Roles of the Drosophila LRRK2 homolog in Rab7-dependent lysosomal positioning

Human Molecular Genetics

Volumn 21, Issue 6, 2012, Pages 1350-1363

  Dodson, Mark W ^a,b   Zhang, Ting ^a,b,c   Jiang, Changan ^a,d   Chen, Shengdi ^c   Guo, Ming ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

^d SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; LEUCINE RICH REPEAT KINASE 2; RAB7 PROTEIN;

ALLELE; ARTICLE; DROSOPHILA; ENDOSOME; FEMALE FERTILITY; GENE CONTROL; GENE INTERACTION; GENE MUTATION; LYSOSOME; MICROTUBULE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SEQUENCE HOMOLOGY;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, WESTERN; CELLS, CULTURED; DROSOPHILA; DROSOPHILA PROTEINS; ENDOSOMES; FEMALE; FERTILITY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOPRECIPITATION; LYSOSOMES; MALE; MUTATION; PROTEIN-SERINE-THREONINE KINASES; RAB GTP-BINDING PROTEINS;

EID: 84863241584     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr573     Document Type: Article

References (76)

1. Paisan-Ruiz, C., Jain, S., Evans, E.W., Gilks, W.P., Simon, J., van der Brug, M., Lopz de Munain, A., Aparicio, S., Gil, A.M., Khan, N. et al. (2004) Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Neuron, 44, 595-600.
2. Zimprich, A., Biskup, S., Leitner, P., Lichtner, P., Farrer, M., Lincoln, S., Kachergus, J., Hulihan, M., Uitti, R.J., Calne, D.B. et al. (2004) Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron, 44, 601-607.
3. Satake, W., Nakabayashi, Y., Mizuta, I., Hirota, Y., Ito, C., Kubo, M., Kawaguchi, T., Tsunoda, T., Watanabe, M., Takeda, A. et al. (2009) Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson's disease. Nat. Genet., 41, 1303-1307.
4. Simon-Sanchez, J., Schulte, C., Bras, J.M., Sharma, M., Gibbs, J.R., Berg, D., Paisan-Ruiz, C., Lichtner, P., Scholz, S.W., Hernandez, D.G. et al. (2009) Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nat. Genet., 41, 1308-1312.
5. Lesage, S., Ibanez, P., Lohmann, E., Pollak, P., Tison, F., Tazir, M., Leutenegger, A.L., Guimaraes, J., Bonnet, A.M., Agid, Y. et al. (2005) G2019S LRRK2 mutation in French and North African families with Parkinson's disease. Ann. Neurol., 58, 784-787.
6. Hardy, J. (2010) Genetic analysis of pathways to Parkinson disease. Neuron, 68, 201-206.
7. Dawson, T.M., Ko, H.S. and Dawson, V.L. (2010) Genetic animal models of Parkinson's disease. Neuron, 66, 646-661.
8. Bosgraaf, L. and Van Haastert, P.J. (2003) Roc, a Ras/GTPase domain in complex proteins. Biochim. Biophys. Acta, 1643, 5-10.
9. Cookson, M.R. (2010) The role of leucine-rich repeat kinase 2 (LRRK2) in Parkinson's disease. Nat. Rev. Neurosci., 11, 791-797.
10. Smith, W.W., Pei, Z., Jiang, H., Moore, D.J., Liang, Y., West, A.B., Dawson, V.L., Dawson, T.M. and Ross, C.A. (2005) Leucine-rich repeat kinase 2 (LRRK2) interacts with parkin, and mutant LRRK2 induces neuronal degeneration. Proc. Natl Acad. Sci. USA, 102, 18676-18681.
11. Kanao, T., Venderova, K., Park, D.S., Unterman, T., Lu, B. and Imai, Y. (2010) Activation of FoxO by LRRK2 induces expression of proapoptotic proteins and alters survival of postmitotic dopaminergic neuron in Drosophila. Hum. Mol. Genet., 19, 3747-3758.
12. 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.
13. Gehrke, S., Imai, Y., Sokol, N. and Lu, B. (2010) Pathogenic LRRK2 negatively regulates microRNA-mediated translational repression. Nature, 466, 637-641.
