Autophagy at synapses in neurodegenerative diseases

  • Wongyoung Lee
  • Sung Hyun KimEmail author


Autophagy is an essential process for maintaining cellular homeostasis, a critical process in all cell types. Because neurons are post-mitotic cells, maintaining cellular and functional homeostasis is more important in neurons than in other types of cells. Synapses are fundamental units needed for neural communication, and synapses with consistent protein quality are essential for neural functionality. Dysregulation of autophagy in neurons has been shown to be related to neurodegenerative diseases, including Alzheimer’s disease and Parkinson’s disease. This review describes the role of autophagy in the maintenance of synaptic functionality and the association between synaptic autophagy and neurodegenerative diseases.


Autophagy Synapse Synaptic transmission Synaptic retrieval Alzheimer’s disease Parkinson’s disease 



We thank Soondo Hwang, Soulmee Koh, and Do Ru Kwon from the Synapse Communication Laboratory for their valuable comments. This work was supported by the National Research Foundation of Korea (2017M3C7A1048268, 2017R1A2B4007019, 2018R1A6A1A03025124).

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.


  1. Alvarez-Erviti L, Rodriguez-Oroz MC, Cooper JM, Caballero C, Ferrer I, Obeso JA, Schapira AH (2010) Chaperone-mediated autophagy markers in Parkinson disease brains. Arch Neurol 67:1464–1472CrossRefGoogle Scholar
  2. Ashrafi G, Schlehe JS, Lavoie MJ, Schwarz TL (2014) Mitophagy of damaged mitochondria occurs locally in distal neuronal axons and requires PINK1 and Parkin. J Cell Biol 206:655–670CrossRefGoogle Scholar
  3. Binotti B, Pavlos NJ, Riedel D, Wenzel D, Vorbruggen G, Schalk AM, Kuhnel K, Boyken J, Erck C, Martens H, Chua JJ, Jahn R (2015) The GTPase Rab26 links synaptic vesicles to the autophagy pathway. Elife 4:e05597CrossRefGoogle Scholar
  4. Bravo-San Pedro JM, Gomez-Sanchez R, Niso-Santano M, Pizarro-Estrella E, Aiastui-Pujana A, Gorostidi A, Climent V, Lopez De Maturana R, Sanchez-Pernaute R, Lopez De Munain A, Fuentes JM, Gonzalez-Polo RA (2012) The MAPK1/3 pathway is essential for the deregulation of autophagy observed in G2019S LRRK2 mutant fibroblasts. Autophagy 8:1537–1539CrossRefGoogle Scholar
  5. Burke RE, O’Malley K (2013) Axon degeneration in Parkinson’s disease. Exp Neurol 246:72–83CrossRefGoogle Scholar
  6. Campbell P, Morris H, Schapira A (2018) Chaperone-mediated autophagy as a therapeutic target for Parkinson disease. Expert Opin Ther Targets 22:823–832CrossRefGoogle Scholar
  7. Catanese A, Garrido D, Walther P, Roselli F, Boeckers TM (2018) Nutrient limitation affects presynaptic structures through dissociable Bassoon autophagic degradation and impaired vesicle release. J Cereb Blood Flow Metab 38:1924–1939CrossRefGoogle Scholar
  8. Chen D, Gao F, Li B, Wang H, Xu Y, Zhu C, Wang G (2010) Parkin mono-ubiquitinates Bcl-2 and regulates autophagy. J Biol Chem 285:38214–38223CrossRefGoogle Scholar
  9. Cheng HC, Ulane CM, Burke RE (2010) Clinical progression in Parkinson disease and the neurobiology of axons. Ann Neurol 67:715–725CrossRefGoogle Scholar
  10. Cremona O, Di Paolo G, Wenk MR, Luthi A, Kim WT, Takei K, Daniell L, Nemoto Y, Shears SB, Flavell RA, Mccormick DA, De Camilli P (1999) Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99:179–188CrossRefGoogle Scholar
  11. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D (2004) Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 305:1292–1295CrossRefGoogle Scholar
