Dysregulation of lysosomal morphology by pathogenic LRRK2 is corrected by TPC2 inhibition

Journal of Cell Science

Volumn 128, Issue 2, 2015, Pages 232-238

  Hockey, L N ^a   Kilpatrick, B S ^a   Eden, Emily R ^b   Lin Moshier, Yaping ^c   Cristina Brailoiu, G ^d   Brailoiu, Eugen ^e   Futter, Clare E ^b   Schapira, Anthony H ^f   Marchant, Jonathan S ^c   Patel, Sandip ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

^e TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Ca2+; LRRK2; Lysosomes; NAADP; Parkinson disease; TPCN2

Indexed keywords

CALCIUM ION; ION CHANNEL; LEUCINE RICH REPEAT KINASE 2; NICOTINIC ACID ADENINE DINUCLEOTIDE PHOSPHATE; RAB7 PROTEIN; TWO PORE CHANNEL 2; UNCLASSIFIED DRUG; CALCIUM; CALCIUM CHANNEL; LRRK2 PROTEIN, HUMAN; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PROTEIN SERINE THREONINE KINASE; TPCN2 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; DRUG TARGETING; FIBROBLAST; GENE MUTATION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LYSOSOME; MEMBRANE CHANNEL; PARKINSON DISEASE; PATHOGENICITY; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; CALCIUM SIGNALING; GENETICS; HEK293 CELL LINE; METABOLISM; PATHOLOGY; PRIMARY CELL CULTURE;

CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; FIBROBLASTS; HEK293 CELLS; HUMANS; LEUCINE-RICH REPEAT SERINE-THREONINE PROTEIN KINASE-2; LYSOSOMES; NADP; PARKINSON DISEASE; PRIMARY CELL CULTURE; PROTEIN-SERINE-THREONINE KINASES;

EID: 84921415558     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.164152     Document Type: Article

References (44)

