Molecular chaperones protect against JNK- and Nmnat-regulated axon degeneration in Drosophila

Journal of Cell Science

Volumn 126, Issue 3, 2013, Pages 838-849

  Rallis, Andrew ^a,b,c   Lu, Bingwei ^b   Ng, Julian ^a,d  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CENTRE DE BIOCHIMIE   (France)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Axon degeneration; Drosophila; Heat shock proteins; JNK; Nmnat

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 26; HEAT SHOCK PROTEIN 70; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE MONONUCLEOTIDE ADENYLYLTRANSFERASE 1; NICOTINAMIDE NUCLEOTIDE ADENYLYLTRANSFERASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVITY; ENZYME INACTIVATION; NERVE DEGENERATION; NERVE FIBER DEGENERATION; NERVE FIBER TRANSECTION; NEUROPROTECTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPPRESSOR GENE;

ADP RIBOSE TRANSFERASES; ANIMALS; AXONS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HEAT-SHOCK PROTEINS; HSP72 HEAT-SHOCK PROTEINS; MAP KINASE KINASE 4; MOLECULAR CHAPERONES; MUSHROOM BODIES; NERVE TISSUE PROTEINS; NICOTINAMIDE-NUCLEOTIDE ADENYLYLTRANSFERASE; SIGNAL TRANSDUCTION; WALLERIAN DEGENERATION;

BASIDIOMYCOTA; WALLERIA;

EID: 84876340896     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.117259     Document Type: Article

References (135)

1. Abou-Sleiman, P. M., Muqit, M. M. and Wood, N. W. (2006). Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat. Rev. Neurosci. 7, 207-219.
2. Ali, Y. O., Ruan, K. and Zhai, R. G. (2012). NMNAT suppresses tau-induced neurodegeneration by promoting clearance of hyperphosphorylated tau oligomers in a Drosophila model of tauopathy. Hum. Mol. Genet. 21, 237-250.
3. Araki, T., Sasaki, Y. and Milbrandt, J. (2004). Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305, 1010-1013.
4. Auluck, P. K., Chan, H. Y., Trojanowski, J. Q., Lee, V. M. and Bonini, N. M. (2002). Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295, 865-868.
5. Avery, M. A., Sheehan, A. E., Kerr, K. S., Wang, J. and Freeman, M. R. (2009). Wld S requires Nmnat1 enzymatic activity and N16-VCP interactions to suppress Wallerian degeneration. J. Cell Biol. 184, 501-513.
6. Avery, M. A., Rooney, T. M., Pandya, J. D., Wishart, T. M., Gillingwater, T. H., Geddes, J. W., Sullivan, P. G. and Freeman, M. R. (2012). WldS prevents axon degeneration through increased mitochondrial flux and enhanced mitochondrial Ca2+ buffering. Curr. Biol. 22, 596-600.
7. Ayaz, D., Leyssen, M., Koch, M., Yan, J., Srahna, M., Sheeba, V., Fogle, K. J., Holmes, T. C. and Hassan, B. A. (2008). Axonal injury and regeneration in the adult brain of Drosophila. J. Neurosci. 28, 6010-6021.
8. Babetto, E., Beirowski, B., Janeckova, L., Brown, R., Gilley, J., Thomson, D., Ribchester, R. R. and Coleman, M. P. (2010). Targeting NMNAT1 to axons and synapses transforms its neuroprotective potency in vivo. J. Neurosci. 30, 13291-13304.
9. Barnat, M., Enslen, H., Propst, F., Davis, R. J., Soares, S. and Nothias, F. (2010). Distinct roles of c-Jun N-terminal kinase isoforms in neurite initiation and elongation during axonal regeneration. J. Neurosci. 30, 7804-7816.
10. Barrientos, S. A., Martinez, N. W., Yoo, S., Jara, J. S., Zamorano, S., Hetz, C., Twiss, J. L., Alvarez, J. and Court, F. A. (2011). Axonal degeneration is mediated by the mitochondrial permeability transition pore. J. Neurosci. 31, 966-978.
11. Beirowski, B., Babetto, E., Coleman, M. P. and Martin, K. R. (2008). The WldS gene delays axonal but not somatic degeneration in a rat glaucoma model. Eur. J. Neurosci. 28, 1166-1179.