  12. Dai S, Wang B, Li W, Wang L, Song X, Guo C, Li Y, Liu F, Zhu F, Wang Q, Wang X, Shi Y, Wang J, Zhao W, Zhang L (2016) Systemic application of 3-methyladenine markedly inhibited atherosclerotic lesion in ApoE(-/-) mice by modulating autophagy, foam cell formation and immune-negative molecules. Cell Death Dis 7:e2498CrossRefGoogle Scholar
  13. Dolan PJ, Johnson GV (2010) A caspase cleaved form of tau is preferentially degraded through the autophagy pathway. J Biol Chem 285:21978–21987CrossRefGoogle Scholar
  14. Ebrahimi-Fakhari D, Saffari A, Wahlster L, Di Nardo A, Turner D, Lewis TL Jr, Conrad C, Rothberg JM, Lipton JO, Kolker S, Hoffmann GF, Han MJ, Polleux F, Sahin M (2016) Impaired mitochondrial dynamics and mitophagy in neuronal models of tuberous sclerosis complex. Cell Rep 17:1053–1070CrossRefGoogle Scholar
  15. Engelender S (2008) Ubiquitination of alpha-synuclein and autophagy in Parkinson’s disease. Autophagy 4:372–374CrossRefGoogle Scholar
  16. Feng Y, He D, Yao Z, Klionsky DJ (2014) The machinery of macroautophagy. Cell Res 24:24–41CrossRefGoogle Scholar
  17. Friedman LG, Lachenmayer ML, Wang J, He L, Poulose SM, Komatsu M, Holstein GR, Yue Z (2012) Disrupted autophagy leads to dopaminergic axon and dendrite degeneration and promotes presynaptic accumulation of alpha-synuclein and LRRK2 in the brain. J Neurosci 32:7585–7593CrossRefGoogle Scholar
  18. George AA, Hayden S, Holzhausen LC, Ma EY, Suzuki SC, Brockerhoff SE (2014) Synaptojanin 1 is required for endolysosomal trafficking of synaptic proteins in cone photoreceptor inner segments. PLoS ONE 9:e84394CrossRefGoogle Scholar
  19. George AA, Hayden S, Stanton GR, Brockerhoff SE (2016) Arf6 and the 5′ phosphatase of synaptojanin 1 regulate autophagy in cone photoreceptors. Inside Cell 1:117–133CrossRefGoogle Scholar
  20. Glatigny M, Moriceau S, Rivagorda M, Ramos-Brossier M, Nascimbeni AC, Lante F, Shanley MR, Boudarene N, Rousseaud A, Friedman AK, Settembre C, Kuperwasser N, Friedlander G, Buisson A, Morel E, Codogno P, Oury F (2019) Autophagy is required for memory formation and reverses age-related memory decline. Curr Biol 29:435–448CrossRefGoogle Scholar
  21. Gomez-Suaga P, Churchill GC, Patel S, Hilfiker S (2012a) A link between LRRK2, autophagy and NAADP-mediated endolysosomal calcium signalling. Biochem Soc Trans 40:1140–1146CrossRefGoogle Scholar
  22. Gomez-Suaga P, Fdez E, Blanca Ramirez M, Hilfiker S (2012b) A link between autophagy and the pathophysiology of LRRK2 in Parkinson’s disease. Parkinsons Dis 2012:324521Google Scholar
  23. Haberman A, Williamson WR, Epstein D, Wang D, Rina S, Meinertzhagen IA, Hiesinger PR (2012) The synaptic vesicle SNARE neuronal synaptobrevin promotes endolysosomal degradation and prevents neurodegeneration. J Cell Biol 196:261–276CrossRefGoogle Scholar
  24. Hernandez D, Torres CA, Setlik W, Cebrian C, Mosharov EV, Tang G, Cheng HC, Kholodilov N, Yarygina O, Burke RE, Gershon M, Sulzer D (2012) Regulation of presynaptic neurotransmission by macroautophagy. Neuron 74:277–284CrossRefGoogle Scholar
  25. Jo C, Gundemir S, Pritchard S, Jin YN, Rahman I, Johnson GV (2014) Nrf2 reduces levels of phosphorylated tau protein by inducing autophagy adaptor protein NDP52. Nat Commun 5:3496CrossRefGoogle Scholar
  26. Joshi G, Gan KA, Johnson DA, Johnson JA (2015) Increased Alzheimer’s disease-like pathology in the APP/PS1ΔE9 mouse model lacking Nrf2 through modulation of autophagy. Neurobiol Aging 36:664–679CrossRefGoogle Scholar