1. Agola, J. O., Hong, L., Surviladze, Z., Ursu, O., Waller, A., Strouse, J. J., Simpson, D. S., Schroeder, C. E., Oprea, T. I., Golden, J. E. et al. (2012). A competitive nucleotide binding inhibitor: in vitro characterization of Rab7 GTPase inhibition. ACS Chem. Biol. 7, 1095-1108.
2. 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.
3. 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.
4. Brailoiu, E., Churamani, D., Cai, X., Schrlau, M. G., Brailoiu, G. C., Gao, X., Hooper, R., Boulware, M. J., Dun, N. J., Marchant, J. S. et al. (2009). Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling. J. Cell Biol. 186, 201-209.
5. Brailoiu, E., Rahman, T., Churamani, D., Prole, D. L., Brailoiu, G. C., Hooper, R., Taylor, C. W. and Patel, S. (2010). An NAADP-gated two-pore channel targeted to the plasma membrane uncouples triggering from amplifying Ca2+ signals. J. Biol. Chem. 285, 38511-38516.
6. 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.
7. Calcraft, P. J., Ruas, M., Pan, Z., Cheng, X., Arredouani, A., Hao, X., Tang, J., Rietdorf, K., Teboul, L., Chuang, K. T. et al. (2009). NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459, 596-600.
8. Cookson, M. R. (2010). The role of leucine-rich repeat kinase 2 (LRRK2) in Parkinson's disease. Nat. Rev. Neurosci. 11, 791-797.
9. Davis, L. C., Morgan, A. J., Chen, J. L., Snead, C. M., Bloor-Young, D., Shenderov, E., Stanton-Humphreys, M. N., Conway, S. J., Churchill, G. C., Parrington, J. et al. (2012). NAADP activates two-pore channels on T cell cytolytic granules to stimulate exocytosis and killing. Curr. Biol. 22, 2331-2337.
10. Deliu, E., Brailoiu, G. C., Mallilankaraman, K., Wang, H., Madesh, M., Undieh, A. S., Koch, W. J. and Brailoiu, E. (2012). Intracellular endothelin type B receptor-driven Ca2+ signal elicits nitric oxide production in endothelial cells. J. Biol. Chem. 287, 41023-41031.
11. Deng, X., Dzamko, N., Prescott, A., Davies, P., Liu, Q., Yang, Q., Lee, J. D., Patricelli, M. P., Nomanbhoy, T. K., Alessi, D. R. et al. (2011). Characterization of a selective inhibitor of the Parkinson's disease kinase LRRK2. Nat. Chem. Biol. 7, 203-205.
12. Dionisio, N., Albarrán, L., López, J. J., Berna-Erro, A., Salido, G. M., Bobe, R. and Rosado, J. A. (2011). Acidic NAADP-releasable Ca(2+) compartments in the megakaryoblastic cell line MEG01. Biochim. Biophys. Acta 1813, 1483-1494.
13. Dodson, M. W., Zhang, T., Jiang, C., Chen, S. and Guo, M. (2012). Roles of the Drosophila LRRK2 homolog in Rab7-dependent lysosomal positioning. Hum. Mol. Genet. 21, 1350-1363.
14. 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.
15. Grimm, C., Holdt, L. M., Chen, C. C., Hassan, S., Müller, C., Jörs, S., Cuny, H., Kissing, S., Schröder, B., Butz, E. et al. (2014). High susceptibility to fatty liver disease in two-pore channel 2-deficient mice. Nat. Commun. 5, 4699.
16. Hardy, J. (2010). Genetic analysis of pathways to Parkinson disease. Neuron 68, 201-206.
17. 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.; International LRRK2 Consortium (2008). Phenotype, genotype, and worldwide genetic penetrance of LRRK2-associated Parkinson's disease: a case-control study. Lancet Neurol. 7, 583-590.
18. Hooper, R. and Patel, S. (2012). NAADP on target. Adv. Exp. Med. Biol. 740, 325-347.
19. Hutagalung, A. H. and Novick, P. J. (2011). Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91, 119-149.
20. Jefferies, H. B., Cooke, F. T., Jat, P., Boucheron, C., Koizumi, T., Hayakawa, M., Kaizawa, H., Ohishi, T., Workman, P., Waterfield, M. D. et al. (2008). A selective PIKfyve inhibitor blocks PtdIns(3,5)P(2) production and disrupts endomembrane transport and retroviral budding. EMBO Rep. 9, 164-170.
21. Jha, A., Ahuja, M., Patel, S., Brailoiu, E. and Muallem, S. (2014). Convergent regulation of the lysosomal two-pore channel-2 by Mg2+, NAADP, PI(3,5)P2 and multiple protein kinases. EMBO J. 33, 501-511.
22. 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.
23. Lin-Moshier, Y., Keebler, M. V., Hooper, R., Boulware, M. J., Liu, X., Churamani, D., Abood, M. E., Walseth, T. F., Brailoiu, E., Patel, S. et al. (2014). The Two-pore channel (TPC) interactome unmasks isoform-specific roles for TPCs in endolysosomal morphology and cell pigmentation. Proc. Natl. Acad. Sci. USA 111, 13087-13092.