14. Sakaguchi-Nakashima, A., Meir, J.Y., Jin, Y., Matsumoto, K. and Hisamoto, N. (2007) LRK-1, a C. elegans PARK8-related kinase, regulates axonal-dendritic polarity of SV proteins. Curr. Biol., 17, 592-598.
15. Ho, C.C., Rideout, H.J., Ribe, E., Troy, C.M. and Dauer, W.T. (2009) The Parkinson disease protein leucine-rich repeat kinase 2 transduces death signals via Fas-associated protein with death domain and caspase-8 in a cellular model of neurodegeneration. J. Neurosci., 29, 1011-1016.
16. Jaleel, M., Nichols, R.J., Deak, M., Campbell, D.G., Gillardon, F., Knebel, A. and Alessi, D.R. (2007) LRRK2 phosphorylates moesin at threonine-558: characterization of how Parkinson's disease mutants affect kinase activity. Biochem. J., 405, 307-317.
17. Parisiadou, L., Xie, C., Cho, H.J., Lin, X., Gu, X.L., Long, C.X., Lobbestael, E., Baekelandt, V., Taymans, J.M., Sun, L. et al. (2009) Phosphorylation of ezrin/radixin/moesin proteins by LRRK2 promotes the rearrangement of actin cytoskeleton in neuronal morphogenesis. J. Neurosci., 29, 13971-13980.
18. Gandhi, P.N., Wang, X., Zhu, X., Chen, S.G. and Wilson-Delfosse, A.L. (2008) The Roc domain of leucine-rich repeat kinase 2 is sufficient for interaction with microtubules. J. Neurosci. Res., 86, 1711-1720.
19. Gillardon, F. (2009) Leucine-rich repeat kinase 2 phosphorylates brain tubulin-beta isoforms and modulates microtubule stability-a point of convergence in parkinsonian neurodegeneration? J. Neurochem., 110, 1514-1522.
20. Lin, X., Parisiadou, L., Gu, X.L., Wang, L., Shim, H., Sun, L., Xie, C., Long, C.X., Yang, W.J., Ding, J. et al. (2009) Leucine-rich repeat kinase 2 regulates the progression of neuropathology induced by Parkinson's-disease-related mutant alpha-synuclein. Neuron, 64, 807-827.
21. West, A.B., Moore, D.J., Biskup, S., Bugayenko, A., Smith, W.W., Ross, C.A., Dawson, V.L. and Dawson, T.M. (2005) Parkinson's disease-associated mutations in leucine-rich repeat kinase 2 augment kinase activity. Proc. Natl Acad. Sci. USA, 102, 16842-16847.
22. Biskup, S., Moore, D.J., Celsi, F., Higashi, S., West, A.B., Andrabi, S.A., Kurkinen, K., Yu, S.W., Savitt, J.M., Waldvogel, H.J. et al. (2006) Localization of LRRK2 to membranous and vesicular structures in mammalian brain. Ann. Neurol., 60, 557-569.
23. Gloeckner, C.J., Kinkl, N., Schumacher, A., Braun, R.J., O'Neill, E., Meitinger, T., Kolch, W., Prokisch, H. and Ueffing, M. (2006) The Parkinson disease causing LRRK2 mutation I2020T is associated with increased kinase activity. Hum. Mol. Genet., 15, 223-232.
24. Hatano, T., Kubo, S., Imai, S., Maeda, M., Ishikawa, K., Mizuno, Y. and Hattori, N. (2007) Leucine-rich repeat kinase 2 associates with lipid rafts. Hum. Mol. Genet., 16, 678-690.
25. Vitte, J., Traver, S., Maues De Paula, A., Lesage, S., Rovelli, G., Corti, O., Duyckaerts, C. and Brice, A. (2010) Leucine-rich repeat kinase 2 is associated with the endoplasmic reticulum in dopaminergic neurons and accumulates in the core of Lewy bodies in Parkinson disease. J. Neuropathol. Exp. Neurol., 69, 959-972.
26. Alegre-Abarrategui, J., Christian, H., Lufino, M.M., Mutihac, R., Venda, L.L., Ansorge, O. and Wade-Martins, R. (2009) LRRK2 regulates autophagic activity and localizes to specific membrane microdomains in a novel human genomic reporter cellular model. Hum. Mol. Genet., 18, 4022-4034.