  27. Kaushik S, Cuervo AM (2012) Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol 22:407–417CrossRefGoogle Scholar
  28. Kim J, Basak JM, Holtzman DM (2009) The role of apolipoprotein E in Alzheimer’s disease. Neuron 63:287–303CrossRefGoogle Scholar
  29. Koh TW, Verstreken P, Bellen HJ (2004) Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43:193–205CrossRefGoogle Scholar
  30. Li Q, Liu Y, Sun M (2017) Autophagy and Alzheimer’s disease. Cell Mol Neurobiol 37:377–388CrossRefGoogle Scholar
  31. Li W, Li K, Gao J, Yang Z (2018) Autophagy is required for human umbilical cord mesenchymal stem cells to improve spatial working memory in APP/PS1 transgenic mouse model. Stem Cell Res Ther 9:9CrossRefGoogle Scholar
  32. Liang Y (2019) Emerging concepts and functions of autophagy as a regulator of synaptic components and plasticity. Cells 8:34CrossRefGoogle Scholar
  33. Liang Y, Sigrist S (2018) Autophagy and proteostasis in the control of synapse aging and disease. Curr Opin Neurobiol 48:113–121CrossRefGoogle Scholar
  34. Lieberman OJ, Mcguirt AF, Tang G, Sulzer D (2018) Roles for neuronal and glial autophagy in synaptic pruning during development. Neurobiol Dis 122:49–63CrossRefGoogle Scholar
  35. Lonskaya I, Hebron ML, Algarzae NK, Desforges N, Moussa CE (2013) Decreased parkin solubility is associated with impairment of autophagy in the nigrostriatum of sporadic Parkinson’s disease. Neuroscience 232:90–105CrossRefGoogle Scholar
  36. Lüningschrör P, Binotti B, Dombert B, Heimann P, Perez-Lara A, Slotta C, Thau-Habermann N, Von Collenberg CR, Karl F, Damme M, Horowitz A, Maystadt I, Füchtbauer A, Füchtbauer EM, Jablonka S, Blum R, Üçeyler N, Petri S, Kaltschmidt B, Jahn R, Kaltschmidt C, Sendtner M (2017) Plekhg5-regulated autophagy of synaptic vesicles reveals a pathogenic mechanism in motoneuron disease. Nat Commun 8:678CrossRefGoogle Scholar
  37. Maday S, Holzbaur ELF (2016) Compartment-specific regulation of autophagy in primary neurons. J Neurosci 36:5933–5945CrossRefGoogle Scholar
  38. Maday S, Wallace KE, Holzbaur ELF (2012) Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J Cell Biol 196:407–417CrossRefGoogle Scholar
  39. Manczak M, Kandimalla R, Yin X, Reddy PH (2018) Hippocampal mutant APP and amyloid beta-induced cognitive decline, dendritic spine loss, defective autophagy, mitophagy and mitochondrial abnormalities in a mouse model of Alzheimer’s disease. Hum Mol Genet 27:1332–1342CrossRefGoogle Scholar
  40. Mani M, Lee SY, Lucast L, Cremona O, Di Paolo G, De Camilli P, Ryan TA (2007) The dual phosphatase activity of synaptojanin1 is required for both efficient synaptic vesicle endocytosis and reavailability at nerve terminals. Neuron 56:1004–1018CrossRefGoogle Scholar
  41. Marie B, Sweeney ST, Poskanzer KE, Roos J, Kelly RB, Davis GW (2004) Dap160/intersectin scaffolds the periactive zone to achieve high-fidelity endocytosis and normal synaptic growth. Neuron 43:207–219CrossRefGoogle Scholar
  42. Martinez-Vicente M, Talloczy Z, Kaushik S, Massey AC, Mazzulli J, Mosharov EV, Hodara R, Fredenburg R, Wu DC, Follenzi A, Dauer W, Przedborski S, Ischiropoulos H, Lansbury PT, Sulzer D, Cuervo AM (2008) Dopamine-modified alpha-synuclein blocks chaperone-mediated autophagy. J Clin Invest 118:777–788Google Scholar
  43. Metaxakis A, Ploumi C, Tavernarakis N (2018) Autophagy in age-associated neurodegeneration. Cells 7:37CrossRefGoogle Scholar
