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Cited by 473Nerve injury and regenerationHereditary Neurological DisordersCell death mechanisms and regulation

Wallerian Degeneration, WldS, and Nmnat

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Coleman, Michael P., Freeman, Marc R.·2010·Annual Review of Neuroscience
DOI 10.1146/annurev-neuro-060909-153248PMC PMC5223592
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Abstract

Traditionally, researchers have believed that axons are highly dependent on their cell bodies for long-term survival. However, recent studies point to the existence of axon-autonomous mechanism(s) that regulate rapid axon degeneration after axotomy. Here, we review the cellular and molecular events that underlie this process, termed Wallerian degeneration. We describe the biphasic nature of axon degeneration after axotomy and our current understanding of how Wld S—an extraordinary protein formed by fusing a Ube4b sequence to Nmnat1—acts to protect severed axons. Interestingly, the neuroprotective effects of Wld S span all species tested, which suggests that there is an ancient, Wld S-sensitive axon destruction program. Recent studies with Wld S also reveal that Wallerian degeneration is genetically related to several dying back axonopathies, thus arguing that Wallerian degeneration can serve as a useful model to understand, and potentially treat, axon degeneration in diverse traumatic or disease contexts.

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  1. Adalbert R Gillingwater TH Haley JE Bridge K Beirowski B A rat model of slow Wallerian degeneration (WldS) with improved preservation of neuromuscular synapses Eur. J. Neurosci 2005 21 271 277 15654865
  2. Adalbert R Nogradi A Szabo A Coleman MP The slow Wallerian degeneration gene in vivo protects motor axons but not their cell bodies after avulsion and neonatal axotomy Eur. J. Neurosci 2006 24 2163 2168 17074042
  3. Alvarez S Moldovan M Krarup C Acute energy restriction triggers Wallerian degeneration in mouse Exp. Neurol 2008 212 166 178 18486130
  4. Araki T Sasaki Y Milbrandt J Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration Science 2004 305 1010 1013 15310905
  5. Avery MA Sheehan A Kerr KS Wang J Freeman MR WldS requires Nmnat1 enzymatic activity and N16-VCP interactions to suppress Wallerian degeneration J. Cell Biol 2009 184 501 513 19237597 PMC2654119
  6. Ayaz D Leyssen M Koch M Yan J Srahna M Axonal injury and regeneration in the adult brain of Drosophila J. Neurosci 2008 28 6010 6021 18524906 PMC2693324
  7. Beirowski B Adalbert R Wagner D Grumme D Addicks K The progressive nature of Wallerian degeneration in wild-type and slow Wallerian degeneration (WldS) nerves BMC Neurosci 2005 6 6 15686598 PMC549193
  8. Beirowski B Babetto E Coleman MP Martin KR The WldS gene delays axonal but not somatic degeneration in a rat glaucoma model Eur. J. Neurosci 2008 28 1166 1179 18783366
  9. Beirowski B Babetto E Gilley J Mazzola F Conforti L Non-nuclear Wld(S) determines its neuroprotective efficacy for axons and synapses in vivo J. Neurosci 2009 29 653 668 19158292 PMC6665162
  10. Benbassat D Spira ME The survival of transected axonal segments of cultured aplysia neurons is prolonged by contact with intact nerve cells Eur. J. Neurosci 1994 6 1605 1614 7850024
  11. Bishop DL Misgeld T Walsh MK Gan WB Lichtman JW Axon branch removal at developing synapses by axosome shedding Neuron 2004 44 651 661 15541313
  12. Braun RJ Zischka H Madeo F Eisenberg T Wissing S Crucial mitochondrial impairment upon CDC48 mutation in apoptotic yeast J. Biol. Chem 2006 281 25757 25767 16822868
