LRRK2 delays degradative receptor trafficking by impeding late endosomal budding through decreasing Rab7 activity

Human Molecular Genetics

Volumn 23, Issue 25, 2014, Pages 6779-6796

  Gómez Suaga, Patricia ^a   Rivero Ríos, Pilar ^a   Fdez, Elena ^a   Ramírez, Marian Blanca ^a   Ferrer, Isidro ^b   Aiastui, Ana ^c   De Munain, Adolfo López ^c,d,e,f   Hilfiker, Sabine ^a  

^a INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c BIODONOSTIA HEALTH RESEARCH INSTITUTE   (Spain)

^d HOSPITAL DONOSTIA   (Spain)

^e CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^f UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; LEUCINE RICH REPEAT KINASE 2; RAB7 PROTEIN; EGFR PROTEIN, HUMAN; LRRK2 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; RAB PROTEIN;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDOSOME; ENZYME ACTIVE SITE; FIBROBLAST; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INTRACELLULAR MEMBRANE; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; BRAIN; CASE CONTROL STUDY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PATHOLOGY; PLASMID; PRIMARY CELL CULTURE; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; ULTRASTRUCTURE;

BRAIN; CASE-CONTROL STUDIES; ENDOSOMES; FIBROBLASTS; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HUMANS; PARKINSON DISEASE; PLASMIDS; PRIMARY CELL CULTURE; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; PROTEOLYSIS; RAB GTP-BINDING PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84910004657     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu395     Document Type: Article

References (60)