  44. Milosevic I, Giovedi S, Lou X, Raimondi A, Collesi C, Shen H, Paradise S, O’toole E, Ferguson S, Cremona O, De Camilli P (2011) Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission. Neuron 72:587–601CrossRefGoogle Scholar
  45. Minakaki G, Menges S, Kittel A, Emmanouilidou E, Schaeffner I, Barkovits K, Bergmann A, Rockenstein E, Adame A, Marxreiter F, Mollenhauer B, Galasko D, Buzas EI, Schlotzer-Schrehardt U, Marcus K, Xiang W, Lie DC, Vekrellis K, Masliah E, Winkler J, Klucken J (2018) Autophagy inhibition promotes SNCA/alpha-synuclein release and transfer via extracellular vesicles with a hybrid autophagosome-exosome-like phenotype. Autophagy 14:98–119CrossRefGoogle Scholar
  46. Mizushima N, Komatsu M (2011) Autophagy: renovation of cells and tissues. Cell 147:728–741CrossRefGoogle Scholar
  47. Moreau K, Fleming A, Imarisio S, Lopez Ramirez A, Mercer JL, Jimenez-Sanchez M, Bento CF, Puri C, Zavodszky E, Siddiqi F, Lavau CP, Betton M, O’kane CJ, Wechsler DS, Rubinsztein DC (2014) PICALM modulates autophagy activity and tau accumulation. Nat Commun 5:4998CrossRefGoogle Scholar
  48. Murdoch JD, Rostosky CM, Gowrisankaran S, Arora AS, Soukup SF, Vidal R, Capece V, Freytag S, Fischer A, Verstreken P, Bonn S, Raimundo N, Milosevic I (2016) Endophilin-A deficiency induces the Foxo3a-Fbxo32 network in the brain and causes dysregulation of autophagy and the ubiquitin-proteasome system. Cell Rep 17:1071–1086CrossRefGoogle Scholar
  49. Nah J, Pyo JO, Jung S, Yoo SM, Kam TI, Chang J, Han J, AaS Soo, Onodera T, Jung YK (2013) BECN1/beclin 1 is recruited into lipid rafts by prion to activate autophagy in response to amyloid beta 42. Autophagy 9:2009–2021CrossRefGoogle Scholar
  50. Narendra D, Tanaka A, Suen DF, Youle RJ (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183:795–803CrossRefGoogle Scholar
  51. Nash Y, Schmukler E, Trudler D, Pinkas-Kramarski R, Frenkel D (2017) DJ-1 deficiency impairs autophagy and reduces alpha-synuclein phagocytosis by microglia. J Neurochem 143:584–594CrossRefGoogle Scholar
  52. Nikoletopoulou V, Tavernarakis N (2018) Regulation and roles of autophagy at synapses. Trends Cell Biol 28:646–661CrossRefGoogle Scholar
  53. Okerlund ND, Schneider K, Leal-Ortiz S, Montenegro-Venegas C, Kim SA, Garner LC, Waites CL, Gundelfinger ED, Reimer RJ, Garner CC (2017) Bassoon controls presynaptic autophagy through Atg5. Neuron 93(897–913):e7Google Scholar
  54. Orenstein SJ, Kuo SH, Tasset I, Arias E, Koga H, Fernandez-Carasa I, Cortes E, Honig LS, Dauer W, Consiglio A, Raya A, Sulzer D, Cuervo AM (2013) Interplay of LRRK2 with chaperone-mediated autophagy. Nat Neurosci 16:394–406CrossRefGoogle Scholar
  55. Peng J, Yang Q, Li AF, Li RQ, Wang Z, Liu LS, Ren Z, Zheng XL, Tang XQ, Li GH, Tang ZH, Jiang ZS, Wei DH (2016) Tet methylcytosine dioxygenase 2 inhibits atherosclerosis via upregulation of autophagy in ApoE-/- mice. Oncotarget 7:76423–76436Google Scholar
  56. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, Wyss-Coray T (2008) The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest 118:2190–2199Google Scholar
  57. Reddy PH, Yin X, Manczak M, Kumar S, Pradeepkiran JA, Vijayan M, Reddy AP (2018) Mutant APP and amyloid beta-induced defective autophagy, mitophagy, mitochondrial structural and functional changes and synaptic damage in hippocampal neurons from Alzheimer’s disease. Hum Mol Genet 27:2502–2516CrossRefGoogle Scholar