  13. Brown MC Perry VH Hunt SP Lapper SR Further studies on motor and sensory nerve regeneration in mice with delayed Wallerian degeneration Eur. J. Neurosci 1994 6 420 428 8019679
  14. Buckmaster EA Perry VH Brown MC The rate of Wallerian degeneration in cultured neurons from wild type and C57BL/WldS mice depends on time in culture and may be extended in the presence of elevated K+ levels Eur. J. Neurosci 1995 7 1596 1602 7551186
  15. Burne JF Staple JK Raff MC Glial cells are increased proportionally in transgenic optic nerves with increased numbers of axons J. Neurosci 1996 16 2064 2073 8604051 PMC6578498
  16. Cajal SRy Degeneration and Regeneration of the Nervous System 1928 London Oxford Univ. Press
  17. Cavanagh JB The ‘dying back’ process. A common denominator in many naturally occurring and toxic neuropathies Arch. Pathol. Lab Med 1979 103 659 664 389195
  18. Chitnis T Imitola J Wang Y Elyaman W Chawla P Elevated neuronal expression of CD200. protects Wlds mice from inflammation-mediated neurodegeneration Am. J. Pathol 2007 170 1695 1712 17456775 PMC1854964
  19. Coleman MP Conforti L Buckmaster EA Tarlton A Ewing RM An 85-kb tandem triplication in the slow Wallerian degeneration (Wlds) mouse Proc. Natl. Acad. Sci. USA 1998 95 9985 9990 9707587 PMC21448
  20. Coleman MP Ribchester RR Programmed axon death, synaptic dysfunction and the ubiquitin proteasome system Curr. Drug Targets CNS Neurol. Disord 2004 3 227 238 15180483
  21. Conforti L A W Morreale G Janeckova L Beirowski B WldS protein requires Nmnat activity and a short N-terminal sequence to protect axons in mice J. Cell Biol 2009 184 491 500 19237596 PMC2654131
  22. Conforti L Adalbert R Coleman MP Neuronal death: Where does the end begin? Trends Neurosci 2007a 30 159 166 17339056
  23. Conforti L Fang G Beirowski B Wang MS Sorci L NAD(+) and axon degeneration revisited: Nmnat1 cannot substitute for Wld(S) to delay Wallerian degeneration Cell Death Differ 2007b 14 116 127 16645633
  24. Conforti L Tarlton A Mack TG Mi W Buckmaster EA A Ufd2/D4Cole1e chimeric protein and overexpression of rbp7 in the slow Wallerian degeneration (WldS) mouse Proc. Natl. Acad. Sci. USA 2000 97 11377 11382 11027338 PMC17208
  25. Court FA Hendriks WT Macgillavry HD Alvarez J van Minnen J Schwann cell to axon transfer of ribosomes: toward a novel understanding of the role of glia in the nervous system J. Neurosci 2008 28 11024 11029 18945910 PMC6671360
  26. De Vos KJ Grierson AJ Ackerley S Miller CC Role of axonal transport in neurodegenerative diseases Annu. Rev. Neurosci 2008 31 151 173 18558852
  27. Deckwerth TL Johnson EM Jr Neurites can remain viable after destruction of the neuronal soma by programmed cell death (apoptosis) Dev. Biol 1994 165 63 72 8088451
  28. Doherty J Logan MA Tasdemir OE Freeman MR Ensheathing glia function as phagocytes in the adult Drosophila brain J. Neurosci 2009 29 4768 4781 19369546 PMC2674269
  29. Ehlers MD Eppendorf 2003 prize-winning essay. Ubiquitin and the deconstruction of synapses Science 2003 302 800 801 14593160
  30. Fainzilber M Twiss JL Tracking in the Wld(s)—the hunting of the SIRT and the luring of the draper Neuron 2006 50 819 821 16772165
  31. Ferguson B Matyszak MK Esiri MM Perry VH Axonal damage in acute multiple sclerosis lesions Brain 1997 120 393 399 9126051
  32. Ferri A Sanes JR Coleman MP Cunningham JM Kato AC Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease Curr. Biol 2003 13 669 673 12699624
  33. Finn JT Weil M Archer F Siman R Srinivasan A Raff MC Evidence that wallerian degeneration and localized axon degeneration induced by local neurotrophin deprivation do not involve caspases J. Neurosci 2000 20 1333 1341 10662823 PMC6772375