1. Cookson, M.R. (2010) The role of leucine-rich repeat kinase 2 (LRRK2) in Parkinson's disease. Nat. Rev. Neurosci., 11, 791-797
2. Healy, D.G., Falchi, M., O'Sullivan, S.S., Bonifati, V., Durr, A., Bressman, S., Brice, A., Aasly, J., Zabetian, C.P., Goldwurm, S. et al. (2008) Phenotype, genotype, and worldwide genetic penetrance of LRRK2-associated Parkinson's disease: a case-control study. Lancet Neurol., 7, 583-590
3. Simón-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
4. Sharma, M., Ioannidis, J.P., Aasly, J.O., Annesi, G., Brice, A., Van Broeckhoven, C., Bertram, L., Bozi, M., Crosiers, D., Clarke, C. et al. (2012) Large-scale replication and heterogeneity in Parkinson disease genetic loci. Neurology, 79, 659-667
5. 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
6. 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
7. Ito, G., Okai, T., Fujino, G., Takeda, K., Ichijo, H., Katada, T. and Iwatsubo, T. (2007)GTP binding is essential to the protein kinase activity of LRRK2, a causative gene product for familial Parkinson's disease. Biochemistry, 46, 1380-1388
8. Jaleel, M., Nichols, R.J., Deak, M., Campbell, D.G., Gillardon, F., Knebel, A. and Alessi, D.R. (2007)LRRK2phosphorylates moesin at threonine-558: characterization of how Parkinson's disease mutants affect kinase activity. Biochem. J., 405, 307-317
9. Lewis, P.A., Greggio, E., Beilina, A., Jain, S., Baker, A. and Cookson, M.R. (2007) The R1441C mutation of LRRK2 disrupts GTP hydrolysis. Biochem. Biophys. Res. Commun., 357, 668-671
10. Li, X., Tan, Y.C., Poulouse, S., Olanow, C.W., Huang, X.Y. and Yue, Z. (2007) Leucine-rich repeat kinase 2 (LRRK2)/PARK8 possesses GTPase activity that is altered in familial Parkinson's disease R1441C/G mutants. J. Neurochem., 103, 238-247
11. 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
12. 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
13. 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
14. Daniels, V., Vancraenenbroeck, R., Law, B.M., Greggio, E., Lobbestael, E., Gao, F., De Maeyer, M., Cookson, M.R., Harvey, K., Baekelandt, V. et al. (2011) Insight into the mode of action of the LRRK2 Y1699C pathogenic mutant. J. Neurochem., 116, 304-315
15. Stafa, K., Grancikova, A., Webber, P.J., Glauser, L., West, A. and Moore, D.J. (2012) GTPase activity and neuronal toxicity of Parkinson's disease-associated LRRk2 is regulated by ArfGAP1. PLoS Genet., 8, e1002527
16. Liao, J., Wu, C.X., Burlak, C., Zhang, S., Sahm, H., Wang, M., Zhang, Z.Y., Vogel, K.W., Federici, M., Riddle, S.M. et al. (2014) Parkinson disease-associated mutation R1441H in LRRK2 prolongs the 'active state' of its GTPase domain. Proc. Natl. Acad. Sci. USA, 111, 4055-4060
17. Smith, W.W., Pei, Z., Jiang, H., Dawson, V.L., Dawson, T.M. and Ross, C.A. (2006) Kinase activity of mutant LRRK2 mediates neuronal toxicity. Nat. Neurosci., 9, 1231-1233
18. Biskup, S., Moore, D.J., Rea, A., Lorenz-Deperieux, B., Coombes, C.E., Dawson, V.L., Dawson, T.M. and West, A.B. (2007) Dynamic and redundant regulation of LRRK2 and LRRK1 expression.BMC Neurosci., 8, 102
19. 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
20. 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
21. 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
22. 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
23. Matta, S., Van Kolen, K., da Cunha, R., van den Bogaart, G., Mandemakers, W., Miskiewicz, K., DeBock, P.J., Morais, V.A., Vilain, S., Haddad, D. et al. (2012) LRRK2 controls an EndoA phosphorylation cycle in synaptic endocytosis. Neuron, 75, 1008-1021
24. 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
25. 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
26. Plowey, E.D., Cherra, S.J. 3rd, Liu, Y.J. and Chu, C.T. (2008) Role of autophagy in G2019S-LRRK2-associated neurite shortening in differentiated SH-SY5Y cells. J. Neurochem., 105, 1048-1056
27. 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
28. Ramonet, D., Daher, J.P., Lin, B.M., Stafa, K., Kim, J., Banerjee, R., Westerlund, M., Pletnikova, O., Glauser, L., Yang, L. et al. (2011) Dopaminergic neuronal loss, reduced neurite complexity and autophagic abnormalities in transgenic mice expressing G2019S mutant LRRK2. PLoS ONE, 6, e18568
29. Dodson, M.W., Zhang, T., Jiang, C., Chen, S. and Guo, M. (2011) Roles of the Drosophila LRRK2 homolog in Rab7-dependent lysosomal positioning. Hum. Mol. Genet., 21, 1350-1363
30. Gómez-Suaga, P., Luzón-Toro, B., Churamani, D., Zhang, L., Bloor-Young, D., Patel, S., Woodman, P.G., Churchill, G.C. and Hilfiker, S. (2012) Leucine-rich repeat kinase 2 regulates autophagy through a calcium-dependent pathway involving NAADP. Hum. Mol. Genet., 21, 511-525
31. MacLeod, D.A., Rhinn, H., Kuwahara, T., Zolin, A., Di Paolo, G., McCabe, B.D., Marder, K.S., Honig, L.S., Clark, L.N., Small, S.A. and Abeliovich, A. (2013) RAB7L1 interacts with LRRK2 to modify intraneuronal protein sorting and Parkinson's disease risk. Neuron, 77, 425-439
32. 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
33. Beilina, A., Rudenko, I.N., Kaganovich, A., Civiero, L., Chau, H., Kalia, S.K., Kalia, L.V., Lobbestael, E., Chia, R., Ndukwe, K. et al. (2014) Unbiased screen for interactors of leucine-rich repeat kinase 2 supports a common pathway for sporadic and familial Parkinson disease. Proc. Natl. Acad. Sci. USA, 111, 2626-2631
