VPS35 in dopamine neurons is required for endosome-to- golgi retrieval of Lamp2a, a receptor of chaperone- mediated autophagy that is critical for α-synuclein degradation and prevention of pathogenesis of Parkinson’s disease

Journal of Neuroscience

Volumn 35, Issue 29, 2015, Pages 10613-10628

  Tang, Fu Lei ^a,b   Erion, Joanna R ^a   Tian, Yun ^a,c   Liu, Wei ^a,d   Yin, Dong Min ^a   Ye, Jian ^d   Tang, Baisha ^c   Mei, Lin ^a,b   Xiong, Wen Cheng ^a,b  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c CENTRAL SOUTH UNIVERSITY   (China)

^d THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Autophagy; LAMP2a; Parkinson s disease; VPS35; synuclein

Indexed keywords

ALPHA SYNUCLEIN; BRAIN MONOAMINE; DOPAMINE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2A; MESSENGER RNA; MICRORNA; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING 35; VESICULAR TRANSPORT PROTEIN; VPS35 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHAPERONE-MEDIATED AUTOPHAGY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; ENDOSOME; GENETIC TRANSFECTION; GOLGI COMPLEX; GRIP STRENGTH; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; LATENT PERIOD; MALE; MOLECULAR CLONING; MORPHOGENESIS; MOTOR PERFORMANCE; MOUSE; MUSCLE STRENGTH; NEUROPATHOLOGY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA ISOLATION; SITE DIRECTED MUTAGENESIS; STEREOTACTIC PROCEDURE; SUBSTANTIA NIGRA PARS COMPACTA; WESTERN BLOTTING; ANIMAL; AUTOPHAGY; C57BL MOUSE; CELL CULTURE; CONFOCAL MICROSCOPY; METABOLISM; MUTANT MOUSE STRAIN; PARKINSONISM; PATHOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT;

ALPHA-SYNUCLEIN; ANIMALS; AUTOPHAGY; BLOTTING, WESTERN; CELLS, CULTURED; DOPAMINERGIC NEURONS; ENDOSOMES; GOLGI APPARATUS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICROSCOPY, CONFOCAL; MUTAGENESIS, SITE-DIRECTED; PARKINSONIAN DISORDERS; PROTEIN TRANSPORT; REAL-TIME POLYMERASE CHAIN REACTION; TRANSFECTION; VESICULAR TRANSPORT PROTEINS;

EID: 84937677490     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0042-15.2015     Document Type: Article

References (53)