  58. Ryter SW, Cloonan SM, Choi AM (2013) Autophagy: a critical regulator of cellular metabolism and homeostasis. Mol Cells 36:7–16CrossRefGoogle Scholar
  59. Saez-Atienzar S, Bonet-Ponce L, Blesa JR, Romero FJ, Murphy MP, Jordan J, Galindo MF (2014) The LRRK2 inhibitor GSK2578215A induces protective autophagy in SH-SY5Y cells: involvement of Drp-1-mediated mitochondrial fission and mitochondrial-derived ROS signaling. Cell Death Dis 5:e1368CrossRefGoogle Scholar
  60. Saha S, Liu-Yesucevitz L, Wolozin B (2014) Regulation of autophagy by LRRK2 in Caenorhabditis elegans. Neurodegener Dis 13:110–113CrossRefGoogle Scholar
  61. Schmidt A, Wolde M, Thiele C, Fest W, Kratzin H, Podtelejnikov AV, Witke W, Huttner WB, Soling HD (1999) Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature 401:133–141CrossRefGoogle Scholar
  62. Schuske KR, Richmond JE, Matthies DS, Davis WS, Runz S, Rube DA, Van Der Bliek AM, Jorgensen EM (2003) Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40:749–762CrossRefGoogle Scholar
  63. Selkoe DJ (2002) Alzheimer’s disease is a synaptic failure. Science 298:789–791CrossRefGoogle Scholar
  64. Shen W, Ganetzky B (2009) Autophagy promotes synapse development in Drosophila. J Cell Biol 187:71–79CrossRefGoogle Scholar
  65. Shen DN, Zhang LH, Wei EQ, Yang Y (2015) Autophagy in synaptic development, function, and pathology. Neurosci Bull 31:416–426CrossRefGoogle Scholar
  66. Silva JM, Rodrigues S, Sampaio-Marques B, Gomes P, Neves-Carvalho A, Dioli C, Soares-Cunha C, Mazuik BF, Takashima A, Ludovico P, Wolozin B, Sousa N, Sotiropoulos I (2018) Dysregulation of autophagy and stress granule-related proteins in stress-driven Tau pathology. Cell Death Differ. Google Scholar
  67. Son JH, Shim JH, Kim KH, Ha JY, Han JY (2012) Neuronal autophagy and neurodegenerative diseases. Exp Mol Med 44:89–98CrossRefGoogle Scholar
  68. Soukup SF, Verstreken P (2017) EndoA/Endophilin-A creates docking stations for autophagic proteins at synapses. Autophagy 13:971–972CrossRefGoogle Scholar
  69. Soukup SF, Vanhauwaert R, Verstreken P (2018) Parkinson’s disease: convergence on synaptic homeostasis. EMBO J 37:e98960CrossRefGoogle Scholar
  70. Stavoe AK, Hill SE, Hall DH, Colon-Ramos DA (2016) KIF1A/UNC-104 transports ATG-9 to regulate neurodevelopment and autophagy at synapses. Dev Cell 38:171–185CrossRefGoogle Scholar
  71. Takagawa T, Kitani A, Fuss I, Levine B, Brant SR, Peter I, Tajima M, Nakamura S, Strober W (2018) An increase in LRRK2 suppresses autophagy and enhances Dectin-1-induced immunity in a mouse model of colitis. Sci Transl Med. Google Scholar
  72. Takahashi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y, Liang C, Jung JU, Cheng JQ, Mule JJ, Pledger WJ, Wang HG (2007) Bif-1 interacts with beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 9:1142–1151CrossRefGoogle Scholar
  73. Takahashi Y, Meyerkord CL, Wang HG (2008) BARgaining membranes for autophagosome formation: regulation of autophagy and tumorigenesis by Bif-1/endophilin B1. Autophagy 4:121–124CrossRefGoogle Scholar
  74. Takahashi Y, Meyerkord CL, Wang HG (2009) Bif-1/endophilin B1: a candidate for crescent driving force in autophagy. Cell Death Differ 16:947–955CrossRefGoogle Scholar
  75. Takahashi Y, Hori T, Cooper TK, Liao J, Desai N, Serfass JM, Young MM, Park S, Izu Y, Wang HG (2013) Bif-1 haploinsufficiency promotes chromosomal instability and accelerates Myc-driven lymphomagenesis via suppression of mitophagy. Blood 121:1622–1632CrossRefGoogle Scholar
