Axon Self-Destruction: New Links among SARM1, MAPKs, and NAD+ Metabolism

Neuron

Volumn 89, Issue 3, 2016, Pages 449-460

  Gerdts, Josiah ^a   Summers, Daniel W ^a   Milbrandt, Jeffrey ^a   DiAntonio, Aaron ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE NUCLEOTIDE ADENYLYLTRANSFERASE; NICOTINAMIDE NUCLEOTIDE ADENYLYLTRANSFERASE 1; PROTEIN SARM1; UNCLASSIFIED DRUG; ARMADILLO DOMAIN PROTEIN; CYTOSKELETON PROTEIN; NEUROPROTECTIVE AGENT; NMNAT2 PROTEIN, MOUSE; SARM1 PROTEIN, MOUSE;

AXOPLASM; BINDING AFFINITY; CELL DEATH; CELL LOSS; CELL PROLIFERATION; CELL SURVIVAL; ENERGY METABOLISM; ENZYME ACTIVITY; ENZYME METABOLISM; HUMAN; NERVE CELL NECROSIS; NERVE FIBER DEGENERATION; NERVE FIBER REGENERATION; NEUROPATHY; NONHUMAN; PALMITOYLATION; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; REVIEW; SYNAPSE; TRAUMATIC BRAIN INJURY; ANIMAL; AXON; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; WALLERIAN DEGENERATION;

ANIMALS; ARMADILLO DOMAIN PROTEINS; AXONS; CYTOSKELETAL PROTEINS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; NAD; NEUROPROTECTIVE AGENTS; NICOTINAMIDE-NUCLEOTIDE ADENYLYLTRANSFERASE; SIGNAL TRANSDUCTION; WALLERIAN DEGENERATION;

EID: 84959314882     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.12.023     Document Type: Review

References (108)

1. Akhouayri I., Turc C., Royet J., Charroux B. Toll-8/Tollo negatively regulates antimicrobial response in the Drosophila respiratory epithelium. PLoS Pathog. 2011, 7:e1002319.
2. Aksoy P., White T.A., Thompson M., Chini E.N. Regulation of intracellular levels of NAD: a novel role for CD38. Biochem. Biophys. Res. Commun. 2006, 345:1386-1392.
3. Alano C.C., Garnier P., Ying W., Higashi Y., Kauppinen T.M., Swanson R.A. NAD+ depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J. Neurosci. 2010, 30:2967-2978.
4. Albers J.W., Pop-Busui R. Diabetic neuropathy: mechanisms, emerging treatments, and subtypes. Curr. Neurol. Neurosci. Rep. 2014, 14:473.
5. Andrabi S.A., Dawson T.M., Dawson V.L. Mitochondrial and nuclear cross talk in cell death: parthanatos. Ann. N Y Acad. Sci. 2008, 1147:233-241.
6. Araki T., Sasaki Y., Milbrandt J. Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 2004, 305:1010-1013.
7. Avery M.A., Sheehan A.E., Kerr K.S., Wang J., Freeman M.R. Wld S requires Nmnat1 enzymatic activity and N16-VCP interactions to suppress Wallerian degeneration. J. Cell Biol. 2009, 184:501-513.
8. Babetto E., Beirowski B., Janeckova L., Brown R., Gilley J., Thomson D., Ribchester R.R., Coleman M.P. Targeting NMNAT1 to axons and synapses transforms its neuroprotective potency in vivo. J. Neurosci. 2010, 30:13291-13304.
9. Babetto E., Beirowski B., Russler E.V., Milbrandt J., DiAntonio A. The Phr1 ubiquitin ligase promotes injury-induced axon self-destruction. Cell Rep. 2013, 3:1422-1429.
10. Barrientos S.A., Martinez N.W., Yoo S., Jara J.S., Zamorano S., Hetz C., Twiss J.L., Alvarez J., Court F.A. Axonal degeneration is mediated by the mitochondrial permeability transition pore. J. Neurosci. 2011, 31:966-978.