27. Berger, Z., Smith, K.A. and Lavoie, M.J. (2010) Membrane localization of LRRK2 is associated with increased formation of the highly active LRRK2 dimer and changes in its phosphorylation. Biochemistry, 49, 5511-5523.
28. Shin, N., Jeong, H., Kwon, J., Heo, H.Y., Kwon, J.J., Yun, H.J., Kim, C.H., Han, B.S., Tong, Y., Shen, J. et al. (2008) LRRK2 regulates synaptic vesicle endocytosis. Exp. Cell Res., 314, 2055-2065.
29. Higashi, S., Moore, D.J., Yamamoto, R., Minegishi, M., Sato, K., Togo, T., Katsuse, O., Uchikado, H., Furukawa, Y., Hino, H. et al. (2009) Abnormal localization of leucine-rich repeat kinase 2 to the endosomal-lysosomal compartment in lewy body disease. J. Neuropathol. Exp. Neurol., 68, 994-1005.
30. Piccoli, G., Condliffe, S.B., Bauer, M., Giesert, F., Boldt, K., De Astis, S., Meixner, A., Sarioglu, H., Vogt-Weisenhorn, D.M., Wurst, W. et al. (2011) LRRK2 controls synaptic vesicle storage and mobilization within the recycling pool. J. Neurosci., 31, 2225-2237.
31. Xiong, Y., Coombes, C.E., Kilaru, A., Li, X., Gitler, A.D., Bowers, W.J., Dawson, V.L., Dawson, T.M. and Moore, D.J. (2010) GTPase activity plays a key role in the pathobiology of LRRK2. PLoS Genet., 6, e1000902.
32. MacLeod, D., Dowman, J., Hammond, R., Leete, T., Inoue, K. and Abeliovich, A. (2006) The familial Parkinsonism gene LRRK2 regulates neurite process morphology. Neuron, 52, 587-593.
33. Tong, Y., Yamaguchi, H., Giaime, E., Boyle, S., Kopan, R., Kelleher, R.J. 3rd and Shen, J. (2010) Loss of leucine-rich repeat kinase 2 causes impairment of protein degradation pathways, accumulation of alpha-synuclein, and apoptotic cell death in aged mice. Proc. Natl Acad. Sci. USA, 107, 9879-9884.
34. Lessing, D. and Bonini, N.M. (2009) Maintaining the brain: insight into human neurodegeneration from Drosophila melanogaster mutants. Nat. Rev. Genet., 10, 359-370.
35. Dodson, M.W. and Guo, M. (2007) Pink1, Parkin, DJ-1 and mitochondrial dysfunction in Parkinson's disease. Curr. Opin. Neurobiol., 17, 331-337.
36. Guo, M. (2010) What have we learned from Drosophila models of Parkinson's disease. Prog. Brain Res., 184, 3-16.
37. Lee, S.B., Kim, W., Lee, S. and Chung, J. (2007) Loss of LRRK2/PARK8 induces degeneration of dopaminergic neurons in Drosophila. Biochem. Biophys. Res. Commun., 358, 534-539.
38. Wang, D., Tang, B., Zhao, G., Pan, Q., Xia, K., Bodmer, R. and Zhang, Z. (2008) Dispensable role of Drosophila ortholog of LRRK2 kinase activity in survival of dopaminergic neurons. Mol. Neurodegener., 3, 3.
39. Lee, S., Liu, H.P., Lin, W.Y., Guo, H. and Lu, B. (2010) LRRK2 kinase regulates synaptic morphology through distinct substrates at the presynaptic and postsynaptic compartments of the Drosophila neuromuscular junction. J. Neurosci., 30, 16959-16969.
40. Liu, Z., Wang, X., Yu, Y., Li, X., Wang, T., Jiang, H., Ren, Q., Jiao, Y., Sawa, A., Moran, T. et al. (2008) A Drosophila model for LRRK2-linked parkinsonism. Proc. Natl Acad. Sci. USA, 105, 2693-2698.
41. Lin, C.H., Tsai, P.I., Wu, R.M. and Chien, C.T. (2010) LRRK2 G2019S mutation induces dendrite degeneration through mislocalization and phosphorylation of tau by recruiting autoactivated GSK3ss. J. Neurosci., 30, 13138-13149.