  34. Fischer LR Culver DG Davis AA Tennant P Wang M The Wld(S) gene modestly prolongs survival in the SOD1(G93A) fALS mouse Neurobiol. Dis 2005 19 293 300 15837585
  35. Gamble HJ Jha BD Some effects of temperature upon the rate and progress of Wallerian degeneration in mammalian nerve fibers J. Anat 1958 92 171 177 13525232 PMC1249691
  36. Gilley J Coleman MP Endogenous Nmnat2 is an essential survival factor for maintenance of health axons PLoS Biol 2010 8 e1000200 PMC2811159 20126265
  37. Gillingwater TH Ingham CA Parry KE Wright AK Haley JE Delayed synaptic degeneration in the CNS of Wlds mice after cortical lesion Brain 2006a 129 1546 1556 16738060
  38. Gillingwater TH Thomson D Mack TG Soffin EM Mattison RJ Age-dependent synapse withdrawal at axotomised neuromuscular junctions in Wld(s) mutant and Ube4b/Nmnat transgenic mice J. Physiol 2002 543 739 755 12231635 PMC2290540
  39. Gillingwater TH Wishart TM Chen PE Haley JE Robertson K The neuroprotective WldS gene regulates expression of PTTG1 and erythroid differentiation regulator 1-like Gene in Mice and human cells Hum. Mol. Genet 2006b 15 625 635 16403805
  40. Glass JD Brushart TM George EB Griffin JW Prolonged survival of transected nerve fibres in C57BL/Ola mice is an intrinsic characteristic of the axon J. Neurocytol 1993 22 311 321 8315413
  41. Griffin JW George EB Chaudhry V Wallerian degeneration in peripheral nerve disease Baillieres Clin. Neurol 1996 5 65 75 8732200
  42. Guo SX Bourgeois F Chokshi T Durr NJ Hilliard MA Femtosecond laser nanoaxotomy labon-a-chip for in vivo nerve regeneration studies Nat. Methods 2008 5 531 533 18408725 PMC3143684
  43. Hammarlund M Jorgensen EM Bastiani MJ Axons break in animals lacking beta-spectrin J. Cell Biol 2007 176 269 275 17261846 PMC2063953
  44. Hammarlund M Nix P Hauth L Jorgensen EM Bastiani M Axon regeneration requires a conserved MAP kinase pathway Science 2009 323 802 806 19164707 PMC2729122
  45. Hasbani DM O’Malley KL Wld(S) mice are protected against the Parkinsonian mimetic MPTP Exp. Neurol 2006 202 93 99 16806180
  46. Hassa PO Haenni SS Elser M Hottiger MO Nuclear ADP-ribosylation reactions in mammalian cells: Where are we today and where are we going? Microbiol. Mol. Biol. Rev 2006 70 789 829 16959969 PMC1594587
  47. Hatakeyama S Yada M Matsumoto M Ishida N Nakayama KI U-Box proteins as a new family of ubiquitin-protein ligases J. Biol. Chem 2001 276 33111 33120 11435423
  48. Hoopfer ED McLaughlin T Watts RJ Schuldiner O O’Leary DD Luo L Wld(s) protection distinguishes axon degeneration following injury from naturally occurring developmental pruning Neuron 2006 50 883 895 16772170
  49. Howell GR Libby RT Jakobs TC Smith RS Phalan FC Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma J. Cell Biol 2007 179 1523 1537 18158332 PMC2373494
  50. Jia H Yan T Feng Y Zeng C Shi X Zhai Q Identification of a critical site in Wld(s): essential for Nmnat enzyme activity and axon-protective function Neurosci. Lett 2007 413 46 51 17207927
  51. Kane RC Bross PF Farrell AT Pazdur R Velcade: U.S. FDA approval for the treatment of multiple myeloma progressing on prior therapy Oncologist 2003 8 508 513 14657528
  52. Kaneko S Wang J Kaneko M Yiu G Hurrell JM Protecting axonal degeneration by increasing nicotinamide adenine dinucleotide levels in experimental autoimmune encephalomyelitis models J. Neurosci 2006 26 9794 9804 16988050 PMC6674451
  53. Kaneko-Oshikawa C Nakagawa T Yamada M Yoshikawa H Matsumoto M Mammalian E4 is required for cardiac development and maintenance of the nervous system Mol. Cell Biol 2005 25 10953 10964 16314518 PMC1316961
  54. Kariya S Mauricio R Dai Y Monani UR The neuroprotective factor Wld(s) fails to mitigate distal axonal and neuromuscular junction (NMJ) defects in mouse models of spinal muscular atrophy Neurosci. Lett 2009 449 246 251 19010394 PMC2671206
