Vacuolar protein sorting 35 (Vps35) rescues locomotor deficits and shortened lifespan in Drosophila expressing a Parkinson's disease mutant of Leucine-rich repeat kinase 2 (LRRK2)

Molecular Neurodegeneration

Volumn 9, Issue 1, 2014, Pages

  Linhart, Radek ^a   Wong, Sarah Anne ^a   Cao, Jieyun ^a   Tran, Melody ^a   Huynh, Anne ^a   Ardrey, Casey ^a   Park, Jong Min ^a   Hsu, Christine ^a   Taha, Saher ^a   Peterson, Rentia ^a   Shea, Shannon ^a   Kurian, Jason ^a   Venderova, Katerina ^a  

^a UNIVERSITY OF THE PACIFIC   (United States)

Author keywords

Drosophila; Endolysosomal pathway; Endosomes; Genetics; LRRK2; Lysosome; Neurodegeneration; Parkinson's disease; Retromer; Rotenone; VPS26; VPS35

Indexed keywords

LEUCINE RICH REPEAT KINASE 2; ROTENONE; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING 26; VACUOLAR PROTEIN SORTING 35; DROSOPHILA PROTEIN; LRRK2 PROTEIN, DROSOPHILA; PROTEIN SERINE THREONINE KINASE; VESICULAR TRANSPORT PROTEIN; VPS35 PROTEIN, DROSOPHILA;

ARTICLE; CELL SURFACE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DROSOPHILA; ENDOSOME; EYE; LIFESPAN; LOCOMOTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PARKINSON DISEASE; PARKINSONISM; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN TARGETING; TRANS GOLGI NETWORK; ANIMAL; DISEASE MODEL; DROSOPHILA MELANOGASTER; GENETICS; METABOLISM; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; PARKINSON DISEASE; PROTEIN-SERINE-THREONINE KINASES; VESICULAR TRANSPORT PROTEINS;

EID: 84906573100     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/1750-1326-9-23     Document Type: Article

References (60)