34. Katzmann, D.J., Odorizzi, G. and Emr, S.D. (2002) Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol., 3, 893-905
35. Schroeder, B., Weller, S.G., Chen, J., Billadeau, D. and McNiven, M.A. (2010)ADyn2-CIN85 complex mediates degradative traffic of theEGFRby regulation of late endosomal budding. EMBO J., 29, 3039-3053
36. Ramsden, N., Perrin, J., Ren, Z., Lee, B.D., Zinn, N., Dawson, V.L., Tam, D., Bova, M., Lang, M., Drewes, G. et al. (2011) Chemoproteomics-based design of potent LRRK2-selective lead compounds that attenuate Parkinson's disease-related toxicity in human neurons. ACS Chem. Biol., 6, 1021-1028
37. Reith, A.D., Bamborough, P., Jandu, K., Andreotti, D., Mensah, L., Dossang, P., Choi, H.G., Deng, X., Zhang, J., Alessi, D.R. and Gray, N.S. (2012) GSK2578215A; a potent and highly selective 2-arylmethyloxy-5-substituent-N-arylbenzamide LRRK2 kinase inhibitor. Bioorg. Med. Chem. Lett., 22, 5625-5629
38. Barr, F. and Lambright, D.G. (2010) Rab GEFs and GAPs. Curr. Opin. Cell Biol., 22, 461-470
39. Mizuno-Yamasaki, E., Rivera-Molina, F. and Novick, P. (2012) GTPase networks in membrane traffic. Annu. Rev. Biochem., 81, 637-659
40. Zhang, X.M., Walsh, B., Mitchell, C.A. and Rowe, T. (2005) TBC domain family, member 15 is a novel mammalian Rab GTPase-activating protein with substrate preference for Rab7. Biochem. Biophys. Res. Commun., 335, 154-161
41. Peralta, E.R., Martin, B.C. and Edinger, A.L. (2010) Differential effects of TBC1D15 and mammalian Vps39 on Rab7 activation state, lysosomal morphology, and growth factor dependence. J. Biol. Chem., 285, 16814-16821
42. Seaman, M.N., Harbour, M.E., Tattersall, D., Read, E. and Bright, N. (2009) Membrane recruitment of the cargo-selective retromer subcomplex is catalysed by the small GTPase Rab7 and inhibited by the Rab-GAP TBC1D5. J. Cell Sci., 122, 2371-2382
43. 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
44. McCray, B.A., Skordalakes, E. and Taylor, J.P. (2010) Disease mutations in Rab7 result in unregulated nucleotide exchange and inappropriate activation. Hum. Mol. Genet., 19, 1033-1047
45. Ceresa, B.P. and Bahr, S.J. (2006) rab7 activity affects epidermal growth factor:epidermal growth factor receptor degradation by regulating endocytic trafficking from the late endosome. J. Biol. Chem., 281, 1099-1106
46. Vanlandingham, P.A. and Ceresa, B.P. (2009) Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. J. Biol. Chem., 284, 12110-12124
47. Shimokawa, N., Haglund, K., Holter, S.M., Grabbe, C., Kirkin, V., Koibuchi, N., Schultz, C., Rozman, J., Hoeller, D., Qiu, C.H. et al. (2010) CIN85 regulates dopamine receptor endocytosis and governs behaviour in mice. EMBO J., 29, 2421-2432
48. Kowanetz, K., Terzic, J. and Dikic, I. (2003) Dab2 links CIN85 with clathrin-mediated receptor internalization. FEBS Lett., 554, 81-87
49. Jiang, Y., He, X. and Howe, P.H. (2012) Disabled-2 (Dab2) inhibits Wnt/ b-catenin signalling by binding LRP6 and promoting its internalization through clathrin. EMBO J., 31, 2336-2349
50. Migheli, R., Del Giudice, M.G., Spissu, Y., Sanna, G., Xiong, Y., Dawson, T.M., Dawson, V.L., Galioto, M., Rocchitta, G., Biosa, A. et al. (2013) LRRK2 affects vesicle trafficking, neurotransmitter extracellular level and membrane receptor localization. PLoS ONE, 8, e77198
51. Berwick, D.C. and Harvey, K. (2012) LRRK2 functions as a Wnt signaling scaffold, bridging cytosolic proteins and membrane-localized LRP6. Hum. Mol. Genet., 21, 4966-4979
52. 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
53. Jager, S., Bucci, C., Tanida, I., Ueno, T., Kominami, E., Saftig, P. and Eskelinen, E.L. (2004) Role for Rab7 in maturation of late autophagic vacuoles. J. Cell Sci., 117, 4837-4848
54. Rojas, R., van Vlijmen, T., Mardones, G.A., Prabhu, Y., Rojas, A.L., Mohammed, S., Heck, A.J., Raposo, G., van der Sluijs, P. and Bonifacino, J.S. (2008) Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol., 183, 513-526
55. Yu, L., McPhee, C.K., Zheng, L., Mardones, G.A., Rong, Y., Peng, J., Mi, N., Zhao, Y., Liu, Z., Wan, F. et al. (2010) Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature, 465, 942-946
56. Orenstein, S.J., Kuo, S.H., Tasset, I., Arias, E., Koga, H., Fernandez-Carasa, I., Cortes, E., Honig, L.S., Dauer, W., Consiglio, A. et al. (2013) Interplay of LRRK2 with chaperone-mediated autophagy. Nat. Neurosci., 16, 394-406
57. Sánches-Danés, A., Richaud-Patin, Y., Carballo-Carbajal, I., Jiménez-Delgado, S., Caig, C., Mora, S., Di Guglielmo, C., Ezquerra, M., Patel, B., Giralt, A. et al. (2012) Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson's disease. EMBO Mol. Med., 4, 380-395
58. Schapansky, J., Nardozzi, J.D., Felizia, F. and LaVoie, M.J. (2014) Membrane recruitment of endogenousLRRK2precedes its potent regulation of autophagy. Hum. Mol. Genet., 23, 4201-4214
59. Manzoni, C., Mamais, A., Dihanich, S., McGoldrick, P., Devine, M.J., Zerle, J., Kara, E., Taanman, J.W., Healy, D.G., Marti-Maso, J.F. et al. (2013) Pathogenic Parkinson's disease mutations across the functional domains of LRRk2 alter the autophagic/lysosomal response to starvation. Biochem. Biophys. Res. Commun., 441, 862-866
60. Rubio de la Torre, E., Luzón-Toro, B., Forte-Lago, I., Minguez-Castellanos, A., Ferrer, I. and Hilfiker, S. (2009) Combined kinase inhibition modulates parkin inactivation. Hum. Mol. Genet., 28, 809-823