Mechanisms of neuronal homeostasis: Autophagy in the axon

Brain Research

Volumn 1649, Issue , 2016, Pages 143-150

  Maday, Sandra ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Autophagy; Axon; Neurodegeneration; Neuron; Retrograde transport

Indexed keywords

AUTOPHAGOSOME; AUTOPHAGY; AXON; BIOGENESIS; CELL MATURATION; HOMEOSTASIS; HUMAN; NERVE CELL NECROSIS; NERVE FIBER DEGENERATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; DEGENERATIVE DISEASE; GENETICS; MITOCHONDRION; MOUSE; MUTATION; NERVE DEGENERATION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

PARKIN; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE; UBIQUITIN PROTEIN LIGASE;

ANIMALS; AUTOPHAGOSOMES; AUTOPHAGY; AXONS; HOMEOSTASIS; HUMANS; MICE; MITOCHONDRIA; MUTATION; NERVE DEGENERATION; NEURODEGENERATIVE DISEASES; PROTEIN KINASES; UBIQUITIN-PROTEIN LIGASES;

EID: 84964620267     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2016.03.047     Document Type: Review

References (92)

1. Ashrafi, G., Schlehe, J.S., LaVoie, M.J., Schwarz, T.L., Mitophagy of damaged mitochondria occurs locally in distal neuronal axons and requires PINK1 and Parkin. J. Cell Biol. 206 (2014), 655–670.
2. Ban, B.K., Jun, M.H., Ryu, H.H., Jang, D.J., Ahmad, S.T., Lee, J.A., Autophagy negatively regulates early axon growth in cortical neurons. Mol. Cell. Biol. 33 (2013), 3907–3919.
3. Barmada, S.J., Serio, A., Arjun, A., Bilican, B., Daub, A., Ando, D.M., Tsvetkov, A., Pleiss, M., Li, X., Peisach, D., Shaw, C., Chandran, S., Finkbeiner, S., Autophagy induction enhances TDP43 turnover and survival in neuronal ALS models. Nat. Chem. Biol. 10 (2014), 677–685.
4. Bjorkoy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Overvatn, A., Stenmark, H., Johansen, T., p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171 (2005), 603–614.
5. Boland, B., Kumar, A., Lee, S., Platt, F.M., Wegiel, J., Yu, W.H., Nixon, R.A., Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J. Neurosci. 28 (2008), 6926–6937.
6. Buchan, J.R., Kolaitis, R.M., Taylor, J.P., Parker, R., Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell 153 (2013), 1461–1474.
7. Bunge, M.B., Fine structure of nerve fibers and growth cones of isolated sympathetic neurons in culture. J. Cell Biol. 56 (1973), 713–735.
8. Cai, Q., Zakaria, H.M., Simone, A., Sheng, Z.H., Spatial parkin translocation and degradation of damaged mitochondria via mitophagy in live cortical neurons. Curr. Biol. 22 (2012), 545–552.
9. Cheng, X.T., Zhou, B., Lin, M.Y., Cai, Q., Sheng, Z.H., Axonal autophagosomes recruit dynein for retrograde transport through fusion with late endosomes. J. Cell Biol. 209 (2015), 377–386.
10. Chowdary, P.D., Che, D.L., Cui, B., Neurotrophin signaling via long-distance axonal transport. Annu. Rev. Phys. Chem. 63 (2012), 571–594.
11. Cirulli, E.T., Lasseigne, B.N., Petrovski, S., Sapp, P.C., Dion, P.A., Leblond, C.S., Couthouis, J., Lu, Y.F., Wang, Q., Krueger, B.J., Ren, Z., Keebler, J., Han, Y., Levy, S.E., Boone, B.E., Wimbish, J.R., Waite, L.L., Jones, A.L., Carulli, J.P., Day-Williams, A.G., Staropoli, J.F., Xin, W.W., Chesi, A., Raphael, A.R., McKenna-Yasek, D., Cady, J., Vianney de Jong, J.M., Kenna, K.P., Smith, B.N., Topp, S., Miller, J., Gkazi, A., Consortium, F.S., Al-Chalabi, A., van den Berg, L.H., Veldink, J., Silani, V., Ticozzi, N., Shaw, C.E., Baloh, R.H., Appel, S., Simpson, E., Lagier-Tourenne, C., Pulst, S.M., Gibson, S., Trojanowski, J.Q., Elman, L., McCluskey, L., Grossman, M., Shneider, N.A., Chung, W.K., Ravits, J.M., Glass, J.D., Sims, K.B., Van Deerlin, V.M., Maniatis, T., Hayes, S.D., Ordureau, A., Swarup, S., Landers, J., Baas, F., Allen, A.S., Bedlack, R.S., Harper, J.W., Gitler, A.D., Rouleau, G.A., Brown, R., Harms, M.B., Cooper, G.M., Harris, T., Myers, R.M., Goldstein, D.B., Exome sequencing in amyotrophic lateral sclerosis identifies risk genes and pathways. Science 347 (2015), 1436–1441.