  55. Keilhoff G Fansa H Wolf G Differences in peripheral nerve degeneration/regeneration between wild-type and neuronal nitric oxide synthase knockout mice J. Neurosci. Res 2002 68 432 441 11992469
  56. Kerschensteiner M Schwab ME Lichtman JW Misgeld T In vivo imaging of axonal degeneration and regeneration in the injured spinal cord Nat. Med 2005 11 572 577 15821747
  57. Koegl M Hoppe T Schlenker S Ulrich HD Mayer TU Jentsch S A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly Cell 1999 96 635 644 10089879
  58. Laser H Conforti L Morreale G Mack TG Heyer M The slow Wallerian degeneration protein, WldS, binds directly to VCP/p97 and partially redistributes it within the nucleus Mol. Biol. Cell 2006 17 1075 1084 16371511 PMC1382299
  59. Laser H Mack TG Wagner D Coleman MP Proteasome inhibition arrests neurite outgrowth and causes “dying-back” degeneration in primary culture J. Neurosci. Res 2003 74 906 916 14648596
  60. Levy D Kubes P Zochodne DW Delayed peripheral nerve degeneration, regeneration, and pain in mice lacking inducible nitric oxide synthase J. Neuropathol. Exp. Neurol 2001 60 411 421 11379816
  61. Libby RT Li Y Savinova OV Barter J Smith RS Susceptibility to neurodegeneration in glaucoma is modified by Bax gene dosage PLoS Genet 2005 1 e4 PMC1183523 16103918
  62. Lopez-Vales R Navarro X Shimizu T Baskakis C Kokotos G Intracellular phospholipase A(2) group IVA and group VIA play important roles in Wallerian degeneration and axon regeneration after peripheral nerve injury Brain 2008 131 2620 2631 18718965 PMC2860706
  63. Lubinska L Early course of Wallerian degeneration in myelinated fibres of the rat phrenic nerve Brain Res 1977 130 47 63 884520
  64. Lubinska L Patterns of Wallerian degeneration of myelinated fibres in short and long peripheral stumps and in isolated segments of rat phrenic nerve. Interpretation of the role of axoplasmic flow of the trophic factor Brain Res 1982 233 227 240 6174177
  65. Lunn ER Perry VH Brown MC Rosen H Gordon S Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve Eur. J. Neurosci 1989 1 27 33 12106171
  66. Lyon MF Ogunkolade BW Brown MC Atherton DJ Perry VH A gene affecting Wallerian nerve degeneration maps distally on mouse chromosome 4 Proc. Natl. Acad. Sci. USA 1993 90 9717 9720 8415768 PMC47641
  67. Macdonald JM Beach MG Porpiglia E Sheehan AE Watts RJ Freeman MR The Drosophila cell corpse engulfment receptor draper mediates glial clearance of severed axons Neuron 2006 50 869 881 16772169
  68. Macinnis BL Campenot RB Regulation of Wallerian degeneration and nerve growth factor withdrawal-induced pruning of axons of sympathetic neurons by the proteasome and the MEK/Erk pathway Mol. Cell Neurosci 2005 28 430 439 15737734
  69. Mack TG Reiner M Beirowski B Mi W Emanuelli M Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene Nat. Neurosci 2001 4 1199 1206 11770485
  70. Magni G Amici A Emanuelli M Orsomando G Raffaelli N Ruggieri S Structure and function of nicotinamide mononucleotide adenylyltransferase Curr. Med. Chem 2004 11 873 885 15078171
  71. Merianda TT Lin AC Lam JS Vuppalanchi D Willis DE A functional equivalent of endoplasmic reticulum and Golgi in axons for secretion of locally synthesized proteins Mol. Cell Neurosci 2009 40 128 142 19022387 PMC3794446
  72. Merkwirth C Langer T Mitofusin 2 builds a bridge between ER and mitochondria Cell 2008 135 1165 1167 19109886
  73. Mi W Beirowski B Gillingwater TH Adalbert R Wagner D The slow Wallerian degeneration gene, WldS, inhibits axonal spheroid pathology in gracile axonal dystrophy mice Brain 2005 128 405 416 15644421