12. Beirowski, B., Babetto, E., Gilley, J., Mazzola, F., Conforti, L., Janeckova, L., Magni, G., Ribchester, R. R. and Coleman, M. P. (2009). Non-nuclear Wld(S) determines its neuroprotective efficacy for axons and synapses in vivo. J. Neurosci. 29, 653-668.
13. Beirowski, B., Morreale, G., Conforti, L., Mazzola, F., Di Stefano, M., Wilbrey, A., Babetto, E., Janeckova, L., Magni, G. and Coleman, M. P. (2010). WldS can delay Wallerian degeneration in mice when interaction with valosin-containing protein is weakened. Neuroscience 166, 201-211.
14. Berger, F., Lau, C., Dahlmann, M. and Ziegler, M. (2005). Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. J. Biol. Chem. 280, 36334-36341.
15. Berger, F., Lau, C. and Ziegler, M. (2007). Regulation of poly(ADP-ribose) polymerase 1 activity by the phosphorylation state of the nuclear NAD biosynthetic enzyme NMN adenylyl transferase 1. Proc. Natl. Acad. Sci. USA 104, 3765-3770.
16. Bhattacharya, M. R., Gerdts, J., Naylor, S. A., Royse, E. X., Ebstein, S. Y., Sasaki, Y., Milbrandt, J. and DiAntonio, A. (2012). A model of toxic neuropathy in Drosophila reveals a role for MORN4 in promoting axonal degeneration. J. Neurosci. 32, 5054-5061.
17. Billuart, P., Winter, C. G., Maresh, A., Zhao, X. and Luo, L. (2001). Regulating axon branch stability: the role of p190 RhoGAP in repressing a retraction signaling pathway. Cell 107, 195-207.
18. Bingol, B. and Sheng, M. (2011). Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease. Neuron 69, 22-32.
19. Brecht, S., Kirchhof, R., Chromik, A., Willesen, M., Nicolaus, T., Raivich, G., Wessig, J., Waetzig, V., Goetz, M., Claussen, M. et al. (2005). Specific pathophysiological functions of JNK isoforms in the brain. Eur. J. Neurosci. 21, 363-377.
20. Chang, L., Jones, Y., Ellisman, M. H., Goldstein, L. S. and Karin, M. (2003). JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev. Cell 4, 521-533.
21. Cherbas, L., Hu, X., Zhimulev, I., Belyaeva, E. and Cherbas, P. (2003). EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development 130, 271-284.
22. Chiang, P. W., Wang, J., Chen, Y., Fu, Q., Zhong, J., Chen, Y., Yi, X., Wu, R., Gan, H., Shi, Y. et al. (2012). Exome sequencing identifies NMNAT1 mutations as a cause of Leber congenital amaurosis. Nat. Genet. 44, 972-974.
23. Coleman, M. (2005). Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 6, 889-898.
24. Coleman, M. P. and Freeman, M. R. (2010). Wallerian degeneration, wld(s), and nmnat. Annu. Rev. Neurosci. 33, 245-267.
25. Conforti, L., Tarlton, A., Mack, T. G., Mi, W., Buckmaster, E. A., Wagner, D., Perry, V. H. and Coleman, M. P. (2000). A Ufd2/D4Cole1e chimeric protein and overexpression of Rbp7 in the slow Wallerian degeneration (WldS) mouse. Proc. Natl. Acad. Sci. USA 97, 11377-11382.
26. Conforti, L., Fang, G., Beirowski, B., Wang, M. S., Sorci, L., Asress, S., Adalbert, R., Silva, A., Bridge, K., Huang, X. P. et al. (2007). NAD(+) and axon degeneration revisited: Nmnat1 cannot substitute for Wld(S) to delay Wallerian degeneration. Cell Death Differ. 14, 116-127.
27. Conforti, L., Wilbrey, A., Morreale, G., Janeckova, L., Beirowski, B., Adalbert, R., Mazzola, F., Di Stefano, M., Hartley, R., Babetto, E. et al. (2009). Wld S protein requires Nmnat activity and a short N-terminal sequence to protect axons in mice. J. Cell Biol. 184, 491-500.
28. Cummings, C. J., Mancini, M. A., Antalffy, B., DeFranco, D. B., Orr, H. T. and Zoghbi, H. Y. (1998). Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat. Genet. 19, 148-154.