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 67:1464-1472. CrossRef Medline
2. Belenkaya TY,WuY, Tang X, Zhou B, Cheng L, Sharma YV, Yan D, Selva EM, Lin X (2008) The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev Cell 14: 120-131. CrossRef Medline
3. Bonifacino JS, Hurley JH (2008) Retromer. Curr Opin Cell Biol 20:427- 436. CrossRef Medline
4. Chen D, Xiao H, Zhang K, Wang B, Gao Z, Jian Y, Qi X, Sun J, Miao L, Yang C (2010) Retromer is required for apoptotic cell clearance by phagocytic receptor recycling. Science 327:1261-1264. CrossRef Medline
5. Cuervo AM, Wong E (2014) Chaperone-mediated autophagy: roles in disease and aging. Cell Res 24:92-104. CrossRef Medline
6. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D (2004) Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 305:1292-1295. CrossRef Medline
7. Dhungel N, Eleuteri S, Li LB, Kramer NJ, Chartron JW, Spencer B, Kosberg K, Fields JA, Stafa K, Adame A, Lashuel H, Frydman J, Shen K, Masliah E, Gitler AD (2015) Parkinson's disease genes VPS35 and EIF4G1 interact genetically and converge on alpha-synuclein. Neuron 85:76-87. CrossRef Medline
8. Feinstein TN, Wehbi VL, Ardura JA, Wheeler DS, Ferrandon S, Gardella TJ, Vilardaga JP (2011) Retromer terminates the generation of cAMP by internalized PTH receptors. Nat Chem Biol 7:278 -284. CrossRef Medline
9. Follett J, Norwood SJ, Hamilton NA, Mohan M, Kovtun O, Tay S, Zhe Y,WoodSA, Mellick GD, Silburn PA, Collins BM, Bugarcic A, Teasdale RD (2014) The Vps35 D620N mutation linked to Parkinson's disease disrupts the cargo sorting function of retromer. Traffic 15:230-244. CrossRef Medline
10. Gasser T (2007) Update on the genetics of Parkinson's disease. Mov Disord 22 [Suppl 17]:S343-S350. CrossRef Medline
11. Huang X, Hartley AV, Yin Y, Herskowitz JH, Lah JJ, Ressler KJ (2013) AAV2 production with optimized N/P ratio and PEI-mediated transfection results in low toxicity and high titer for in vitro and in vivo applications. J Virol Methods 193:270 -277. CrossRef Medline
12. Kamp F, Exner N, Lutz AK, Wender N, Hegermann J, Brunner B, Nuscher B, Bartels T, Giese A, Beyer K, Eimer S, Winklhofer KF, Haass C (2010) Inhibition of mitochondrial fusion by alpha-synuclein is rescued by PINK1, Parkin and DJ-1. EMBO J 29:3571-3589. CrossRef Medline
13. Lee Y, Dawson VL, Dawson TM (2012) Animal models of Parkinson's disease: vertebrate genetics. Cold Spring Harb Perspect Med 2:a009324. CrossRef Medline
14. Lim KL, Ng XH, Grace LG, Yao TP (2012) Mitochondrial dynamics and Parkinson's disease: focus on parkin. Antioxid Redox Signal 16:935-949. CrossRef Medline
15. Lin X, Parisiadou L, Sgobio C, Liu G, Yu J, Sun L, Shim H, Gu XL, Luo J, Long CX, Ding J, Mateo Y, Sullivan PH,WuLG, Goldstein DS, Lovinger D, Cai H (2012) Conditional expression of Parkinson's disease-related mutant alpha-synuclein in the midbrain dopaminergic neurons causes progressive neurodegeneration and degradation of transcription factor nuclear receptor related 1. J Neurosci 32:9248 -9264. CrossRef Medline
16. Liu W, Tang FL, Erion J, Xiao H, Ye J, Xiong WC (2014) Vps35 haploinsufficiency results in degenerative-like deficit in mouse retinal ganglion neurons and impairment of optic nerve injury-induced gliosis. Mol Brain 7:10. CrossRef Medline
17. MacLeod DA, Rhinn H, Kuwahara T, Zolin A, Di Paolo G, McCabe BD, Marder KS, Honig LS, Clark LN, Small SA, AbeliovichA (2013) RAB7L1 interacts with LRRK2 to modify intraneuronal protein sorting and Parkinson's disease risk. Neuron 77:425-439. CrossRef Medline
18. Mak SK, McCormack AL, Manning-Bog AB, Cuervo AM, Di Monte DA (2010) Lysosomal degradation of alpha-synuclein in vivo. J Biol Chem 285:13621-13629. CrossRef Medline
19. Malkus KA, Ischiropoulos H (2012) Regional deficiencies in chaperonemediated autophagy underlie alpha-synuclein aggregation and neurodegeneration. Neurobiol Dis 46:732-744. CrossRef Medline