42. Spradling, A.C. (1993) In Arias, M.B.a.A.M. (ed.), The Development of Drosophila Melanogaster. Cold Spring Harbor Laboratory Press, Plainview, NY, Vol. I, pp. 1-70.
43. Chavrier, P., Parton, R.G., Hauri, H.P., Simons, K. and Zerial, M. (1990) Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell, 62, 317-329.
44. Lombardi, D., Soldati, T., Riederer, M.A., Goda, Y., Zerial, M. and Pfeffer, S.R. (1993) Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J., 12, 677-682.
45. Rohrer, J., Schweizer, A., Russell, D. and Kornfeld, S. (1996) The targeting of Lamp1 to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane. J. Cell Biol., 132, 565-576.
46. Pulipparacharuvil, S., Akbar, M.A., Ray, S., Sevrioukov, E.A., Haberman, A.S., Rohrer, J. and Kramer, H. (2005) Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules. J. Cell Sci., 118, 3663-3673.
47. Wucherpfennig, T., Wilsch-Brauninger, M. and Gonzalez-Gaitan, M. (2003) Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol., 161, 609-624.
48. Komada, M., Masaki, R., Yamamoto, A. and Kitamura, N. (1997) Hrs, a tyrosine kinase substrate with a conserved double zinc finger domain, is localized to the cytoplasmic surface of early endosomes. J. Biol. Chem., 272, 20538-20544.
49. Urbe, S., Mills, I.G., Stenmark, H., Kitamura, N. and Clague, M.J. (2000) Endosomal localization and receptor dynamics determine tyrosine phosphorylation of hepatocyte growth factor-regulated tyrosine kinase substrate. Mol. Cell Biol., 20, 7685-7692.
50. Bache, K.G., Brech, A., Mehlum, A. and Stenmark, H. (2003) Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J. Cell Biol., 162, 435-442.
51. Urbe, S., Huber, L.A., Zerial, M., Tooze, S.A. and Parton, R.G. (1993) Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells. FEBS Lett., 334, 175-182.
52. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M. and Parton, R.G. (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol., 135, 913-924.
53. Pilling, A.D., Horiuchi, D., Lively, C.M. and Saxton, W.M. (2006) Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol. Biol. Cell, 17, 2057-2068.
54. Kondylis, V., Spoorendonk, K.M. and Rabouille, C. (2005) dGRASP localization and function in the early exocytic pathway in Drosophila S2 cells. Mol. Biol. Cell, 16, 4061-4072.
55. Bucci, C., Thomsen, P., Nicoziani, P., McCarthy, J. and van Deurs, B. (2000) Rab7: a key to lysosome biogenesis. Mol. Biol. Cell, 11, 467-480.
56. Jordens, I., Fernandez-Borja, M., Marsman, M., Dusseljee, S., Janssen, L., Calafat, J., Janssen, H., Wubbolts, R. and Neefjes, J. (2001) The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol., 11, 1680-1685.
57. Cantalupo, G., Alifano, P., Roberti, V., Bruni, C.B. and Bucci, C. (2001) Rab-interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes. EMBO J., 20, 683-693.
58. Johansson, M., Rocha, N., Zwart, W., Jordens, I., Janssen, L., Kuijl, C., Olkkonen, V.M. and Neefjes, J. (2007) Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor betalll spectrin. J. Cell Biol., 176, 459-471.
59. Korolchuk, V.I., Saiki, S., Lichtenberg, M., Siddiqi, F.H., Roberts, E.A., Imarisio, S., Jahreiss, L., Sarkar, S., Futter, M., Menzies, F.M. et al. (2011) Lysosomal positioning coordinates cellular nutrient responses. Nat. Cell Biol., 13, 453-460.
60. Taylor, J.P., Mata, I.F. and Farrer, M.J. (2006) LRRK2: a common pathway for parkinsonism, pathogenesis and prevention? Trends Mol. Med., 12, 76-82.
61. Bonifati, V. (2007) LRRK2 low-penetrance mutations (Gly2019Ser) and risk alleles (Gly2385Arg)-linking familial and sporadic Parkinson's disease. Neurochem. Res., 32, 1700-1708.