29. Cummings, C. J., Sun, Y., Opal, P., Antalffy, B., Mestril, R., Orr, H. T., Dillmann, W. H. and Zoghbi, H. Y. (2001). Over-expression of inducible HSP70 chaperone suppresses neuropathology and improves motor function in SCA1 mice. Hum. Mol. Genet. 10, 1511-1518.
30. Dawes-Hoang, R. E., Parmar, K. M., Christiansen, A. E., Phelps, C. B., Brand, A. H. and Wieschaus, E. F. (2005). folded gastrulation, cell shape change and the control of myosin localization. Development 132, 4165-4178.
31. DiAntonio, A., Haghighi, A. P., Portman, S. L., Lee, J. D., Amaranto, A. M. and Goodman, C. S. (2001). Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412, 449-452.
32. Eilers, A., Whitfield, J., Babij, C., Rubin, L. L. and Ham, J. (1998). Role of the Jun kinase pathway in the regulation of c-Jun expression and apoptosis in sympathetic neurons. J. Neurosci. 18, 1713-1724.
33. Falk, M. J., Zhang, Q., Nakamaru-Ogiso, E., Kannabiran, C., Fonseca-Kelly, Z., Chakarova, C., Audo, I., Mackay, D. S., Zeitz, C., Borman, A. D. et al. (2012). NMNAT1 mutations cause Leber congenital amaurosis. Nat. Genet. 44, 1040-1045.
34. Fang, Y., Soares, L., Teng, X., Geary, M. and Bonini, N. M. (2012). A novel Drosophila model of nerve injury reveals an essential role of Nmnat in maintaining axonal integrity. Curr. Biol. 22, 590-595.
35. Farrer, M. J. (2006). Genetics of Parkinson disease: paradigm shifts and future prospects. Nat. Rev. Genet. 7, 306-318.
36. Feng, Y., Yan, T., Zheng, J., Ge, X., Mu, Y., Zhang, Y., Wu, D., Du, J. L. and Zhai, Q. (2010). Overexpression of Wld(S) or Nmnat2 in mauthner cells by single-cell electroporation delays axon degeneration in live zebrafish. J. Neurosci. Res. 88, 3319-3327.
37. Ferri, A., Sanes, J. R., Coleman, M. P., Cunningham, J. M. and 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.
38. Finn, J. T., Weil, M., Archer, F., Siman, R., Srinivasan, A. and Raff, M. C. (2000). Evidence that Wallerian degeneration and localized axon degeneration induced by local neurotrophin deprivation do not involve caspases. J. Neurosci. 20, 1333-1341.
39. Fonte, V., Kipp, D. R., Yerg, J., 3rd, Merin, D., Forrestal, M., Wagner, E., Roberts, C. M. and Link, C. D. (2008). Suppression of in vivo beta-amyloid peptide toxicity by overexpression of the HSP-16.2 small chaperone protein. J. Biol. Chem. 283, 784-791. Gallo, G. (2004). Myosin II activity is required for severing-induced axon retraction in vitro. Exp. Neurol. 189, 112-121.
40. Gallo, G. (2004). Myosin II activity is required for severing-induced axon retraction in vitro. Exp. Neurol. 189, 112-121.
41. Gallo, G. (2006). RhoA-kinase coordinates F-actin organization and myosin II activity during semaphorin-3A-induced axon retraction. J. Cell Sci. 119, 3413-3423.
42. Ghosh, S. and Feany, M. B. (2004). Comparison of pathways controlling toxicity in the eye and brain in Drosophila models of human neurodegenerative diseases. Hum. Mol. Genet. 13, 2011-2018.
43. Ghosh, A. S., Wang, B., Pozniak, C. D., Chen, M., Watts, R. J. and Lewcock, J. W. (2011). DLK induces developmental neuronal degeneration via selective regulation of proapoptotic JNK activity. J. Cell Biol. 194, 751-764.
44. Gifondorwa, D. J., Robinson, M. B., Hayes, C. D., Taylor, A. R., Prevette, D. M., Oppenheim, R. W., Caress, J. and Milligan, C. E. (2007). Exogenous delivery of heat shock protein 70 increases lifespan in a mouse model of amyotrophic lateral sclerosis. J. Neurosci. 27, 13173-13180.