1. Impaired dopaminergic neurotransmission and microtubule-associated protein tau alterations in human LRRK2 transgenic mice. Melrose HL, Dachsel JC, Behrouz B, Lincoln SJ, Yue M, Hinkle KM, Kent CB, Korvatska E, Taylor JP, Witten L, Liang YQ, Beevers JE, Boules M, Dugger BN, Serna VA, Gaukhman A, Yu X, Castanedes-Casey M, Braithwaite AT, Ogholikhan S, Yu N, Bass D, Tyndall G, Schellenberg GD, Dickson DW, Janus C, Farrer MJ, Neurobiol Dis 2010 40 503 517
2. Leucine-rich repeat kinase 2 induces alpha-synuclein expression via the extracellular signal-regulated kinase pathway. Carballo-Carbajal I, Weber-Endress S, Rovelli G, Chan D, Wolozin B, Klein CL, Patenge N, Gasser T, Kahle PJ, Cell Signal 2010 22 821 827
3. Loss of leucine-rich repeat kinase 2 causes impairment of protein degradation pathways, accumulation of alpha-synuclein, and apoptotic cell death in aged mice. Tong Y, Yamaguchi H, Giaime E, Boyle S, Kopan R, Kelleher RJ 3rd, Shen J, Proc Natl Acad Sci U S A 2010 107 9879 9884
4. Leucine-rich repeat kinase 2 regulates the progression of neuropathology induced by Parkinson's-disease-related mutant alpha-synuclein. Lin X, Parisiadou L, Gu XL, Wang L, Shim H, Sun L, Xie C, Long CX, Yang WJ, Ding J, Chen ZZ, Gallant PE, Tao-Cheng JH, Rudow G, Troncoso JC, Liu Z, Li Z, Cai H, Neuron 2009 64 807 827
5. Parkinson's disease: insights from pathways. Cookson MR, Bandmann O, Hum Mol Genet 2010 19 21 R27
6. A drosophila model of Parkinson's disease. Feany MB, Bender WW, Nature 2000 404 394 398
7. What have we learned from Drosophila models of Parkinson's disease? Guo M, Prog Brain Res 2010 184 3 16
8. Parkinson's disease: insights from non-traditional model organisms. Pienaar IS, Gotz J, Feany MB, Prog Neurobiol 2010 92 558 571
9. Genome-wide screen for modifiers of ataxin-3 neurodegeneration in Drosophila. Bilen J, Bonini NM, PLoS Genet 2007 3 1950 1964
10. A genomic screen for modifiers of tauopathy identifies puromycin-sensitive aminopeptidase as an inhibitor of tau-induced neurodegeneration. Karsten SL, Sang TK, Gehman LT, Chatterjee S, Liu J, Lawless GM, Sengupta S, Berry RW, Pomakian J, Oh HS, Schulz C, Hui KS, Wiedau-Pazos M, Vinters HV, Binder LI, Geschwind DH, Jackson GR, Neuron 2006 51 549 560
11. Genome-wide screen for modifiers of Parkinson's disease genes in Drosophila. Fernandes C, Rao Y, Mol Brain 2011 4 17
12. Neurodegenerative models in Drosophila: polyglutamine disorders, Parkinson disease, and amyotrophic lateral sclerosis. Ambegaokar SS, Roy B, Jackson GR, Neurobiol Dis 2010 40 29 39
13. Leucine-Rich Repeat Kinase 2 interacts with Parkin, DJ-1 and PINK-1 in a Drosophila melanogaster model of Parkinson's disease. Venderova K, Kabbach G, Abdel-Messih E, Zhang Y, Parks RJ, Imai Y, Gehrke S, Ngsee J, Lavoie MJ, Slack RS, Rao Y, Zhang Z, Lu B, Haque ME, Park DS, Hum Mol Genet 2009 18 4390 4404
14. Activation of FoxO by LRRK2 induces expression of proapoptotic proteins and alters survival of postmitotic dopaminergic neuron in Drosophila. Kanao T, Venderova K, Park DS, Unterman T, Lu B, Imai Y, Hum Mol Genet 2010 19 3747 3758
15. Dopaminergic expression of the Parkinsonian gene LRRK2-G2019S leads to non-autonomous visual neurodegeneration, accelerated by increased neural demands for energy. Hindle S, Afsari F, Stark M, Middleton CA, Evans GJ, Sweeney ST, Elliott CJ, Hum Mol Genet 2013 22 2129 2140
16. A Drosophila model for LRRK2-linked parkinsonism. Liu Z, Wang X, Yu Y, Li X, Wang T, Jiang H, Ren Q, Jiao Y, Sawa A, Moran T, Ross CA, Montell C, Smith WW, Proc Natl Acad Sci U S A 2008 105 2693 2698
17. Leucine-rich repeat kinase 2 (LRRK2) interacts with parkin, and mutant LRRK2 induces neuronal degeneration. Smith WW, Pei Z, Jiang H, Moore DJ, Liang Y, West AB, Dawson VL, Dawson TM, Ross CA, Proc Natl Acad Sci U S A 2005 102 18676 18681
18. Parkin protects against LRRK2 G2019S mutant-induced dopaminergic neurodegeneration in Drosophila. Ng CH, Mok SZ, Koh C, Ouyang X, Fivaz ML, Tan EK, Dawson VL, Dawson TM, Yu F, Lim KL, J Neurosci 2009 29 11257 11262
19. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Brand AH, Perrimon N, Development 1993 118 401 415
20. RNAi screening in Drosophila cells identifies new modifiers of mutant huntingtin aggregation. Doumanis J, Wada K, Kino Y, Moore AW, Nukina N, PLoS One 2009 4 7275