11. S gene delays axonal but not somatic degeneration in a rat glaucoma model. Eur. J. Neurosci. 2008, 28:1166-1179.
12. Belenky P., Bogan K.L., Brenner C. NAD+ metabolism in health and disease. Trends Biochem. Sci. 2007, 32:12-19.
13. Benarroch E.E. Acquired axonal degeneration and regeneration: Recent insights and clinical correlations. Neurology 2015, 84:2076-2085.
14. Bennett B.L., Sasaki D.T., Murray B.W., O'Leary E.C., Sakata S.T., Xu W., Leisten J.C., Motiwala A., Pierce S., Satoh Y., et al. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. U S A 2001, 98:13681-13686.
15. Berger N.A. Poly(ADP-ribose) in the cellular response to DNA damage. Radiat. Res. 1985, 101:4-15.
16. Bhattacharya M.R.C., Gerdts J., Naylor S.A., Royse E.X., Ebstein S.Y., Sasaki Y., Milbrandt J., DiAntonio A. A model of toxic neuropathy in Drosophila reveals a role for MORN4 in promoting axonal degeneration. J. Neurosci. 2012, 32:5054-5061.
17. Blum E.S., Abraham M.C., Yoshimura S., Lu Y., Shaham S. Control of nonapoptotic developmental cell death in Caenorhabditis elegans by a polyglutamine-repeat protein. Science 2012, 335:970-973.
18. Bounoutas A., Kratz J., Emtage L., Ma C., Nguyen K.C., Chalfie M. Microtubule depolymerization in Caenorhabditis elegans touch receptor neurons reduces gene expression through a p38 MAPK pathway. Proc. Natl. Acad. Sci. U S A 2011, 108:3982-3987.
19. Brace E.J., Wu C., Valakh V., DiAntonio A. SkpA restrains synaptic terminal growth during development and promotes axonal degeneration following injury. J. Neurosci. 2014, 34:8398-8410.
20. Burke R.E., O'Malley K. Axon degeneration in Parkinson's disease. Exp. Neurol. 2013, 246:72-83.
21. Carty M., Goodbody R., Schröder M., Stack J., Moynagh P.N., Bowie A.G. The human adaptor SARM negatively regulates adaptor protein TRIF-dependent Toll-like receptor signaling. Nat. Immunol. 2006, 7:1074-1081.
22. Cashman C.R., Höke A. Mechanisms of distal axonal degeneration in peripheral neuropathies. Neurosci. Lett. 2015, 596:33-50.
23. Chen C.-Y., Lin C.-W., Chang C.-Y., Jiang S.-T., Hsueh Y.-P. Sarm1, a negative regulator of innate immunity, interacts with syndecan-2 and regulates neuronal morphology. J. Cell Biol. 2011, 193:769-784.
24. Chiarugi A., Dölle C., Felici R., Ziegler M. The NAD metabolome--a key determinant of cancer cell biology. Nat. Rev. Cancer 2012, 12:741-752.
25. Chuang C.F., Bargmann C.I. A Toll-interleukin 1 repeat protein at the synapse specifies asymmetric odorant receptor expression via ASK1 MAPKKK signaling. Genes Dev. 2005, 19:270-281.
26. Coleman M. Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 2005, 6:889-898.
27. Collins C.A., Wairkar Y.P., Johnson S.L., DiAntonio A. Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron 2006, 51:57-69.
28. Conforti L., Tarlton A., Mack T.G., Mi W., Buckmaster E.A., Wagner D., Perry V.H., Coleman M.P. A Ufd2/D4Cole1e chimeric protein and overexpression of Rbp7 in the slow Wallerian degeneration (WldS) mouse. Proc. Natl. Acad. Sci. U S A 2000, 97:11377-11382.
29. Couillault C., Pujol N., Reboul J., Sabatier L., Guichou J.-F., Kohara Y., Ewbank J.J. TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat. Immunol. 2004, 5:488-494.
30. Di Stefano M., Nascimento-Ferreira I., Orsomando G., Mori V., Gilley J., Brown R., Janeckova L., Vargas M.E., Worrell L.A., Loreto A., et al. A rise in NAD precursor nicotinamide mononucleotide (NMN) after injury promotes axon degeneration. Cell Death Differ. 2015, 22:731-742.
31. Ferri A., Sanes J.R., Coleman M.P., Cunningham J.M., Kato A.C. Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease. Curr. Biol. 2003, 13:669-673.