45. Gilley, J. and Coleman, M. P. (2010). Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol. 8, e1000300.
46. Glise, B., Bourbon, H. and Noselli, S. (1995). hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 83, 451-461.
47. Greene, J. C., Whitworth, A. J., Kuo, I., Andrews, L. A., Feany, M. B. and Pallanck, L. J. (2003). Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc. Natl. Acad. Sci. USA 100, 4078-4083.
48. Hasbani, D. M. and O'Malley, K. L. (2006). Wld(S) mice are protected against the Parkinsonian mimetic MPTP. Exp. Neurol. 202, 93-99.
49. Hawkins, C. J., Yoo, S. J., Peterson, E. P., Wang, S. L., Vernooy, S. Y. and Hay, B. A. (2000). The Drosophila caspase DRONC cleaves following glutamate or aspartate and is regulated by DIAP1, HID, and GRIM. J. Biol. Chem. 275, 27084-27093.
50. Hay, B. A., Wassarman, D. A. and Rubin, G. M. (1995). Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83, 1253-1262.
51. Hennig, K. M. and Neufeld, T. P. (2002). Inhibition of cellular growth and proliferation by dTOR overexpression in Drosophila. Genesis 34, 107-110.
52. Herdegen, T., Claret, F. X., Kallunki, T., Martin-Villalba, A., Winter, C., Hunter, T. and Karin, M. (1998). Lasting N-terminal phosphorylation of c-Jun and activation of c-Jun N-terminal kinases after neuronal injury. J. Neurosci. 18, 5124-5135.
53. Hicks, A. N., Lorenzetti, D., Gilley, J., Lu, B., Andersson, K. E., Miligan, C., Overbeek, P. A., Oppenheim, R. and Bishop, C. E. (2012). Nicotinamide mononucleotide adenylyltransferase 2 (Nmnat2) regulates axon integrity in the mouse embryo. PLoS ONE 7, e47869.
54. Hoopfer, E. D., McLaughlin, T., Watts, R. J., Schuldiner, O., O'Leary, D. D. and Luo, L. (2006). Wlds protection distinguishes axon degeneration following injury from naturally occurring developmental pruning. Neuron 50, 883-895.
55. Howell, G. R., Libby, R. T., Jakobs, T. C., Smith, R. S., Phalan, F. C., Barter, J. W., Barbay, J. M., Marchant, J. K., Mahesh, N., Porciatti, V. et al. (2007). Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J. Cell Biol. 179, 1523-1537.
56. Imai, Y., Gehrke, S., Wang, H. Q., Takahashi, R., Hasegawa, K., Oota, E. and Lu, B. (2008). Phosphorylation of 4E-BP by LRRK2 affects the maintenance of dopaminergic neurons in Drosophila. EMBO J. 27, 2432-2443.
57. Kaneko, S., Wang, J., Kaneko, M., Yiu, G., Hurrell, J. M., Chitnis, T., Khoury, S. J. and He, Z. (2006). Protecting axonal degeneration by increasing nicotinamide adenine dinucleotide levels in experimental autoimmune encephalomyelitis models. J. Neurosci. 26, 9794-9804.
58. Khandelwal, P. J., Herman, A. M., Hoe, H. S., Rebeck, G. W. and Moussa, C. E. (2011). Parkin mediates beclin-dependent autophagic clearance of defective mitochondria and ubiquitinated Abeta in AD models. Hum. Mol. Genet. 20, 2091-2102.
59. Koenekoop, R. K., Wang, H., Majewski, J., Wang, X., Lopez, I., Ren, H., Chen, Y., Li, Y., Fishman, G. A., Genead, M. et al.; Finding of Rare Disease Genes (FORGE) Canada Consortium (2012). Mutations in NMNAT1 cause Leber congenital amaurosis and identify a new disease pathway for retinal degeneration. Nat. Genet. 44, 1035-1039.
60. Kuan, C. Y., Whitmarsh, A. J., Yang, D. D., Liao, G., Schloemer, A. J., Dong, C., Bao, J., Banasiak, K. J., Haddad, G. G., Flavell, R. A. et al. (2003). A critical role of neural-specific JNK3 for ischemic apoptosis. Proc. Natl. Acad. Sci. USA 100, 15184-15189.
61. Kuo, C. T., Zhu, S., Younger, S., Jan, L. Y. and Jan, Y. N. (2006). Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51, 283-290.
62. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.
63. Lee, T., Marticke, S., Sung, C., Robinow, S. and Luo, L. (2000). Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 28, 807-818.
64. Lee, J. Y., Koga, H., Kawaguchi, Y., Tang, W., Wong, E., Gao, Y. S., Pandey, U. B., Kaushik, S., Tresse, E., Lu, J. et al. (2010). HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J. 29, 969-980.
65. Leyssen, M., Ayaz, D., Hébert, S. S., Reeve, S., De Strooper, B. and Hassan, B. A. (2005). Amyloid precursor protein promotes post-developmental neurite arborization in the Drosophila brain. EMBO J. 24, 2944-2955.
66. Lin, M. T. and Beal, M. F. (2006). Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787-795.
67. Lin, H., Kwan, A. L. and Dutcher, S. K. (2010). Synthesizing and salvaging NAD: lessons learned from Chlamydomonas reinhardtii. PLoS Genet. 6, e1001105.
68. Liu, S. and Lu, B. (2010). Reduction of protein translation and activation of autophagy protect against PINK1 pathogenesis in Drosophila melanogaster. PLoS Genet. 6, e1001237.
69. Lunn, E. R., Perry, V. H., Brown, M. C., Rosen, H. and Gordon, S. (1989). Absence of Wallerian Degeneration does not Hinder Regeneration in Peripheral Nerve. Eur. J. Neurosci. 1, 27-33.
70. Luo, L. and O'Leary, D. D. (2005). Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 28, 127-156.
71. Ma, C. H., Omura, T., Cobos, E. J., Latrémolière, A., Ghasemlou, N., Brenner, G. J., van Veen, E., Barrett, L., Sawada, T., Gao, F. et al. (2011). Accelerating axonal growth promotes motor recovery after peripheral nerve injury in mice. J. Clin. Invest. 121, 4332-4347.
72. Mack, T. G., Reiner, M., Beirowski, B., Mi, W., Emanuelli, M., Wagner, D., Thomson, D., Gillingwater, T., Court, F., Conforti, L. et al. (2001). Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 4, 1199-1206.
73. Magrané, J., Smith, R. C., Walsh, K. and Querfurth, H. W. (2004). Heat shock protein 70 participates in the neuroprotective response to intracellularly expressed beta-amyloid in neurons. J. Neurosci. 24, 1700-1706.
74. Maroney, A. C., Glicksman, M. A., Basma, A. N., Walton, K. M., Knight, E., Jr, Murphy, C. A., Bartlett, B. A., Finn, J. P., Angeles, T., Matsuda, Y. et al. (1998). Motoneuron apoptosis is blocked by CEP-1347 (KT 7515), a novel inhibitor of the JNK signaling pathway. J. Neurosci. 18, 104-111.
75. McGuire, S. E., Le, P. T., Osborn, A. J., Matsumoto, K. and Davis, R. L. (2003). Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302, 1765-1768.
76. Meier, P., Silke, J., Leevers, S. J. and Evan, G. I. (2000). The Drosophila caspase DRONC is regulated by DIAP1. EMBO J. 19, 598-611.
77. Mi, W., Beirowski, B., Gillingwater, T. H., Adalbert, R., Wagner, D., Grumme, D., Osaka, H., Conforti, L., Arnhold, S., Addicks, K. et al. (2005). The slow Wallerian degeneration gene, WldS, inhibits axonal spheroid pathology in gracile axonal dystrophy mice. Brain 128, 405-416.
78. Miller, B. R., Press, C., Daniels, R. W., Sasaki, Y., Milbrandt, J. and DiAntonio, A. (2009). A dual leucine kinase-dependent axon self-destruction program promotes Wallerian degeneration. Nat. Neurosci. 12, 387-389.
79. Miron, M., Verdú, J., Lachance, P. E., Birnbaum, M. J., Lasko, P. F. and Sonenberg, N. (2001). The translational inhibitor 4E-BP is an effector of PI(3)K/Akt signalling and cell growth in Drosophila. Nat. Cell Biol. 3, 596-601.
80. Morfini, G. A., You, Y. M., Pollema, S. L., Kaminska, A., Liu, K., Yoshioka, K., Björkblom, B., Coffey, E. T., Bagnato, C., Han, D. et al. (2009). Pathogenic huntingtin inhibits fast axonal transport by activating JNK3 and phosphorylating kinesin. Nat. Neurosci. 12, 864-871.