21. An over-expression system for characterizing Ppt1 function in Drosophila. Korey CA, MacDonald ME, BMC Neurosci 2003 4 30
22. Genetic screen identifies serpin5 as a regulator of the toll pathway and CHMP2B toxicity associated with frontotemporal dementia. Ahmad ST, Sweeney ST, Lee JA, Sweeney NT, Gao FB, Proc Natl Acad Sci U S A 2009 106 12168 12173
23. Antioxidants protect PINK1-dependent dopaminergic neurons in Drosophila. Wang D, Qian L, Xiong H, Liu J, Neckameyer WS, Oldham S, Xia K, Wang J, Bodmer R, Zhang Z, Proc Natl Acad Sci U S A 2006 103 13520 13525
24. A Drosophila model for TDP-43 proteinopathy. Li Y, Ray P, Rao EJ, Shi C, Guo W, Chen X, Woodruff EA 3rd, Fushimi K, Wu JY, Proc Natl Acad Sci U S A 2010 107 3169 3174
25. Inhibitors of LRRK2 kinase attenuate neurodegeneration and Parkinson-like phenotypes in Caenorhabditis elegans and Drosophila Parkinson's disease models. Liu Z, Hamamichi S, Lee BD, Yang D, Ray A, Caldwell GA, Caldwell KA, Dawson TM, Smith WW, Dawson VL, Hum Mol Genet 2011 20 3933 3942
26. Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Paisan-Ruiz C, Jain S, Evans EW, Gilks WP, Simon J, van der Brug M, Lopez de Munain A, Aparicio S, Gil AM, Khan N, Johnson J, Martinez JR, Nicholl D, Carrera IM, Pena AS, de Silva R, Lees A, Marti-Masso JF, Perez-Tur J, Wood NW, Singleton AB, Neuron 2004 44 595 600
27. Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Zimprich A, Biskup S, Leitner P, Lichtner P, Farrer M, Lincoln S, Kachergus J, Hulihan M, Uitti RJ, Calne DB, Stoessl AJ, Pfeiffer RF, Patenge N, Carbajal IC, Vieregge P, Asmus F, Muller-Myhsok B, Dickson DW, Meitinger T, Strom TM, Wszolek ZK, Gasser T, Neuron 2004 44 601 607
28. The genetics of Parkinson's disease: progress and therapeutic implications. Singleton AB, Farrer MJ, Bonifati V, Mov Disord 2013 28 14 23
29. Animal models of Parkinson's disease. Jackson-Lewis V, Blesa J, Przedborski S, Parkinsonism Relat Disord 2012 18 Suppl 1 183 S185
30. GTPase activity plays a key role in the pathobiology of LRRK2. Xiong Y, Coombes CE, Kilaru A, Li X, Gitler AD, Bowers WJ, Dawson VL, Dawson TM, Moore DJ, PLoS Genet 2010 6 1000902
31. LRRK2 controls synaptic vesicle storage and mobilization within the recycling pool. Piccoli G, Condliffe SB, Bauer M, Giesert F, Boldt K, De Astis S, Meixner A, Sarioglu H, Vogt-Weisenhorn DM, Wurst W, Gloeckner CJ, Matteoli M, Sala C, Ueffing M, J Neurosci 2011 31 2225 2237
32. LRK-1, a C. elegans PARK8-related kinase, regulates axonal-dendritic polarity of SV proteins. Sakaguchi-Nakashima A, Meir JY, Jin Y, Matsumoto K, Hisamoto N, Curr Biol 2007 17 592 598
33. LRRK2 regulates synaptic vesicle endocytosis. Shin N, Jeong H, Kwon J, Heo HY, Kwon JJ, Yun HJ, Kim CH, Han BS, Tong Y, Shen J, Hatano T, Hattori N, Kim KS, Chang S, Seol W, Exp Cell Res 2008 314 2055 2065
34. The familial Parkinsonism gene LRRK2 regulates neurite process morphology. MacLeod D, Dowman J, Hammond R, Leete T, Inoue K, Abeliovich A, Neuron 2006 52 587 593
35. Role of autophagy in G2019S-LRRK2-associated neurite shortening in differentiated SH-SY5Y cells. Plowey ED, Cherra SJ 3rd, Liu YJ, Chu CT, J Neurochem 2008 105 1048 1056
36. VPS35 mutations in Parkinson disease. 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, Ghika J, Hentati F, Krygowska-Wajs A, Lynch T, Melamed E, Rajput A, Rajput AH, Solida A, Wu RM, Uitti RJ, et al. Am J Hum Genet 2011 89 162 167
37. A mutation in VPS35, encoding a subunit of the retromer complex, causes late-onset Parkinson disease. Zimprich A, Benet-Pages 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, Reinthaler E, Harutyunyan A, Kralovics R, Peters A, Zimprich F, Brucke T, Poewe W, Auff E, Trenkwalder C, Rost B, et al. Am J Hum Genet 2011 89 168 175
38. Identification of VPS35 mutations replicated in French families with Parkinson disease. Lesage S, Condroyer C, Klebe S, Honore A, Tison F, Brefel-Courbon C, Durr A, Brice A, French Parkinson's Disease Genetics Study G, Neurology 2012 78 1449 1450
39. Frequency of the D620N mutation in VPS35 in Parkinson disease. Kumar KR, Weissbach A, Heldmann M, Kasten M, Tunc S, Sue CM, Svetel M, Kostic VS, Segura-Aguilar J, Ramirez A, Simon DK, Vieregge P, Munte TF, Hagenah J, Klein C, Lohmann K, Arch Neurol 2012 69 1360 1364