32. Fu D., Jordan J.J., Samson L.D. Human ALKBH7 is required for alkylation and oxidation-induced programmed necrosis. Genes Dev. 2013, 27:1089-1100.
33. Gerdts J., Summers D.W., Sasaki Y., DiAntonio A., Milbrandt J. Sarm1-mediated axon degeneration requires both SAM and TIR interactions. J. Neurosci. 2013, 33:13569-13580.
34. + destruction. Science 2015, 348:453-457.
35. Gilley J., Coleman M.P. Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol. 2010, 8:e1000300.
36. Gilley J., Adalbert R., Yu G., Coleman M.P. Rescue of peripheral and CNS axon defects in mice lacking NMNAT2. J. Neurosci. 2013, 33:13410-13424.
37. Gilley J., Orsomando G., Nascimento-Ferreira I., Coleman M.P. Absence of SARM1 rescues development and survival of NMNAT2-deficient axons. Cell Rep. 2015, 10:1974-1981.
38. Gossmann T.I., Ziegler M., Puntervoll P., de Figueiredo L.F., Schuster S., Heiland I. NAD(+) biosynthesis and salvage--a phylogenetic perspective. FEBS J. 2012, 279:3355-3363.
39. Grisold W., Cavaletti G., Windebank A.J. Peripheral neuropathies from chemotherapeutics and targeted agents: diagnosis, treatment, and prevention. Neuro-oncol. 2012, 14(Suppl 4):iv45-iv54.
40. Hammarlund M., Nix P., Hauth L., Jorgensen E.M., Bastiani M. Axon regeneration requires a conserved MAP kinase pathway. Science 2009, 323:802-806.
41. Hasbani D.M., O'Malley K.L. Wld(S) mice are protected against the Parkinsonian mimetic MPTP. Exp. Neurol. 2006, 202:93-99.
42. Hayakawa T., Kato K., Hayakawa R., Hisamoto N., Matsumoto K., Takeda K., Ichijo H. Regulation of anoxic death in Caenorhabditis elegans by mammalian apoptosis signal-regulating kinase (ASK) family proteins. Genetics 2011, 187:785-792.
43. Hoopfer E.D., McLaughlin T., Watts R.J., Schuldiner O., O'Leary D.D.M., Luo L. Wlds protection distinguishes axon degeneration following injury from naturally occurring developmental pruning. Neuron 2006, 50:883-895.
44. Huntwork-Rodriguez S., Wang B., Watkins T., Ghosh A.S., Pozniak C.D., Bustos D., Newton K., Kirkpatrick D.S., Lewcock J.W. JNK-mediated phosphorylation of DLK suppresses its ubiquitination to promote neuronal apoptosis. J. Cell Biol. 2013, 202:747-763.
45. Johnson V.E., Stewart W., Smith D.H. Axonal pathology in traumatic brain injury. Exp. Neurol. 2013, 246:35-43.
46. Kang J.Y., Lee J.-O. Structural biology of the Toll-like receptor family. Annu. Rev. Biochem. 2011, 80:917-941.
47. Kim Y., Zhou P., Qian L., Chuang J.-Z., Lee J., Li C., Iadecola C., Nathan C., Ding A. MyD88-5 links mitochondria, microtubules, and JNK3 in neurons and regulates neuronal survival. J. Exp. Med. 2007, 204:2063-2074.
48. Kroemer G., Galluzzi L., Vandenabeele P., Abrams J., Alnemri E.S., Baehrecke E.H., Blagosklonny M.V., El-Deiry W.S., Golstein P., Green D.R., et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009, 16:3-11. Nomenclature Committee on Cell Death 2009.
49. Kurant E. Keeping the CNS clear: glial phagocytic functions in Drosophila. Glia 2011, 59:1304-1311.
50. Leppä S., Bohmann D. Diverse functions of JNK signaling and c-Jun in stress response and apoptosis. Oncogene 1999, 18:6158-6162.
51. Liberati N.T., Fitzgerald K.A., Kim D.H., Feinbaum R., Golenbock D.T., Ausubel F.M. Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc. Natl. Acad. Sci. U S A 2004, 101:6593-6598.