  74. Miledi R Slater CR On the degeneration of rat neuromuscular junctions after nerve section J. Physiol 1970 207 507 528 5499034 PMC1348721
  75. Miller BR Press C Daniels RW Sasaki Y Milbrandt J DiAntonio A A dual leucine kinase-dependent axon self-destruction program promotes Wallerian degeneration Nat. Neurosci 2009 12 387 389 19287387 PMC2696160
  76. Misgeld T Kerschensteiner M Bareyre FM Burgess RW Lichtman JW Imaging axonal transport of mitochondria in vivo Nat. Methods 2007 4 559 561 17558414
  77. Moldovan M Alvarez S Krarup C Motor axon excitability during Wallerian degeneration Brain 2009 132 511 523 19074190
  78. Morreale G Conforti L Coadwell J Wilbrey AL Coleman MP Evolutionary divergence of valosin-containing protein/cell division cycle protein 48 binding interactions among endoplasmic reticulum-associated degradation proteins FEBS J 2009 276 1208 1220 19175675
  79. Narciso MS Mietto Bde S Marques SA Soares CP Mermelstein Cdos S Sciatic nerve regeneration is accelerated in galectin-3 knockout mice Exp. Neurol 2009 217 7 15 19416680
  80. Nave KA Trapp BD Axon-glial signaling and the glial support of axon function Annu. Rev. Neurosci 2008 31 535 561 18558866
  81. Neumann H Medana IM Bauer J Lassmann H Cytotoxic T lymphocytes in autoimmune and degenerative CNS diseases Trends Neurosci 2002 25 313 319 12086750
  82. Nikolaev A McLaughlin T O’Leary DD Tessier-Lavigne M APP binds DR6 to trigger axon pruning and neuron death via distinct caspases Nature 2009 457 981 989 19225519 PMC2677572
  83. Nordlander RH Singer M Electron microscopy of severed motor fibers in the crayfish Z. Zellforsch. Mikrosk. Anat 1972 126 157 181 4336217
  84. Parnas I Dudel J Atwood HL Synaptic transmission in decentralized axons of rock lobster J. Neurosci 1991 11 1309 1315 1851218 PMC6575305
  85. Parson SH Mackintosh CL Ribchester RR Elimination of motor nerve terminals in neonatal mice expressing a gene for slow Wallerian degeneration (C57Bl/Wlds) Eur. J. Neurosci 1997 9 1586 1592 9283813
  86. Perlson E Hanz S Ben-Yaakov K Segal-Ruder Y Seger R Fainzilber M Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve Neuron 2005 45 715 726 15748847
  87. Perry VH Brown MC Lunn ER Very slow retrograde and Wallerian degeneration in the CNS of C57BL/Ola mice Eur. J. Neurosci 1991 3 102 105 12106273
  88. Perry VH Brown MC Lunn ER Tree P Gordon S Evidence that very slow Wallerian degeneration in C57BL/Ola mice is an intrinsic property of the peripheral nerve Eur. J. Neurosci 1990a 2 802 808 12106282
  89. Perry VH Lunn ER Brown MC Cahusac S Gordon S Evidence that the rate of Wallerian degeneration is controlled by a single autosomal dominant gene Eur. J. Neurosci 1990b 2 408 413 12106028
  90. Pollak N Dolle C Ziegler M The power to reduce: pyridine nucleotides–small molecules with a multitude of functions Biochem. J 2007 402 205 218 17295611 PMC1798440
  91. Raff MC Whitmore AV Finn JT Axonal self-destruction and neurodegeneration Science 2002 296 868 871 11988563
  92. Raffaelli N Sorci L Amici A Emanuelli M Mazzola F Magni G Identification of a novel human nicotinamide mononucleotide adenylyltransferase Biochem. Biophys. Res. Commun 2002 297 835 840 12359228
  93. Ramaglia V King RH Nourallah M Wolterman R de Jonge R The membrane attack complex of the complement system is essential for rapid Wallerian degeneration J. Neurosci 2007 27 7663 7672 17634361 PMC6672891
  94. Ribchester RR Tsao JW Barry JA Asgari-Jirhandeh N Perry VH Brown MC Persistence of neuromuscular junctions after axotomy in mice with slow Wallerian degeneration (C57BL/WldS) Eur. J. Neurosci 1995 7 1641 1650 7551190