20. Mani M, Ryan TA (2009) Live imaging of synaptic vesicle release and retrieval in dopaminergic neurons. Front Neural Circuits 3:3. CrossRef Medline
21. Martinez-Vicente M, Talloczy Z, Kaushik S, Massey AC, Mazzulli J, Mosharov EV, Hodara R, Fredenburg R,WuDC, 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- 788. CrossRef Medline
22. McFarland NR, Lee JS, Hyman BT, McLean PJ (2009) Comparison of transduction efficiency of recombinant AAV serotypes 1, 2, 5, and 8 in the rat nigrostriatal system. J Neurochem 109:838-845. CrossRef Medline
23. Miura E, Hasegawa T, Konno M, Suzuki M, Sugeno N, Fujikake N, Geisler S, Tabuchi M, Oshima R, Kikuchi A, Baba T, Wada K, Nagai Y, Takeda A, Aoki M (2014) VPS35 dysfunction impairs lysosomal degradation of alpha-synuclein and exacerbates neurotoxicity in a Drosophila model of Parkinson's disease. Neurobiol Dis 71:1-13. CrossRef Medline
24. Munsie LN, Milnerwood AJ, Seibler P, Beccano-Kelly DA, Tatarnikov I, Khinda J, Volta M, Kadgien C, Cao LP, Tapia L, Klein C, Farrer MJ (2015) Retromer-dependent neurotransmitter receptor trafficking to synapses is altered by the Parkinson's disease VPS35 mutation p.D620N. Hum Mol Genet 24:1691-1703. CrossRef Medline
25. Murphy KE, Gysbers AM, Abbott SK, Spiro AS, Furuta A, Cooper A, Garner B, Kabuta T, HallidayGM (2015) Lysosomal-associated membrane protein 2 Isoforms are differentially affected in early Parkinson's disease.Mov Disord. Advance online publication. Retrieved January 16, 2015. doi: 10.1002/mds.26141. CrossRef
26. 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, CuervoAM (2013) Interplay of LRRK2 with chaperone-mediated autophagy. Nat Neurosci 16:394-406. CrossRef Medline
27. Pan CL, Baum PD, Gu M, Jorgensen EM, Clark SG, Garriga G (2008) C. elegans AP-2 and retromer control Wnt signaling by regulating mig-14/ Wntless. Dev Cell 14:132-139. CrossRef Medline
28. Perez RG, Waymire JC, Lin E, Liu JJ, Guo F, Zigmond MJ (2002) A role for alpha-synuclein in the regulation of dopamine biosynthesis. J Neurosci 22:3090 -3099. Medline
29. Qiao LY, Hamamichi S, Caldwell KA, Caldwell GA, Yacoubian TA, Wilson S, Xie ZL, Speake LD, Parks R, Crabtree D, Liang Q, Crimmins S, Schneider L, Uchiyama Y, Iwatsubo T, Zhou Y, Peng L, Lu Y, Standaert DG, Walls KC, et al. (2008) Lysosomal enzyme cathepsin D protects against alphasynuclein aggregation and toxicity. Mol Brain 1:17. CrossRef Medline
30. Rogaeva E, Meng Y, Lee JH, Gu Y, Kawarai T, Zou F, Katayama T, Baldwin CT, Cheng R, Hasegawa H, Chen F, Shibata N, Lunetta KL, Pardossi-Piquard R, Bohm C, Wakutani Y, Cupples LA, Cuenco KT, Green RC, Pinessi L, et al. (2007) The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. Nat Genet 39:168 -177. CrossRef Medline
31. Savitt JM, Dawson VL, DawsonTM (2006) Diagnosis and treatment of Parkinson disease: molecules to medicine. J Clin Invest 116:1744 -1754. CrossRef Medline
32. Seaman MN (2004) Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J Cell Biol 165:111-122. CrossRef Medline
33. Seaman MN (2005) Recycle your receptors with retromer. Trends Cell Biol 15:68 -75. CrossRef Medline
34. Small SA, Kent K, Pierce A,LeungC,KangMS,OkadaH,HonigL, Vonsattel JP,Kim TW (2005) Model-guided microarray implicates the retromer complex in Alzheimer's disease. Ann Neurol 58:909-919. CrossRef Medline
35. Tabuchi M, Yanatori I, Kawai Y, Kishi F (2010) Retromer-mediated direct sorting is required for proper endosomal recycling of the mammalian iron transporter DMT1. J Cell Sci 123:756 -766. CrossRef Medline
36. Temkin P, Lauffer B, Jäger S, Cimermancic P, Krogan NJ, von Zastrow M (2011) SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat Cell Biol 13:715-721. CrossRef Medline
37. van Weering JR, Verkade P, Cullen PJ (2010) SNX-BAR proteins in phosphoinositide-mediated, tubular-based endosomal sorting. Semin Cell Dev Biol 21:371-380. CrossRef Medline