24. Lu, Y., Hao, B. X., Graeff, R., Wong, C. W., Wu, W. T. and Yue, J. (2013). Two pore channel 2 (TPC2) inhibits autophagosomal-lysosomal fusion by alkalinizing lysosomal pH. J. Biol. Chem. 288, 24247-24263.
25. Luzio, J. P., Pryor, P. R. and Bright, N. A. (2007). Lysosomes: fusion and function. Nat. Rev. Mol. Cell Biol. 8, 622-632.
26. MacLeod, D. A., Rhinn, H., Kuwahara, T., Zolin, A., Di Paolo, G., McCabe, D., Marder, K. S., Honig, L. S., Clark, L. N., Small, S. A. et al. (2013). RAB7L1 interacts with LRRK2 to modify intraneuronal protein sorting and Parkinson's disease risk. Neuron 77, 425-439.
27. Morgan, A. J., Davis, L. C., Wagner, S. K., Lewis, A. M., Parrington, J., Churchill, G. C. and Galione, A. (2013). Bidirectional Ca2+ signaling occurs between the endoplasmic reticulum and acidic organelles. J. Cell Biol. 200, 789-805.
28. Naylor, E., Arredouani, A., Vasudevan, S. R., Lewis, A. M., Parkesh, R., Mizote, A., Rosen, D., Thomas, J. M., Izumi, M., Ganesan, A. et al. (2009). Identification of a chemical probe for NAADP by virtual screening. Nat. Chem. Biol. 5, 220-226.
29. Nixon, R. A., Yang, D. S. and Lee, J. H. (2008). Neurodegenerative lysosomal disorders: a continuum from development to late age. Autophagy 4, 590-599.
30. Paisán-Ruíz, C., Jain, S., Evans, E. W., Gilks, W. P., Simón, J., van der Brug, M., López 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.
31. Papkovskaia, T. D., Chau, K. Y., Inesta-Vaquera, F., Papkovsky, D. B., Healy, D. G., Nishio, K., Staddon, J., Duchen, M. R., Hardy, J., Schapira, A. H. et al. (2012). G2019S leucine-rich repeat kinase 2 causes uncoupling protein-mediated mitochondrial depolarization. Hum. Mol. Genet. 21, 4201-4213.
32. Pryor, P. R., Mullock, B. M., Bright, N. A., Gray, S. R. and Luzio, J. P. (2000). The role of intraorganellar Ca(2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J. Cell Biol. 149, 1053-1062.
33. Reith, A. D., Bamborough, P., Jandu, K., Andreotti, D., Mensah, L., Dossang, P., Choi, H. G., Deng, X., Zhang, J., Alessi, D. R. et al. (2012). GSK2578215A; a potent and highly selective 2-arylmethyloxy-5-substitutent-N-arylbenzamide LRRK2 kinase inhibitor. Bioorg. Med. Chem. Lett. 22, 5625-5629.
34. Ruas, M., Rietdorf, K., Arredouani, A., Davis, L. C., Lloyd-Evans, E., Koegel, H., Funnell, T. M., Morgan, A. J., Ward, J. A., Watanabe, K. et al. (2010). Purified TPC isoforms form NAADP receptors with distinct roles for Ca(2+) signaling and endolysosomal trafficking. Curr. Biol. 20, 703-709.
35. Ruas, M., Chuang, K. T., Davis, L. C., Al-Douri, A., Tynan, P. W., Tunn, R., Teboul, L., Galione, A. and Parrington, J. (2014). TPC1 has two variant isoforms and their removal has different effects on endo-lysosomal functions compared to loss of TPC2. Mol. Cell Biol. [Epub ahead of print] doi: 10.1128/MCB.00113-14.
36. Sardiello, M., Palmieri, M., di Ronza, A., Medina, D. L., Valenza, M., Gennarino, V. A., Di Malta, C., Donaudy, F., Embrione, V., Polishchuk, R. S. et al. (2009). A gene network regulating lysosomal biogenesis and function. Science 325, 473-477.
37. Schapira, A. H. and Jenner, P. (2011). Etiology and pathogenesis of Parkinson's disease. Mov. Disord. 26, 1049-1055.
38. 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.
39. te Vruchte, D., Speak, A. O., Wallom, K. L., Al Eisa, N., Smith, D. A., Hendriksz, C. J., Simmons, L., Lachmann, R. H., Cousins, A., Hartung, R. et al. (2014). Relative acidic compartment volume as a lysosomal storage disorder-associated biomarker. J. Clin. Invest. 124, 1320-1328.
40. Tomas, A., Futter, C. and Moss, S. E. (2004). Annexin 11 is required for midbody formation and completion of the terminal phase of cytokinesis. J. Cell Biol. 165, 813-822.
41. Wang, X., Zhang, X., Dong, X. P., Samie, M., Li, X., Cheng, X., Goschka, A., Shen, D., Zhou, Y., Harlow, J. et al. (2012). TPC proteins are phosphoinositide-activated sodium-selective ion channels in endosomes and lysosomes. Cell 151, 372-383.
42. 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.
43. 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.
44. Zong, X., Schieder, M., Cuny, H., Fenske, S., Gruner, C., Rötzer, K., Griesbeck, O., Harz, H., Biel, M. and Wahl-Schott, C. (2009). The two-pore channel TPCN2 mediates NAADP-dependent Ca(2+)-release from lysosomal stores. Pflugers Arch. 458, 891-899.