81. Morishima, Y., Gotoh, Y., Zieg, J., Barrett, T., Takano, H., Flavell, R., Davis, R. J., Shirasaki, Y. and Greenberg, M. E. (2001). Beta-amyloid induces neuronal apoptosis via a mechanism that involves the c-Jun N-terminal kinase pathway and the induction of Fas ligand. J. Neurosci. 21, 7551-7560.
82. Muro, I., Hay, B. A. and Clem, R. J. (2002). The Drosophila DIAP1 protein is required to prevent accumulation of a continuously generated, processed form of the apical caspase DRONC. J. Biol. Chem. 277, 49644-49650.
83. Narendra, D. P. and Youle, R. J. (2011). Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control. Antioxid. Redox Signal. 14, 1929-1938.
84. Narendra, D. P., Jin, S. M., Tanaka, A., Suen, D. F., Gautier, C. A., Shen, J., Cookson, M. R. and Youle, R. J. (2010). PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 8, e1000298.
85. Nikolaev, A., McLaughlin, T., O'Leary, D. D. and Tessier-Lavigne, M. (2009). APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457, 981-989.
86. Nix, P., Hisamoto, N., Matsumoto, K. and Bastiani, M. (2011). Axon regeneration requires coordinate activation of p38 and JNK MAPK pathways. Proc. Natl. Acad. Sci. USA 108, 10738-10743.
87. Okazawa, H. and Estus, S. (2002). The JNK/c-Jun cascade and Alzheimer's disease. Am. J. Alzheimers Dis. Other Demen. 17, 79-88.
88. Oliva, A. A., Jr, Atkins, C. M., Copenagle, L. and Banker, G. A. (2006). Activated c-Jun N-terminal kinase is required for axon formation. J. Neurosci. 26, 9462-9470.
89. Pandey, U. B., Nie, Z., Batlevi, Y., McCray, B. A., Ritson, G. P., Nedelsky, N. B., Schwartz, S. L., DiProspero, N. A., Knight, M. A., Schuldiner, O. et al. (2007). HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447, 859-863.
90. Park, J., Lee, S. B., Lee, S., Kim, Y., Song, S., Kim, S., Bae, E., Kim, J., Shong, M., Kim, J. M. et al. (2006). Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441, 1157-1161.
91. Peng, J. and Andersen, J. K. (2003). The role of c-Jun N-terminal kinase (JNK) in Parkinson's disease. IUBMB Life 55, 267-271.
92. Perrault, I., Hanein, S., Zanlonghi, X., Serre, V., Nicouleau, M., Defoort-Delhemmes, S., Delphin, N., Fares-Taie, L., Gerber, S., Xerri, O. et al. (2012). Mutations in NMNAT1 cause Leber congenital amaurosis with early-onset severe macular and optic atrophy. Nat. Genet. 44, 975-977.
93. Perrin, V., Dufour, N., Raoul, C., Hassig, R., Brouillet, E., Aebischer, P., Luthi-Carter, R. and Déglon, N. (2009). Implication of the JNK pathway in a rat model of Huntington's disease. Exp. Neurol. 215, 191-200.
94. Pun, S., Santos, A. F., Saxena, S., Xu, L. and Caroni, P. (2006). Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat. Neurosci. 9, 408-419.
95. Quinn, L., Coombe, M., Mills, K., Daish, T., Colussi, P., Kumar, S. and Richardson, H. (2003). Buffy, a Drosophila Bcl-2 protein, has anti-apoptotic and cell cycle inhibitory functions. EMBO J. 22, 3568-3579.
96. Raivich, G., Bohatschek, M., Da Costa, C., Iwata, O., Galiano, M., Hristova, M., Nateri, A. S., Makwana, M., Riera-Sans, L., Wolfer, D. P. et al. (2004). The AP-1 transcription factor c-Jun is required for efficient axonal regeneration. Neuron 43, 57-67.
97. Rallis, A., Moore, C. and Ng, J. (2010). Signal strength and signal duration define two distinct aspects of JNK-regulated axon stability. Dev. Biol. 339, 65-77.
98. Ravikumar, B., Duden, R. and Rubinsztein, D. C. (2002). Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum. Mol. Genet. 11, 1107-1117.