12. Cuervo, A.M., Autophagy and aging: keeping that old broom working. Trends Genet. 24 (2008), 604–612.
13. Deng, H.X., Chen, W., Hong, S.T., Boycott, K.M., Gorrie, G.H., Siddique, N., Yang, Y., Fecto, F., Shi, Y., Zhai, H., Jiang, H., Hirano, M., Rampersaud, E., Jansen, G.H., Donkervoort, S., Bigio, E.H., Brooks, B.R., Ajroud, K., Sufit, R.L., Haines, J.L., Mugnaini, E., Pericak-Vance, M.A., Siddique, T., Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 477 (2011), 211–215.
14. Devireddy, S., Liu, A., Lampe, T., Hollenbeck, P.J., The organization of mitochondrial quality control and life cycle in the nervous system in vivo in the absence of PINK1. J. Neurosci. 35 (2015), 9391–9401.
15. Dixon, J.S., “Phagocytic” lysosomes in chromatolytic neurones. Nature 215 (1967), 657–658.
16. Fecto, F., Yan, J., Vemula, S.P., Liu, E., Yang, Y., Chen, W., Zheng, J.G., Shi, Y., Siddique, N., Arrat, H., Donkervoort, S., Ajroud-Driss, S., Sufit, R.L., Heller, S.L., Deng, H.X., Siddique, T., SQSTM1 mutations in familial and sporadic amyotrophic lateral sclerosis. Arch. Neurol. 68 (2011), 1440–1446.
17. Ferree, A.W., Trudeau, K., Zik, E., Benador, I.Y., Twig, G., Gottlieb, R.A., Shirihai, O.S., MitoTimer probe reveals the impact of autophagy, fusion, and motility on subcellular distribution of young and old mitochondrial protein and on relative mitochondrial protein age. Autophagy 9 (2013), 1887–1896.
18. Fimia, G.M., Stoykova, A., Romagnoli, A., Giunta, L., Di Bartolomeo, S., Nardacci, R., Corazzari, M., Fuoco, C., Ucar, A., Schwartz, P., Gruss, P., Piacentini, M., Chowdhury, K., Cecconi, F., Ambra1 regulates autophagy and development of the nervous system. Nature 447 (2007), 1121–1125.
19. Friedman, L.G., Lachenmayer, M.L., Wang, J., He, L., Poulose, S.M., Komatsu, M., Holstein, G.R., Yue, Z., Disrupted autophagy leads to dopaminergic axon and dendrite degeneration and promotes presynaptic accumulation of alpha-synuclein and LRRK2 in the brain. J. Neurosci. 32 (2012), 7585–7593.
20. Fu, M.M., Nirschl, J.J., Holzbaur, E.L., LC3 binding to the scaffolding protein JIP1 regulates processive dynein-driven transport of autophagosomes. Dev. Cell 29 (2014), 577–590.
21. Gowrishankar, S., Yuan, P., Wu, Y., Schrag, M., Paradise, S., Grutzendler, J., De Camilli, P., Ferguson, S.M., Massive accumulation of luminal protease-deficient axonal lysosomes at Alzheimer's disease amyloid plaques. Proc. Natl. Acad. Sci. USA 112 (2015), E3699–E3708.
22. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H., Mizushima, N., Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441 (2006), 885–889.
23. Harrington, A.W., Ginty, D.D., Long-distance retrograde neurotrophic factor signalling in neurons. Nat. Rev. Neurosci. 14 (2013), 177–187.
