culver D. G. Glass J. D. (2000) Pathogenesis of axonal degeneration: parallels between Wallerian degeneration and vincristine neuropathy. J. Neuropath. Exp. Neurol. 59, 599 606.
90. S) is also protective against vincristine neuropathy. Neurobiol. Dis. 8, 155 161.
91. S mice are resistant to paclitaxel (taxol) neuropathy. Ann. Neurol. 52, 442 447.
92. Wang K. C., Koprivica V., Kim J. A., Sivasankaran R., Guo Y., Neve R. L. He Z. (2002b) Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417, 941 944.
93. Wang K. C., Kim J. A., Sivasankaran R., Segal R. He Z. (2002c) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420, 74 78.
94. Wang J., Zhai Q., Chen Y., Lin E., Gu W., McBurney M. W. He Z. (2005) A local mechanism mediates NAD-dependent protection of axon degeneration. J. Cell Biol. 170, 349 355.
95. S expression and the independence of the activity of Nmnat1. Neurosci. Lett. 411, 228 232.
96. Watts R. J., Hoopfer E. D. Luo L. (2003) Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 38, 871 885.
97. S. Mol. Cell. Neurosci. 38, 325 340.
98. S) gene. Mol. Cell Proteomics 6, 1318 1330.
99. S). Genome Biol. 9, R101.
100. Wong S. T., Henley J. R., Kanning K. C., Huang K. H., Bothwell M. Poo M. M. (2002) A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat. Neurosci. 5, 1302 1308.
101. Wu Z., Ghosh-Roy A., Yanik M. F., Zhang J. Z., Jin Y. Chisholm A. D. (2007) Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching. Proc. Natl Acad. Sci. USA 104, 15132 15137.
102. Yamashita T., Higuchi H. Tohyama M. (2002) The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho. J. Cell Biol. 157, 565 570.
103. Yanik M. F., Cinar H., Cinar H. N., Chisholm A. D., Jin Y. Ben-Yakar A. (2004) Neurosurgery: functional regeneration after laser axotomy. Nature 432, 822.
104. Yanik M. F., Cinar H., Cinar H. N., Chisholm A., Jin Y. Yakar A. B. (2006) Nerve regeneration in Caenorhabditis elegans after femtosecond laser axotomy. IEEE J. Quantum Electron. 12, 1283 1291.
105. Yiu G. He Z. (2006) Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 7, 617 627.
106. Zhai Q., Wang J., Kim A., Liu Q., Watts R., Hoopfer E., Mitchison T., Luo L. He Z. (2003) Involvement of the ubiquitin-proteasome system in the early stages of Wallerian degeneration. Neuron 39, 217 225.
107. Zhou Z., Hartwieg E. Horvitz H. R. (2001) CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104, 43 56.