99. Ribeiro, P. S., Kuranaga, E., Tenev, T., Leulier, F., Miura, M. and Meier, P. (2007). DIAP2 functions as a mechanism-based regulator of drICE that contributes to the caspase activity threshold in living cells. J. Cell Biol. 179, 1467-1480.
100. Rosso, S. B., Sussman, D., Wynshaw-Boris, A. and Salinas, P. C. (2005). Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat. Neurosci. 8, 34-42.
101. Sagot, Y., Dubois-Dauphin, M., Tan, S. A., de Bilbao, F., Aebischer, P., Martinou, J. C. and 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.
102. Sajadi, A., Schneider, B. L. and Aebischer, P. (2004). Wlds-mediated protection of dopaminergic fibers in an animal model of Parkinson disease. Curr. Biol. 14, 326-330.
103. Sanyal, S., Sandstrom, D. J., Hoeffer, C. A. and Ramaswami, M. (2002). AP-1 functions upstream of CREB to control synaptic plasticity in Drosophila. Nature 416, 870-874.
104. Sasaki, Y. and Milbrandt, J. (2010). Axonal degeneration is blocked by nicotinamide mononucleotide adenylyltransferase (Nmnat) protein transduction into transected axons. J. Biol. Chem. 285, 41211-41215.
105. Sasaki, Y., Vohra, B. P., Lund, F. E. and Milbrandt, J. (2009). Nicotinamide mononucleotide adenylyl transferase-mediated axonal protection requires enzymatic activity but not increased levels of neuronal nicotinamide adenine dinucleotide. J. Neurosci. 29, 5525-5535.
106. Saxena, S. and Caroni, P. (2007). Mechanisms of axon degeneration: from development to disease. Prog. Neurobiol. 83, 174-191.
107. Schoenmann, Z., Assa-Kunik, E., Tiomny, S., Minis, A., Haklai-Topper, L., Arama, E. and Yaron, A. (2010). Axonal degeneration is regulated by the apoptotic machinery or a NAD+-sensitive pathway in insects and mammals. J. Neurosci. 30, 6375-6386.
108. Schweiger, M., Hennig, K., Lerner, F., Niere, M., Hirsch-Kauffmann, M., Specht, T., Weise, C., Oei, S. L. and Ziegler, M. (2001). Characterization of recombinant human nicotinamide mononucleotide adenylyl transferase (NMNAT), a nuclear enzyme essential for NAD synthesis. FEBS Lett. 492, 95-100.
109. Sluss, H. K., Han, Z., Barrett, T., Goberdhan, D. C., Wilson, C., Davis, R. J. and Ip, Y. T. (1996). A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes Dev. 10, 2745-2758.
110. Tain, L. S., Mortiboys, H., Tao, R. N., Ziviani, E., Bandmann, O. and Whitworth, A. J. (2009). Rapamycin activation of 4E-BP prevents parkinsonian dopaminergic neuron loss. Nat. Neurosci. 12, 1129-1135.
111. Tao, J. and Rolls, M. M. (2011). Dendrites have a rapid program of injury-induced degeneration that is molecularly distinct from developmental pruning. J. Neurosci. 31, 5398-5405.
112. Thibault, S. T., Singer, M. A., Miyazaki, W. Y., Milash, B., Dompe, N. A., Singh, C. M., Buchholz, R., Demsky, M., Fawcett, R., Francis-Lang, H. L. et al. (2004). A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 36, 283-287.
113. Thomas, G. M., Lin, D. T., Nuriya, M. and Huganir, R. L. (2008). Rapid and bidirectional regulation of AMPA receptor phosphorylation and trafficking by JNK. EMBO J. 27, 361-372.
114. Vander Heiden, M. G., Chandel, N. S., Williamson, E. K., Schumacker, P. T. and Thompson, C. B. (1997). Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell 91, 627-637.
115. Vohra, B. P., Sasaki, Y., Miller, B. R., Chang, J., DiAntonio, A. and Milbrandt, J. (2010). Amyloid precursor protein cleavage-dependent and -independent axonal degeneration programs share a common nicotinamide mononucleotide adenylyltransferase 1-sensitive pathway. J. Neurosci. 30, 13729-13738.