24. Heo, J.M., Ordureau, A., Paulo, J.A., Rinehart, J., Harper, J.W., The PINK1-PARKIN mitochondrial ubiquitylation pathway drives a program of OPTN/NDP52 recruitment and TBK1 activation to promote mitophagy. Mol. Cell 60 (2015), 7–20.
25. Hernandez, D., Torres, C.A., Setlik, W., Cebrian, C., Mosharov, E.V., Tang, G., Cheng, H.C., Kholodilov, N., Yarygina, O., Burke, R.E., Gershon, M., Sulzer, D., Regulation of presynaptic neurotransmission by macroautophagy. Neuron 74 (2012), 277–284.
26. Hollenbeck, P.J., Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J. Cell Biol. 121 (1993), 305–315.
27. Johnson, J.O., Mandrioli, J., Benatar, M., Abramzon, Y., Van Deerlin, V.M., Trojanowski, J.Q., Gibbs, J.R., Brunetti, M., Gronka, S., Wuu, J., Ding, J., McCluskey, L., Martinez-Lage, M., Falcone, D., Hernandez, D.G., Arepalli, S., Chong, S., Schymick, J.C., Rothstein, J., Landi, F., Wang, Y.D., Calvo, A., Mora, G., Sabatelli, M., Monsurro, M.R., Battistini, S., Salvi, F., Spataro, R., Sola, P., Borghero, G., Consortium, I., Galassi, G., Scholz, S.W., Taylor, J.P., Restagno, G., Chio, A., Traynor, B.J., Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 68 (2010), 857–864.
28. Ju, J.S., Fuentealba, R.A., Miller, S.E., Jackson, E., Piwnica-Worms, D., Baloh, R.H., Weihl, C.C., Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease. J. Cell Biol. 187 (2009), 875–888.
29. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., Yoshimori, T., LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19 (2000), 5720–5728.
30. Kane, L.A., Lazarou, M., Fogel, A.I., Li, Y., Yamano, K., Sarraf, S.A., Banerjee, S., Youle, R.J., PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J. Cell Biol. 205 (2014), 143–153.
31. Kim, N.C., Tresse, E., Kolaitis, R.M., Molliex, A., Thomas, R.E., Alami, N.H., Wang, B., Joshi, A., Smith, R.B., Ritson, G.P., Winborn, B.J., Moore, J., Lee, J.Y., Yao, T.P., Pallanck, L., Kundu, M., Taylor, J.P., VCP is essential for mitochondrial quality control by PINK1/Parkin and this function is impaired by VCP mutations. Neuron 78 (2013), 65–80.
32. Kiriyama, Y., Nochi, H., The function of autophagy in neurodegenerative diseases. Int. J. Mol. Sci. 16 (2015), 26797–26812.
33. Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., Shimizu, N., Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392 (1998), 605–608.
34. Komatsu, M., Wang, Q.J., Holstein, G.R., Friedrich, V.L. Jr., Iwata, J., Kominami, E., Chait, B.T., Tanaka, K., Yue, Z., Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc. Natl. Acad. Sci. USA 104 (2007), 14489–14494.
35. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., Tanaka, K., Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441 (2006), 880–884.
36. Labbadia, J., Morimoto, R.I., Proteostasis and longevity: when does aging really begin?. F1000Prime Rep., 6, 2014, 7.
37. Lazarou, M., Sliter, D.A., Kane, L.A., Sarraf, S.A., Wang, C., Burman, J.L., Sideris, D.P., Fogel, A.I., Youle, R.J., The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature 524 (2015), 309–314.
38. Lee, J.H., Yu, W.H., Kumar, A., Lee, S., Mohan, P.S., Peterhoff, C.M., Wolfe, D.M., Martinez-Vicente, M., Massey, A.C., Sovak, G., Uchiyama, Y., Westaway, D., Cuervo, A.M., Nixon, R.A., Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 141 (2010), 1146–1158.
39. Lee, K.M., Hwang, S.K., Lee, J.A., Neuronal autophagy and neurodevelopmental disorders. Exp. Neurobiol. 22 (2013), 133–142.
40. Lee, S., Sato, Y., Nixon, R.A., Lysosomal proteolysis inhibition selectively disrupts axonal transport of degradative organelles and causes an Alzheimer's-like axonal dystrophy. J. Neurosci. 31 (2011), 7817–7830.