40. VPS35 mutation in Japanese patients with typical Parkinson's disease. Ando M, Funayama M, Li Y, Kashihara K, Murakami Y, Ishizu N, Toyoda C, Noguchi K, Hashimoto T, Nakano N, Simon DK, Vieregge P, Munte TF, Hagenah J, Klein C, Lohmann K, Mov Disord 2012 27 1413 1417
41. A multi-centre clinico-genetic analysis of the VPS35 gene in Parkinson disease indicates reduced penetrance for disease-associated variants. Sharma M, Ioannidis JP, Aasly JO, Annesi G, Brice A, Bertram L, Bozi M, Barcikowska M, Crosiers D, Clarke CE, Facheris MF, Farrer M, Garraux G, Gispert S, Auburger G, Vilarino-Guell C, Hadjigeorgiou GM, Hicks AA, Hattori N, Jeon BS, Jamrozik Z, Krygowska-Wajs A, Lesage S, Lill CM, Lin JJ, Lynch T, Lichtner P, Lang AE, Libioulle C, Murata M, et al. J Med Genet 2012 49 721 726
42. Whole exome sequencing of rare variants in EIF4G1 and VPS35 in Parkinson disease. Nuytemans K, Bademci G, Inchausti V, Dressen A, Kinnamon DD, Mehta A, Wang L, Zuchner S, Beecham GW, Martin ER, Scott WK, Vance JM, Neurology 2013 80 982 989
43. Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. Arighi CN, Hartnell LM, Aguilar RC, Haft CR, Bonifacino JS, J Cell Biol 2004 165 123 133
44. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. Seaman MN, J Cell Biol 2004 165 111 122
45. Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35: assembly into multimeric complexes. Haft CR, de la Luz SM, Bafford R, Lesniak MA, Barr VA, Taylor SI, Mol Biol Cell 2000 11 4105 4116
46. Endosome-to-Golgi transport pathways in physiological processes. Lieu ZZ, Gleeson PA, Histol Histopathol 2011 26 395 408
47. A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. Seaman MN, McCaffery JM, Emr SD, J Cell Biol 1998 142 665 681
48. A loss-of-function screen reveals SNX5 and SNX6 as potential components of the mammalian retromer. Wassmer T, Attar N, Bujny MV, Oakley J, Traer CJ, Cullen PJ, J Cell Sci 2007 120 45 54
49. SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Temkin P, Lauffer B, Jager S, Cimermancic P, Krogan NJ, von Zastrow M, Nat Cell Biol 2011 13 715 721
50. Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. Seaman MN, J Cell Sci 2007 120 2378 2389
51. The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. 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, Rainero I, Sorbi S, Bruni A, Duara R, Friedland RP, Inzelberg R, Hampe W, Bujo H, Song YQ, Andersen OM, et al. Nat Genet 2007 39 168 177
52. Genomic convergence to identify candidate genes for Alzheimer disease on chromosome 10. Liang X, Slifer M, Martin ER, Schnetz-Boutaud N, Bartlett J, Anderson B, Zuchner S, Gwirtsman H, Gilbert JR, Pericak-Vance MA, Haines JL, Hum Mutat 2009 30 463 471
53. Loss of apolipoprotein E receptor LR11 in Alzheimer disease. Scherzer CR, Offe K, Gearing M, Rees HD, Fang G, Heilman CJ, Schaller C, Bujo H, Levey AI, Lah JJ, Arch Neurol 2004 61 1200 1205
54. BACE1 retrograde trafficking is uniquely regulated by the cytoplasmic domain of sortilin. Finan GM, Okada H, Kim TW, J Biol Chem 2011 286 12602 12616
55. Retromer deficiency observed in Alzheimer's disease causes hippocampal dysfunction, neurodegeneration, and Abeta accumulation. Muhammad A, Flores I, Zhang H, Yu R, Staniszewski A, Planel E, Herman M, Ho L, Kreber R, Honig LS, Ganetzky B, Duff K, Arancio O, Small SA, Proc Natl Acad Sci U S A 2008 105 7327 7332
56. Retromer disruption promotes amyloidogenic APP processing. Sullivan CP, Jay AG, Stack EC, Pakaluk M, Wadlinger E, Fine RE, Wells JM, Morin PJ, Neurobiol Dis 2011 43 338 345
57. RAB7L1 interacts with LRRK2 to modify intraneuronal protein sorting and Parkinson's disease risk. Macleod DA, Rhinn H, Kuwahara T, Zolin A, Di Paolo G, Maccabe BD, Marder KS, Honig LS, Clark LN, Small SA, Abeliovich A, Neuron 2013 77 425 439
58. Pathogenic mutation in VPS35 impairs its protection against MPP(+) cytotoxicity. Bi F, Li F, Huang C, Zhou H, Int J Biol Sci 2013 9 149 155
59. Drosophila Vps35 function is necessary for normal endocytic trafficking and actin cytoskeleton organisation. Korolchuk VI, Schutz MM, Gomez-Llorente C, Rocha J, Lansu NR, Collins SM, Wairkar YP, Robinson IM, O'Kane CJ, J Cell Sci 2007 120 4367 4376
60. The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Bellen HJ, Levis RW, Liao G, He Y, Carlson JW, Tsang G, Evans-Holm M, Hiesinger PR, Schulze KL, Rubin GM, Hoskins RA, Spradling AC, Genetics 2004 167 761 781