52. Lunn E.R., Perry V.H., Brown M.C., Rosen H., Gordon S. Absence of Wallerian Degeneration does not Hinder Regeneration in Peripheral Nerve. Eur. J. Neurosci. 1989, 1:27-33.
53. Luo L., O'Leary D.D.M. Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 2005, 28:127-156.
54. MacDonald J.M., Beach M.G., Porpiglia E., Sheehan A.E., Watts R.J., Freeman M.R. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 2006, 50:869-881.
55. Mack T.G., Reiner M., Beirowski B., Mi W., Emanuelli M., Wagner D., Thomson D., Gillingwater T., Court F., Conforti L., et al. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 2001, 4:1199-1206.
56. Marcette J.D., Chen J.J., Nonet M.L. The Caenorhabditis elegans microtubule minus-end binding homolog PTRN-1 stabilizes synapses and neurites. eLife 2014, 3:e01637.
57. McLennan A.G. The Nudix hydrolase superfamily. Cell. Mol. Life Sci. 2006, 63:123-143.
58. Mi W., Beirowski B., Gillingwater T.H., Adalbert R., Wagner D., Grumme D., Osaka H., Conforti L., Arnhold S., Addicks K., et al. The slow Wallerian degeneration gene, WldS, inhibits axonal spheroid pathology in gracile axonal dystrophy mice. Brain 2005, 128:405-416.
59. Milde S., Gilley J., Coleman M.P. Axonal trafficking of NMNAT2 and its roles in axon growth and survival in vivo. BioArchitecture 2013, 3:133-140.
60. Miller B.R., Press C., Daniels R.W., Sasaki Y., Milbrandt J., DiAntonio A. A dual leucine kinase-dependent axon self-destruction program promotes Wallerian degeneration. Nat. Neurosci. 2009, 12:387-389.
61. Mishra B., Carson R., Hume R.I., Collins C.A. Sodium and potassium currents influence Wallerian degeneration of injured Drosophila axons. J. Neurosci. 2013, 33:18728-18739.
62. Mukherjee P., Woods T.A., Moore R.A., Peterson K.E. Activation of the innate signaling molecule MAVS by bunyavirus infection upregulates the adaptor protein SARM1, leading to neuronal death. Immunity 2013, 38:705-716.
63. Nakata K., Abrams B., Grill B., Goncharov A., Huang X., Chisholm A.D., Jin Y. Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 2005, 120:407-420.
64. Nikolaev A., McLaughlin T., O'Leary D.D.M., Tessier-Lavigne M. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 2009, 457:981-989.
65. Osterloh J.M., Yang J., Rooney T.M., Fox A.N., Adalbert R., Powell E.H., Sheehan A.E., Avery M.A., Hackett R., Logan M.A., et al. dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science 2012, 337:481-484.
66. Panneerselvam P., Singh L.P., Ho B., Chen J., Ding J.L. Targeting of pro-apoptotic TLR adaptor SARM to mitochondria: definition of the critical region and residues in the signal sequence. Biochem. J. 2012, 442:263-271.
67. Panneerselvam P., Singh L.P., Selvarajan V., Chng W.J., Ng S.B., Tan N.S., Ho B., Chen J., Ding J.L. T-cell death following immune activation is mediated by mitochondria-localized SARM. Cell Death Differ. 2013, 20:478-489.
68. Patel S., Cohen F., Dean B.J., De La Torre K., Deshmukh G., Estrada A.A., Ghosh A.S., Gibbons P., Gustafson A., Huestis M.P., et al. Discovery of dual leucine zipper kinase (DLK, MAP3K12) inhibitors with activity in neurodegeneration models. J. Med. Chem. 2015, 58:401-418.
69. Pease S.E., Segal R.A. Preserve and protect: maintaining axons within functional circuits. Trends Neurosci. 2014, 37:572-582.
70. Qiao F., Bowie J.U. The many faces of SAM. Sci. STKE 2005, 2005:re7.
71. Rudhard Y., Sengupta Ghosh A., Lippert B., Böcker A., Pedaran M., Krämer J., Ngu H., Foreman O., Liu Y., Lewcock J.W. Identification of 12/15-lipoxygenase as a regulator of axon degeneration through high-content screening. J. Neurosci. 2015, 35:2927-2941.