116. Voisine, C., Pedersen, J. S. and Morimoto, R. I. (2010). Chaperone networks: tipping the balance in protein folding diseases. Neurobiol. Dis. 40, 12-20.
117. Waetzig, V., Zhao, Y. and Herdegen, T. (2006). The bright side of JNKs-Multitalented mediators in neuronal sprouting, brain development and nerve fiber regeneration. Prog. Neurobiol. 80, 84-97.
118. Wang, H. D., Kazemi-Esfarjani, P. and Benzer, S. (2004). Multiple-stress analysis for isolation of Drosophila longevity genes. Proc. Natl. Acad. Sci. USA 101, 12610-12615.
119. Wang, J., Zhai, Q., Chen, Y., Lin, E., Gu, W., McBurney, M. W. and He, Z. (2005). A local mechanism mediates NAD-dependent protection of axon degeneration. J. Cell Biol. 170, 349-355.
120. Wang, J. T., Medress, Z. A. and Barres, B. A. (2012). Axon degeneration: molecular mechanisms of a self-destruction pathway. J. Cell Biol. 196, 7-18.
121. Warrick, J. M., Chan, H. Y., Gray-Board, G. L., Chai, Y., Paulson, H. L. and Bonini, N. M. (1999). Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat. Genet. 23, 425-428.
122. Watanabe, M., Tsukiyama, T. and Hatakeyama, S. (2007). Protection of vincristineinduced neuropathy by WldS expression and the independence of the activity of Nmnat1. Neurosci. Lett. 411, 228-232.
123. Watts, R. J., Hoopfer, E. D. and Luo, L. (2003). Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitinproteasome system. Neuron 38, 871-885.
124. Wen, Y., Parrish, J. Z., He, R., Zhai, R. G. and Kim, M. D. (2011). Nmnat exerts neuroprotective effects in dendrites and axons. Mol. Cell. Neurosci. 48, 1-8.
125. Williams, D. W., Kondo, S., Krzyzanowska, A., Hiromi, Y. and Truman, J. W. (2006). Local caspase activity directs engulfment of dendrites during pruning. Nat. Neurosci. 9, 1234-1236.
126. Willis, D., Li, K. W., Zheng, J. Q., Chang, J. H., Smit, A. B., Kelly, T., Merianda, T. T., Sylvester, J., van Minnen, J. and Twiss, J. L. (2005). Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J. Neurosci. 25, 778-791.
127. Wong, E. and Cuervo, A. M. (2010). Autophagy gone awry in neurodegenerative diseases. Nat. Neurosci. 13, 805-811.
128. Wylie, S. R. and Chantler, P. D. (2003). Myosin IIA drives neurite retraction. Mol. Biol. Cell 14, 4654-4666.
129. Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J. and Greenberg, M. E. (1995). Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331.
130. Yahata, N., Yuasa, S. and Araki, T. (2009). Nicotinamide mononucleotide adenylyltransferase expression in mitochondrial matrix delays Wallerian degeneration. J. Neurosci. 29, 6276-6284.
131. Yang, D. D., Kuan, C. Y., Whitmarsh, A. J., Rincón, M., Zheng, T. S., Davis, R. J., Rakic, P. and Flavell, R. A. (1997). Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 389, 865-870.
132. Zhai, Q., Wang, J., Kim, A., Liu, Q., Watts, R., Hoopfer, E., Mitchison, T., Luo, L. and He, Z. (2003). Involvement of the ubiquitin-proteasome system in the early stages of wallerian degeneration. Neuron 39, 217-225.
133. Zhai, R. G., Cao, Y., Hiesinger, P. R., Zhou, Y., Mehta, S. Q., Schulze, K. L., Verstreken, P. and Bellen, H. J. (2006). Drosophila NMNAT maintains neural integrity independent of its NAD synthesis activity. PLoS Biol. 4, e416.
134. Zhai, R. G., Zhang, F., Hiesinger, P. R., Cao, Y., Haueter, C. M. and Bellen, H. J. (2008). NAD synthaseNMNAT acts as a chaperone to protect against neurodegeneration. Nature 452, 887-891.
135. Zhai, R. G., Rizzi, M. and Garavaglia, S. (2009). Nicotinamide/nicotinic acid mononucleotide adenylyltransferase, new insights into an ancient enzyme. Cell. Mol. Life Sci. 66, 2805-2818.