41. Lehmann, H.C., Chen, W., Borzan, J., Mankowski, J.L., Hoke, A., Mitochondrial dysfunction in distal axons contributes to human immunodeficiency virus sensory neuropathy. Ann. Neurol. 69 (2011), 100–110.
42. Li, L., Zhang, X., Le, W., Altered macroautophagy in the spinal cord of SOD1 mutant mice. Autophagy 4 (2008), 290–293.
43. Lipinski, M.M., Zheng, B., Lu, T., Yan, Z., Py, B.F., Ng, A., Xavier, R.J., Li, C., Yankner, B.A., Scherzer, C.R., Yuan, J., Genome-wide analysis reveals mechanisms modulating autophagy in normal brain aging and in Alzheimer's disease. Proc. Natl. Acad. Sci. USA 107 (2010), 14164–14169.
44. Maday, S., Holzbaur, E.L., Autophagosome assembly and cargo capture in the distal axon. Autophagy 8 (2012), 858–860.
45. Maday, S., Holzbaur, E.L., Autophagosome biogenesis in primary neurons follows an ordered and spatially regulated pathway. Dev. Cell 30 (2014), 71–85.
46. Maday, S., Wallace, K.E., Holzbaur, E.L., Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J. Cell Biol. 196 (2012), 407–417.
47. Maday, S., Twelvetrees, A.E., Moughamian, A.J., Holzbaur, E.L., Axonal transport: cargo-specific mechanisms of motility and regulation. Neuron 84 (2014), 292–309.
48. Majcher, V., Goode, A., James, V., Layfield, R., Autophagy receptor defects and ALS-FTLD. Mol. Cell. Neurosci. 66 (2015), 43–52.
49. Martinez-Vicente, M., Talloczy, Z., Wong, E., Tang, G., Koga, H., Kaushik, S., de Vries, R., Arias, E., Harris, S., Sulzer, D., Cuervo, A.M., Cargo recognition failure is responsible for inefficient autophagy in Huntington's disease. Nat. Neurosci. 13 (2010), 567–576.
50. Maruyama, H., Morino, H., Ito, H., Izumi, Y., Kato, H., Watanabe, Y., Kinoshita, Y., Kamada, M., Nodera, H., Suzuki, H., Komure, O., Matsuura, S., Kobatake, K., Morimoto, N., Abe, K., Suzuki, N., Aoki, M., Kawata, A., Hirai, T., Kato, T., Ogasawara, K., Hirano, A., Takumi, T., Kusaka, H., Hagiwara, K., Kaji, R., Kawakami, H., Mutations of optineurin in amyotrophic lateral sclerosis. Nature 465 (2010), 223–226.
51. Matsumoto, G., Shimogori, T., Hattori, N., Nukina, N., TBK1 controls autophagosomal engulfment of polyubiquitinated mitochondria through p62/SQSTM1 phosphorylation. Hum. Mol. Genet. 24 (2015), 4429–4442.
52. Matthews, M.R., Raisman, G., A light and electron microscopic study of the cellular response to axonal injury in the superior cervical ganglion of the rat. Proc. R. Soc. Lond. B Biol. Sci. 181 (1972), 43–79.
53. Millecamps, S., Julien, J.P., Axonal transport deficits and neurodegenerative diseases. Nat. Rev. Neurosci. 14 (2013), 161–176.
54. Mizushima, N., Yoshimori, T., Ohsumi, Y., The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27 (2011), 107–132.
55. Mizushima, N., Levine, B., Cuervo, A.M., Klionsky, D.J., Autophagy fights disease through cellular self-digestion. Nature 451 (2008), 1069–1075.
56. Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., Ohsumi, Y., In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15 (2004), 1101–1111.
57. Morimoto, N., Nagai, M., Ohta, Y., Miyazaki, K., Kurata, T., Morimoto, M., Murakami, T., Takehisa, Y., Ikeda, Y., Kamiya, T., Abe, K., Increased autophagy in transgenic mice with a G93A mutant SOD1 gene. Brain Res. 1167 (2007), 112–117.
58. N'Diaye, E.N., Kajihara, K.K., Hsieh, I., Morisaki, H., Debnath, J., Brown, E.J., PLIC proteins or ubiquilins regulate autophagy-dependent cell survival during nutrient starvation. EMBO Rep. 10 (2009), 173–179.