72. Sajadi A., Schneider B.L., Aebischer P. Wlds-mediated protection of dopaminergic fibers in an animal model of Parkinson disease. Curr. Biol. 2004, 14:326-330.
73. Sasaki Y., Milbrandt J. Axonal degeneration is blocked by nicotinamide mononucleotide adenylyltransferase (Nmnat) protein transduction into transected axons. J. Biol. Chem. 2010, 285:41211-41215.
74. Sasaki Y., Araki T., Milbrandt J. Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. J. Neurosci. 2006, 26:8484-8491.
75. Sasaki Y., Vohra B.P.S., Baloh R.H., Milbrandt J. Transgenic mice expressing the Nmnat1 protein manifest robust delay in axonal degeneration in vivo. J. Neurosci. 2009, 29:6526-6534.
76. Sasaki Y., Vohra B.P.S., Lund F.E., Milbrandt J. Nicotinamide mononucleotide adenylyl transferase-mediated axonal protection requires enzymatic activity but not increased levels of neuronal nicotinamide adenine dinucleotide. J. Neurosci. 2009, 29:5525-5535.
77. Schoenmann Z., Assa-Kunik E., Tiomny S., Minis A., Haklai-Topper L., Arama E., Yaron A. Axonal degeneration is regulated by the apoptotic machinery or a NAD+-sensitive pathway in insects and mammals. J. Neurosci. 2010, 30:6375-6386.
78. Schuldiner O., Yaron A. Mechanisms of developmental neurite pruning. Cell. Mol. Life Sci. 2015, 72:101-119.
79. Shin J.E., Miller B.R., Babetto E., Cho Y., Sasaki Y., Qayum S., Russler E.V., Cavalli V., Milbrandt J., DiAntonio A. SCG10 is a JNK target in the axonal degeneration pathway. Proc. Natl. Acad. Sci. U S A 2012, 109:E3696-E3705.
80. Shin J.E., Cho Y., Beirowski B., Milbrandt J., Cavalli V., DiAntonio A. Dual leucine zipper kinase is required for retrograde injury signaling and axonal regeneration. Neuron 2012, 74:1015-1022.
81. Shin J.E., Geisler S., DiAntonio A. Dynamic regulation of SCG10 in regenerating axons after injury. Exp. Neurol. 2014, 252:1-11.
82. Summers D.W., DiAntonio A., Milbrandt J. Mitochondrial dysfunction induces Sarm1-dependent cell death in sensory neurons. J. Neurosci. 2014, 34:9338-9350.
83. Tsao J.W., Brown M.C., Carden M.J., McLean W.G., Perry V.H. Loss of the compound action potential: an electrophysiological, biochemical and morphological study of early events in axonal degeneration in the C57BL/Ola mouse. Eur. J. Neurosci. 1994, 6:516-524.
84. Valakh V., Walker L.J., Skeath J.B., DiAntonio A. Loss of the spectraplakin short stop activates the DLK injury response pathway in Drosophila. J. Neurosci. 2013, 33:17863-17873.
85. Valakh V., Frey E., Babetto E., Walker L.J., DiAntonio A. Cytoskeletal disruption activates the DLK/JNK pathway, which promotes axonal regeneration and mimics a preconditioning injury. Neurobiol. Dis. 2015, 77:13-25.
86. Vanden Berghe T., Linkermann A., Jouan-Lanhouet S., Walczak H., Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat. Rev. Mol. Cell Biol. 2014, 15:135-147.
87. Vérièpe J., Fossouo L., Parker J.A. Neurodegeneration in C. elegans models of ALS requires TIR-1/Sarm1 immune pathway activation in neurons. Nat. Commun. 2015, 6:7319.
88. Vohra B.P.S., Sasaki Y., Miller B.R., Chang J., DiAntonio A., Milbrandt J. Amyloid precursor protein cleavage-dependent and -independent axonal degeneration programs share a common nicotinamide mononucleotide adenylyltransferase 1-sensitive pathway. J. Neurosci. 2010, 30:13729-13738.
89. Wakatsuki S., Saitoh F., Araki T. ZNRF1 promotes Wallerian degeneration by degrading AKT to induce GSK3B-dependent CRMP2 phosphorylation. Nat. Cell Biol. 2011, 13:1415-1423.