  95. Rose FF Jr Meehan PW Coady TH Garcia VB Garcia ML Lorson CL The Wallerian degeneration slow (Wld(s)) gene does not attenuate disease in a mouse model of spinal muscular atrophy Biochem. Biophys. Res. Commun 2008 375 119 123 18680723 PMC2603628
  96. Sagot Y Dubois-Dauphin M Tan SA de Bilbao F Aebischer P Bcl-2 overexpression prevents motoneuron cell body loss but not axonal degeneration in a mouse model of a neurodegenerative disease J. Neurosci 1995 15 7727 7733 7472523 PMC6578059
  97. Saigoh K Wang YL Suh JG Yamanishi T Sakai Y Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice Nat. Genet 1999 23 47 51 10471497
  98. Sajadi A Schneider BL Aebischer P Wld(s)-mediated protection of dopaminergic fibers in an animal model of parkinson disease Curr. Biol 2004 14 326 330 14972684
  99. Samsam M Mi W Wessig C Zielasek J Toyka KV The Wlds mutation delays robust loss of motor and sensory axons in a genetic model for myelin-related axonopathy J. Neurosci 2003 23 2833 2839 12684470 PMC6742108
  100. Sasaki Y Vohra BP Baloh RH Milbrandt J Transgenic mice expressing theNmnat1 protein manifest robust delay in axonal degeneration in vivo J. Neurosci 2009a 29 6526 6534 19458223 PMC2697066
  101. Sasaki Y Vohra BP Lund FE Milbrandt J Nicotinamide mononucleotide adenylyl transferase-mediated axonal protection requires enzymatic activity but not increased levels of neuronal nicotinamide adenine dinucleotide J. Neurosci 2009b 29 5525 5535 19403820 PMC3162248
  102. Schlaepfer WW Effects of energy deprivation on Wallerian degeneration in isolated segments of rat peripheral nerve Brain Res 1974 78 71 81 4458917
  103. Simonin Y Perrin FE Kato AC Axonal involvement in the Wlds neuroprotective effect: analysis of pure motoneurons in a mouse model protected from motor neuron disease at a presymptomatic age J. Neurochem 2007 101 530 542 17402973
  104. Sorci L Cimadamore F Scotti S Petrelli R Cappellacci L Initial-rate kinetics of human NMN-adenylyltransferases: substrate and metal ion specificity, inhibition by products and multisubstrate analogues, and isozyme contributions to NAD+ biosynthesis Biochemistry 2007 46 4912 4922 17402747
  105. Tamsett TJ Picchione KE Bhattacharjee A NAD+ activates KNa channels in dorsal root ganglion neurons J. Neurosci 2009 29 5127 5134 19386908 PMC6665483
  106. Todisco S Agrimi G Castegna A Palmieri F Identification of the mitochondrial NAD+ transporter in Saccharomyces cerevisiae J. Biol. Chem 2006 281 1524 1531 16291748
  107. Vargas ME Barres BA Why is Wallerian degeneration in the CNS so slow? Annu. Rev. Neurosci 2007 30 153 179 17506644
  108. Velde CV Garcia ML Yin X Trapp BD Cleveland DW The neuroprotective factor Wlds does not attenuate mutant SOD1-mediated motor neuron disease Neuromolecular Med 2004 5 193 204 15626820
  109. Waller A Experiments on the section of glossopharyngeal and hypoglossal nerves of the frog and observations of the alternatives produced thereby in the structure of their primitive fibres Philos. Trans. R. Soc. Lond. B Biol. Sci 1850 140 423 429
  110. Wang J Zhai Q Chen Y Lin E Gu W A local mechanism mediates NAD-dependent protection of axon degeneration J. Cell Biol 2005 170 349 355 16043516 PMC2171458
  111. Wang MS Davis AA Culver DG Glass JD WldS mice are resistant to paclitaxel (taxol) neuropathy Ann. Neurol 2002 52 442 447 12325073
  112. Wang MS Fang G Culver DG Davis AA Rich MM Glass JD The WldS protein protects against axonal degeneration: a model of gene therapy for peripheral neuropathy Ann. Neurol 2001 50 773 779 11761475
  113. Wang MS Wu Y Culver DG Glass JD Pathogenesis of axonal degeneration: parallels between Wallerian degeneration and vincristine neuropathy J. Neuropathol. Exp. Neurol 2000 59 599 606 10901231