38. Vieira SI, Rebelo S, Esselmann H, Wiltfang J, Lah J, Lane R, Small SA, Gandy S, da Cruz E Silva EF, da Cruz E Silva OA (2010) Retrieval of the Alzheimer's amyloid precursor protein from the endosome to the TGN is S655 phosphorylation state-dependent and retromer-mediated. Mol Neurodegener 5:40. CrossRef Medline
39. Vilarino-Guell C, Wider C, Ross OA, Dachsel JC, Kachergus JM, Lincoln SJ, Soto-Ortolaza AI, Cobb SA, Wilhoite GJ, Bacon JA, Behrouz B, Melrose HL, Hentati E, Puschmann A, Evans DM, Conibear E, Wasserman WW, Aasly JO, Burkhard PR, Djaldetti R, et al. (2011) VPS35 Mutations in Parkinson disease. Am J Hum Genet 89:162-167. CrossRef Medline
40. Vogiatzi T, Xilouri M, Vekrellis K, Stefanis L (2008) Wild type alpha-synuclein is degraded by chaperone-mediated autophagy and macroautophagy in neuronal cells. J Biol Chem 283:23542-23556. CrossRef Medline
41. vonCoelln R,ThomasB,AndrabiSA,LimKL,SavittJM,Saffary R, StirlingW,Bruno K, Hess EJ, Lee MK, Dawson VL, Dawson TM (2006) Inclusion body formation and neurodegeneration are parkin independent in a mouse model of alphasynucleinopathy. J Neurosci 26:3685-3696. CrossRef Medline
42. Wang CL, Tang FL, Peng Y, Shen CY, Mei L, Xiong WC (2012) VPS35 regulates developing mouse hippocampal neuronal morphogenesis by promoting retrograde trafficking of BACE1. Biol Open 1:1248 -1257. CrossRef Medline
43. 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 -25013. CrossRef Medline
44. Wen L, Tang FL, Hong Y, Luo SW, Wang CL, He W, Shen C, Jung JU, Xiong F, Lee DH, Zhang QG, Brann D, Kim TW, Yan R, Mei L, Xiong WC (2011) VPS35 haploinsufficiency increases Alzheimer's disease neuropathology. J Cell Biol 195:765-779. CrossRef Medline
45. Winslow AR, Chen CW, Corrochano S, Acevedo-Arozena A, Gordon DE, Peden AA, Lichtenberg M, Menzies FM, Ravikumar B, Imarisio S, Brown S, O'Kane CJ, Rubinsztein DC (2010) alpha-Synuclein impairs macroautophagy: implications for Parkinson's disease. J Cell Biol 190:1023- 1037. CrossRef Medline
46. Xia WF, Tang FL, Xiong L, Xiong S, Jung JU, Lee DH, Li XS, Feng X, Mei L, XiongWC (2013) Vps35 loss promotes hyperresorptive osteoclastogenesis and osteoporosis via sustained RANKL signaling. J Cell Biol 200:821- 837. CrossRef Medline
47. Xie Y, Ding YQ, Hong Y, Feng Z, Navarre S, Xi CX, Zhu XJ, Wang CL, Ackerman SL, Kozlowski D, Mei L, XiongWC (2005) Phosphatidylinositol transfer protein-alpha in netrin-1-induced PLC signalling and neurite outgrowth. Nat Cell Biol 7:1124 -1132. CrossRef Medline
48. Xilouri M, Brekk OR, Stefanis L (2013a) alpha-Synuclein and protein degradation systems: a reciprocal relationship. Mol Neurobiol 47:537-551. CrossRef Medline
49. Xilouri M, Brekk OR, Landeck N, Pitychoutis PM, Papasilekas T, Papadopoulou-Daifoti Z, KirikD,StefanisL (2013b) Boostingchaperone-mediatedautophagy in vivo mitigates alpha-synuclein-induced neurodegeneration. Brain 136:2130- 2146. CrossRef Medline
50. Yang PT, Lorenowicz MJ, Silhankova M, Coudreuse DY, Betist MC, KorswagenHC (2008) Wnt signaling requires retromer-dependent recycling of MIG-14/Wntless in Wnt-producing cells. Dev Cell 14:140-147. CrossRef Medline
51. Yin DM, Chen YJ, Lu YS, Bean JC, Sathyamurthy A, Shen C, Liu X, Lin TW, Smith CA, Xiong WC, Mei L (2013) Reversal of behavioral deficits and synaptic dysfunction in mice overexpressing neuregulin 1. Neuron 78: 644-657. CrossRef Medline
52. Yoshimori T, Yamamoto A, Moriyama Y, Futai M, Tashiro Y (1991) Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem 266:17707-17712. Medline
53. Zimprich A, Benet-Pagès A, Struhal W, Graf E, Eck SH, Offman MN, Haubenberger D, Spielberger S, Schulte EC, Lichtner P, Rossle SC, Klopp N, Wolf E, Seppi K, Pirker W, Presslauer S, Mollenhauer B, Katzenschlager R, Foki T, Hotzy C, et al. (2011) A mutation in VPS35, encoding a subunit of the retromer complex, causes late-onset Parkinson disease. Am J Hum Genet 89:168 -175. CrossRef Medline