  76. Tian Y, Chang JC, Fan EY, Flajolet M, Greengard P (2013) Adaptor complex AP2/PICALM, through interaction with LC3, targets Alzheimer’s APP-CTF for terminal degradation via autophagy. Proc Natl Acad Sci USA 110:17071–17076CrossRefGoogle Scholar
  77. Torres CA, Sulzer D (2012) Macroautophagy can press a brake on presynaptic neurotransmission. Autophagy 8:1540–1541CrossRefGoogle Scholar
  78. Uytterhoeven V, Lauwers E, Maes I, Miskiewicz K, Melo MN, Swerts J, Kuenen S, Wittocx R, Corthout N, Marrink SJ, Munck S, Verstreken P (2015) Hsc70-4 deforms membranes to promote synaptic protein turnover by endosomal microautophagy. Neuron 88:735–748CrossRefGoogle Scholar
  79. Vanhauwaert R, Kuenen S, Masius R, Bademosi A, Manetsberger J, Schoovaerts N, Bounti L, Gontcharenko S, Swerts J, Vilain S, Picillo M, Barone P, Munshi ST, De Vrij FM, Kushner SA, Gounko NV, Mandemakers W, Bonifati V, Meunier FA, Soukup SF, Verstreken P (2017) The SAC1 domain in synaptojanin is required for autophagosome maturation at presynaptic terminals. EMBO J 36:1392–1411CrossRefGoogle Scholar
  80. Vijayan V, Verstreken P (2017) Autophagy in the presynaptic compartment in health and disease. J Cell Biol 216:1895–1906CrossRefGoogle Scholar
  81. Wang Y, Nartiss Y, Steipe B, Mcquibban GA, Kim PK (2012) ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy. Autophagy 8:1462–1476CrossRefGoogle Scholar
  82. Wang DB, Uo T, Kinoshita C, Sopher BL, Lee RJ, Murphy SP, Kinoshita Y, Garden GA, Wang HG, Morrison RS (2014) Bax interacting factor-1 promotes survival and mitochondrial elongation in neurons. J Neurosci 34:2674–2683CrossRefGoogle Scholar
  83. Webb JL, Ravikumar B, Atkins J, Skepper JN, Rubinsztein DC (2003) Alpha-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem 278:25009–25013CrossRefGoogle Scholar
  84. Winckler B, Faundez V, Maday S, Cai Q, Guimas Almeida C, Zhang H (2018) The endolysosomal system and proteostasis: from development to degeneration. J Neurosci 38:9364–9374CrossRefGoogle Scholar
  85. Wong AS, Lee RH, Cheung AY, Yeung PK, Chung SK, Cheung ZH, Ip NY (2011) Cdk5-mediated phosphorylation of endophilin B1 is required for induced autophagy in models of Parkinson’s disease. Nat Cell Biol 13:568–579CrossRefGoogle Scholar
  86. Xu CY, Kang WY, Chen YM, Jiang TF, Zhang J, Zhang LN, Ding JQ, Liu J, Chen SD (2017) DJ-1 inhibits alpha-synuclein aggregation by regulating chaperone-mediated autophagy. Front Aging Neurosci 9:308CrossRefGoogle Scholar
  87. Xue Z, Zhang S, Huang L, He Y, Fang R, Fang Y (2013) Increased expression of beclin-1-dependent autophagy protects against beta-amyloid-induced cell injury in PC12 cells [corrected]. J Mol Neurosci 51:180–186CrossRefGoogle Scholar
  88. Yang Q, Mao Z (2010) Parkinson disease: a role for autophagy? Neuroscientist 16:335–341CrossRefGoogle Scholar
  89. Zare-Shahabadi A, Masliah E, Johnson GV, Rezaei N (2015) Autophagy in Alzheimer’s disease. Rev Neurosci 26:385–395CrossRefGoogle Scholar

Copyright information

© The Pharmaceutical Society of Korea 2019

Authors and Affiliations

  1. 1.Department of Neuroscience, Graduate SchoolKyung Hee UniversitySeoulSouth Korea
  2. 2.Department of Physiology, School of MedicineKyung Hee UniversitySeoulSouth Korea
  3. 3.Medical Research Center for Bioreaction to Reactive Oxygen Species and Biomedical Science Institute, School of MedicineKyung Hee UniversitySeoulSouth Korea

Personalised recommendations