  114. Wang Q Song C Li CC Molecular perspectives on p97-VCP: progress in understanding its structure and diverse biological functions J. Struct. Biol 2004 146 44 57 15037236
  115. Whitmore AV Lindsten T Raff MC Thompson CB The proapoptotic proteins Bax and Bak are not involved in Wallerian degeneration Cell Death Differ 2003 10 260 261 12700655
  116. Wilbrey AL Haley JE Wishart TM Conforti L Morreale G VCP binding influences intracellular distribution of the slow Wallerian degeneration protein, Wld(S) Mol. Cell Neurosci 2008 38 325 340 18468455
  117. Wishart TM Paterson JM Short DM Meredith S Robertson KA Differential proteomic analysis of synaptic proteins identifies potential cellular targets and protein mediators of synaptic neuroprotection conferred by the slow Wallerian degeneration (Wlds) gene Mol. Cell Proteomics 2007 6 8 1318 1330 17470424 PMC2225590
  118. Wishart TM Pemberton HN James SR McCabe CJ Gillingwater TH Modified cell cycle status in a mouse model of altered neuronal vulnerability (slow Wallerian degeneration; Wlds) Genome Biol 2008 9 R101 18570652 PMC2481432
  119. Wong F Fan L Wells S Hartley R Mackenzie FE Axonal and neuromuscular synaptic phenotypes in WldS, SOD1(G93A) and ostes mutant mice identified by fiber-optic confocal microendoscopy Mol. Cell Neurosci 2009 42 296 307 19683573
  120. Wu Z Ghosh-Roy A Yanik MF Zhang JZ Jin Y Chisholm AD Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching Proc. Natl. Acad. Sci. USA 2007 104 15132 15137 17848506 PMC1975853
  121. Zhai Q Wang J Kim A Liu Q Watts R Involvement of the ubiquitin-proteasome system in the early stages of wallerian degeneration Neuron 2003 39 217 225 12873380
  122. Zhai RG Cao Y Hiesinger PR Zhou Y Mehta SQ Drosophila NMNAT maintains neural integrity independent of its NAD synthesis activity PLoS Biol 2006 4 e416 17132048 PMC1665629
  123. Zhai RG Zhang F Hiesinger PR Cao Y Haueter CM Bellen HJ NAD synthase NMNAT acts as a chaperone to protect against neurodegeneration Nature 2008 452 887 891 18344983 PMC3150538
  124. Zottoli SJ Marek LE Agostini MA Strittmatter SL Morphological and physiological survival of goldfish Mauthner axons isolated from their somata by spinal cord crush J. Comp. Neurol 1987 255 272 282 3819017

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Authors
Coleman, M. P., & Freeman, M. R.
Affiliations
  • Babraham Institute (GB)
  • Howard Hughes Medical Institute (US)
ORCID
Coleman, Michael P.
Venue
Annual Review of Neuroscience
Publisher
Annual Reviews
Published
2010-06-01
Volume
33
Issue
1
Pages
245-267
ISSN
  • 0147-006X (ISSN-L)
  • 1545-4126
DOI
10.1146/annurev-neuro-060909-153248
PMC
PMC5223592
OpenAlex
W2118145481
Cited by
473
References
9
Citations by year
2026: 11 · 2025: 16 · 2024: 20 · 2023: 15 · 2022: 30 · 2021: 20 · 2020: 39 · 2019: 30 · 2018: 36 · 2017: 28 · 2016: 30 · 2015: 28 · 2014: 44 · 2013: 39 · 2012: 51
FWCI
3.63
Type
journal article
Language
en
Open access
Locations
  • Annual Review of Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship@UMassChan (submittedVersion)
Funders
  • Howard Hughes Medical Institute
  • Biotechnology and Biological Sciences Research Council
  • National Institute of Neurological Disorders and Stroke (R01NS059991, NS059991)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Hereditary Neurological Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Keywords
Wallerian degeneration, NMNAT1, axonal degeneration, axotomy, UBE4B, axon survival, neuroprotection, axonopathy
MeSH terms
Animals, Axons, Humans, Nerve Tissue Proteins, Nicotinamide-Nucleotide Adenylyltransferase, Wallerian Degeneration, Axotomy, Ubiquitin-Protein Ligases, Gene Fusion

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