59. Narendra, D., Tanaka, A., Suen, D.F., Youle, R.J., Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183 (2008), 795–803.
60. Narendra, D.P., Jin, S.M., Tanaka, A., Suen, D.F., Gautier, C.A., Shen, J., Cookson, M.R., Youle, R.J., PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol., 8, 2010, e1000298.
61. Nishiyama, J., Miura, E., Mizushima, N., Watanabe, M., Yuzaki, M., Aberrant membranes and double-membrane structures accumulate in the axons of Atg5-null Purkinje cells before neuronal death. Autophagy 3 (2007), 591–596.
62. Nixon, R.A., Wegiel, J., Kumar, A., Yu, W.H., Peterhoff, C., Cataldo, A., Cuervo, A.M., Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J. Neuropathol. Exp. Neurol. 64 (2005), 113–122.
63. Pankiv, S., Clausen, T.H., Lamark, T., Brech, A., Bruun, J.A., Outzen, H., Overvatn, A., Bjorkoy, G., Johansen, T., p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282 (2007), 24131–24145.
64. Pickrell, A.M., Youle, R.J., The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson's disease. Neuron 85 (2015), 257–273.
65. Price, J.C., Guan, S., Burlingame, A., Prusiner, S.B., Ghaemmaghami, S., Analysis of proteome dynamics in the mouse brain. Proc. Natl. Acad. Sci. USA 107 (2010), 14508–14513.
66. Ravikumar, B., Acevedo-Arozena, A., Imarisio, S., Berger, Z., Vacher, C., O'Kane, C.J., Brown, S.D., Rubinsztein, D.C., Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat. Genet. 37 (2005), 771–776.
67. Rothenberg, C., Srinivasan, D., Mah, L., Kaushik, S., Peterhoff, C.M., Ugolino, J., Fang, S., Cuervo, A.M., Nixon, R.A., Monteiro, M.J., Ubiquilin functions in autophagy and is degraded by chaperone-mediated autophagy. Hum. Mol. Genet. 19 (2010), 3219–3232.
68. Rubinsztein, D.C., DiFiglia, M., Heintz, N., Nixon, R.A., Qin, Z.H., Ravikumar, B., Stefanis, L., Tolkovsky, A., Autophagy and its possible roles in nervous system diseases, damage and repair. Autophagy 1 (2005), 11–22.
69. Saitsu, H., Nishimura, T., Muramatsu, K., Kodera, H., Kumada, S., Sugai, K., Kasai-Yoshida, E., Sawaura, N., Nishida, H., Hoshino, A., Ryujin, F., Yoshioka, S., Nishiyama, K., Kondo, Y., Tsurusaki, Y., Nakashima, M., Miyake, N., Arakawa, H., Kato, M., Mizushima, N., Matsumoto, N., De novo mutations in the autophagy gene WDR45 cause static encephalopathy of childhood with neurodegeneration in adulthood. Nat. Genet., 45(445–449), 2013, 449e1.
70. Scott, D.A., Das, U., Tang, Y., Roy, S., Mechanistic logic underlying the axonal transport of cytosolic proteins. Neuron 70 (2011), 441–454.
71. Shen, D.N., Zhang, L.H., Wei, E.Q., Yang, Y., Autophagy in synaptic development, function, and pathology. Neurosci. Bull. 31 (2015), 416–426.
72. Shen, W., Ganetzky, B., Autophagy promotes synapse development in Drosophila. J. Cell Biol. 187 (2009), 71–79.
73. Spalding, K.L., Bhardwaj, R.D., Buchholz, B.A., Druid, H., Frisen, J., Retrospective birth dating of cells in humans. Cell 122 (2005), 133–143.
74. Tang, G., Gudsnuk, K., Kuo, S.H., Cotrina, M.L., Rosoklija, G., Sosunov, A., Sonders, M.S., Kanter, E., Castagna, C., Yamamoto, A., Yue, Z., Arancio, O., Peterson, B.S., Champagne, F., Dwork, A.J., Goldman, J., Sulzer, D., Loss of mTOR-dependent macroautophagy causes autistic-like synaptic pruning deficits. Neuron 83 (2014), 1131–1143.
75. Tresse, E., Salomons, F.A., Vesa, J., Bott, L.C., Kimonis, V., Yao, T.P., Dantuma, N.P., Taylor, J.P., VCP/p97 is essential for maturation of ubiquitin-containing autophagosomes and this function is impaired by mutations that cause IBMPFD. Autophagy 6 (2010), 217–227.