62. Greggio, E., Jain, S., Kingsbury, A., Bandopadhyay, R., Lewis, P., Kaganovich, A., van der Brug, M.P., Beilina, A., Blackinton, J., Thomas, K.J. et al. (2006) Kinase activity is required for the toxic effects of mutant LRRK2/dardarin. Neurobiol. Dis., 23, 329-341.
63. West, A.B., Moore, D.J., Choi, C., Andrabi, S.A., Li, X., Dikeman, D., Biskup, S., Zhang, Z., Lim, K.L., Dawson, V.L. et al. (2007) Parkinson's disease-associated mutations in LRRK2 link enhanced GTP-binding and kinase activities to neuronal toxicity. Hum. Mol. Genet., 16, 223-232.
64. Chu, Y., Dodiya, H., Aebischer, P., Olanow, C.W. and Kordower, J.H. (2009) Alterations in lysosomal and proteasomal markers in Parkinson's disease: relationship to alpha-synuclein inclusions. Neurobiol. Dis., 35, 385-398.
65. Dehay, B., Bove, J., Rodriguez-Muela, N., Perier, C., Recasens, A., Boya, P. and Vila, M. (2010) Pathogenic lysosomal depletion in Parkinson's disease. J. Neurosci., 30, 12535-12544.
66. Aharon-Peretz, J., Rosenbaum, H. and Gershoni-Baruch, R. (2004) Mutations in the glucocerebrosidase gene and Parkinson's disease in Ashkenazi Jews. N. Engl. J. Med., 351, 1972-1977.
67. Gan-Or, Z., Giladi, N., Rozovski, U., Shifrin, C., Rosner, S., Gurevich, T., Bar-Shira, A. and Orr-Urtreger, A. (2008) Genotype-phenotype correlations between GBA mutations and Parkinson disease risk and onset. Neurology, 70, 2277-2283.
68. Ramirez, A., Heimbach, A., Grundemann, J., Stiller, B., Hampshire, D., Cid, L.P., Goebel, I., Mubaidin, A.F., Wriekat, A.L., Roeper, J. et al. (2006) Hereditary parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5 P-type ATPase. Nat. Genet., 38, 1184-1191.
69. Wurmser, A.E., Sato, T.K. and Emr, S.D. (2000) New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. J. Cell Biol., 151, 551-562.
70. Lee, B.D., Shin, J.H., VanKampen, J., Petrucelli, L., West, A.B., Ko, H.S., Lee, Y.I., Maguire-Zeiss, K.A., Bowers, W.J., Federoff, H.J. et al. (2010) Inhibitors of leucine-rich repeat kinase-2 protect against models of Parkinson's disease. Nat. Med., 16, 998-1000.
71. Kawauchi, T., Sekine, K., Shikanai, M., Chihama, K., Tomita, K., Kubo, K., Nakajima, K., Nabeshima, Y. and Hoshino, M. (2010) Rab GTPases-dependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron, 67, 588-602.
72. Saxena, S., Bucci, C., Weis, J. and Kruttgen, A. (2005) The small GTPase Rab7 controls the endosomal trafficking and neuritogenic signaling of the nerve growth factor receptor TrkA. J. Neurosci., 25, 10930-10940.
73. Deinhardt, K., Salinas, S., Verastegui, C., Watson, R., Worth, D., Hanrahan, S., Bucci, C. and Schiavo, G. (2006) Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron, 52, 293-305.
74. Verhoeven, K., De Jonghe, P., Coen, K., Verpoorten, N., Auer-Grumbach, M., Kwon, J.M., FitzPatrick, D., Schmedding, E., De Vriendt, E., Jacobs, A. et al. (2003) Mutations in the small GTP-ase late endosomal protein RAB7 cause Charcot-Marie-Tooth type 2B neuropathy. Am. J. Hum. Genet., 72, 722-727.
75. Cogli, L., Progida, C., Lecci, R., Bramato, R., Kruttgen, A. and Bucci, C. (2010) CMT2B-associated Rab7 mutants inhibit neurite outgrowth. Acta Neuropathol., 120, 491-501.
76. Zhang, J., Schulze, K.L., Hiesinger, P.R., Suyama, K., Wang, S., Fish, M., Acar, M., Hoskins, R.A., Bellen, H.J. and Scott, M.P. (2007) Thirty-one flavors of Drosophila rab proteins. Genetics, 176, 1307-1322.