90. Waller A. Experiments on the Section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibres. Philos. Trans. R. Soc. Lond. 1850, 140:423-429.
91. Wang M.S., Davis A.A., Culver D.G., Glass J.D. WldS mice are resistant to paclitaxel (taxol) neuropathy. Ann. Neurol. 2002, 52:442-447.
92. Wang J., Zhai Q., Chen Y., Lin E., Gu W., McBurney M.W., He Z. A local mechanism mediates NAD-dependent protection of axon degeneration. J. Cell Biol. 2005, 170:349-355.
93. Wang J.T., Medress Z.A., Barres B.A. Axon degeneration: molecular mechanisms of a self-destruction pathway. J. Cell Biol. 2012, 196:7-18.
94. Wang G., Han T., Nijhawan D., Theodoropoulos P., Naidoo J., Yadavalli S., Mirzaei H., Pieper A.A., Ready J.M., McKnight S.L. P7C3 neuroprotective chemicals function by activating the rate-limiting enzyme in NAD salvage. Cell 2014, 158:1324-1334.
95. Wang J.T., Medress Z.A., Vargas M.E., Barres B.A. Local axonal protection by WldS as revealed by conditional regulation of protein stability. Proc. Natl. Acad. Sci. U S A 2015, 112:10093-10100.
96. Wishart T.M., Rooney T.M., Lamont D.J., Wright A.K., Morton A.J., Jackson M., Freeman M.R., Gillingwater T.H. Combining comparative proteomics and molecular genetics uncovers regulators of synaptic and axonal stability and degeneration in vivo. PLoS Genet. 2012, 8:e1002936.
97. Xiong X., Wang X., Ewanek R., Bhat P., Diantonio A., Collins C.A. Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury. J. Cell Biol. 2010, 191:211-223.
98. Xiong X., Hao Y., Sun K., Li J., Li X., Mishra B., Soppina P., Wu C., Hume R.I., Collins C.A. The Highwire ubiquitin ligase promotes axonal degeneration by tuning levels of Nmnat protein. PLoS Biol. 2012, 10:e1001440.
99. Yahata N., Yuasa S., Araki T. Nicotinamide mononucleotide adenylyltransferase expression in mitochondrial matrix delays Wallerian degeneration. J. Neurosci. 2009, 29:6276-6284.
100. Yan D., Jin Y. Regulation of DLK-1 kinase activity by calcium-mediated dissociation from an inhibitory isoform. Neuron 2012, 76:534-548.
101. Yan D., Wu Z., Chisholm A.D., Jin Y. The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration. Cell 2009, 138:1005-1018.
102. Yan T., Feng Y., Zheng J., Ge X., Zhang Y., Wu D., Zhao J., Zhai Q. Nmnat2 delays axon degeneration in superior cervical ganglia dependent on its NAD synthesis activity. Neurochem. Int. 2010, 56:101-106.
103. Yang J., Weimer R.M., Kallop D., Olsen O., Wu Z., Renier N., Uryu K., Tessier-Lavigne M. Regulation of axon degeneration after injury and in development by the endogenous calpain inhibitor calpastatin. Neuron 2013, 80:1175-1189.
104. Yang J., Wu Z., Renier N., Simon D.J., Uryu K., Park D.S., Greer P.A., Tournier C., Davis R.J., Tessier-Lavigne M. Pathological axonal death through a MAPK cascade that triggers a local energy deficit. Cell 2015, 160:161-176.
105. Yuan J. Neuroprotective strategies targeting apoptotic and necrotic cell death for stroke. Apoptosis 2009, 14:469-477.
106. Yuan J., Yankner B.A. Apoptosis in the nervous system. Nature 2000, 407:802-809.
107. Zhai R.G., Zhang F., Hiesinger P.R., Cao Y., Haueter C.M., Bellen H.J. NAD synthase NMNAT acts as a chaperone to protect against neurodegeneration. Nature 2008, 452:887-891.
108. Zhang Q., Zmasek C.M., Cai X., Godzik A. TIR domain-containing adaptor SARM is a late addition to the ongoing microbe-host dialog. Dev. Comp. Immunol. 2011, 35:461-468.