76. Tsukada, M., Ohsumi, Y., Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333 (1993), 169–174.
77. Valente, E.M., Abou-Sleiman, P.M., Caputo, V., Muqit, M.M., Harvey, K., Gispert, S., Ali, Z., Del Turco, D., Bentivoglio, A.R., Healy, D.G., Albanese, A., Nussbaum, R., Gonzalez-Maldonado, R., Deller, T., Salvi, S., Cortelli, P., Gilks, W.P., Latchman, D.S., Harvey, R.J., Dallapiccola, B., Auburger, G., Wood, N.W., Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304 (2004), 1158–1160.
78. Van Laar, V.S., Arnold, B., Cassady, S.J., Chu, C.T., Burton, E.A., Berman, S.B., Bioenergetics of neurons inhibit the translocation response of Parkin following rapid mitochondrial depolarization. Hum. Mol. Genet. 20 (2011), 927–940.
79. Wang, Q.J., Ding, Y., Kohtz, D.S., Mizushima, N., Cristea, I.M., Rout, M.P., Chait, B.T., Zhong, Y., Heintz, N., Yue, Z., Induction of autophagy in axonal dystrophy and degeneration. J. Neurosci. 26 (2006), 8057–8068.
80. Wang, T., Martin, S., Papadopulos, A., Harper, C.B., Mavlyutov, T.A., Niranjan, D., Glass, N.R., Cooper-White, J.J., Sibarita, J.B., Choquet, D., Davletov, B., Meunier, F.A., Control of autophagosome axonal retrograde flux by presynaptic activity unveiled using botulinum neurotoxin type a. J. Neurosci. 35 (2015), 6179–6194.
81. Weidberg, H., Shvets, E., Elazar, Z., Biogenesis and cargo selectivity of autophagosomes. Annu. Rev. Biochem. 80 (2011), 125–156.
82. Wild, P., Farhan, H., McEwan, D.G., Wagner, S., Rogov, V.V., Brady, N.R., Richter, B., Korac, J., Waidmann, O., Choudhary, C., Dotsch, V., Bumann, D., Dikic, I., Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333 (2011), 228–233.
83. Wong, Y.C., Holzbaur, E.L., The regulation of autophagosome dynamics by huntingtin and HAP1 is disrupted by expression of mutant huntingtin, leading to defective cargo degradation. J. Neurosci. 34 (2014), 1293–1305.
84. Wong, Y.C., Holzbaur, E.L., Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc. Natl. Acad. Sci. USA 111 (2014), E4439–E4448.
85. Xie, Y., Zhou, B., Lin, M.Y., Wang, S., Foust, K.D., Sheng, Z.H., Endolysosomal deficits augment mitochondria pathology in spinal motor neurons of asymptomatic fALS mice. Neuron 87 (2015), 355–370.
86. Xie, Z., Klionsky, D.J., Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9 (2007), 1102–1109.
87. Yamamoto, A., Yue, Z., Autophagy and its normal and pathogenic states in the brain. Annu. Rev. Neurosci. 37 (2014), 55–78.
88. Yang, Y., Coleman, M., Zhang, L., Zheng, X., Yue, Z., Autophagy in axonal and dendritic degeneration. Trends Neurosci. 36 (2013), 418–428.
89. Yue, Z., Regulation of neuronal autophagy in axon: implication of autophagy in axonal function and dysfunction/degeneration. Autophagy 3 (2007), 139–141.
90. Yue, Z., Friedman, L., Komatsu, M., Tanaka, K., The cellular pathways of neuronal autophagy and their implication in neurodegenerative diseases. Biochim. Biophys. Acta 1793 (2009), 1496–1507.
91. Zhao, C., Deng, W., Gage, F.H., Mechanisms and functional implications of adult neurogenesis. Cell 132 (2008), 645–660.
92. Zhao, Y.G., Sun, L., Miao, G., Ji, C., Zhao, H., Sun, H., Miao, L., Yoshii, S.R., Mizushima, N., Wang, X., Zhang, H., The autophagy gene Wdr45/Wipi4 regulates learning and memory function and axonal homeostasis. Autophagy 11 (2015), 881–890.