PARK9-associated ATP13A2 localizes to intracellular acidic vesicles and regulates cation homeostasis and neuronal integrity

Human Molecular Genetics

Volumn 21, Issue 8, 2012, Pages 1725-1743

  Ramonet, David ^a   Podhajska, Agata ^a   Stafa, Klodjan ^a   Sonnay, Sarah ^a   Trancikova, Alzbeta ^a   Tsika, Elpida ^a   Pletnikova, Olga ^b   Troncoso, Juan C ^b   Glauser, Liliane ^a   Moore, Darren J ^a  

^a EPFL   (Switzerland)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATP13A2 PROTEIN; CADMIUM; PARKIN; PARKIN 9; PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN CELL; BRAIN CORTEX; CALCIUM CELL LEVEL; CELL PH; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; HOMEOSTASIS; HUMAN; HUMAN CELL; INTRACELLULAR ACIDIC VESICLE; LEWY BODY; MITOCHONDRION; MOUSE; NERVE FIBER GROWTH; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; RAT; SUBSTANTIA NIGRA;

ADENOSINE TRIPHOSPHATASES; ANIMALS; AUTOPHAGY; BRAIN; CALCIUM; CELLS, CULTURED; CYTOPLASMIC VESICLES; DOPAMINERGIC NEURONS; HUMANS; HYDROGEN-ION CONCENTRATION; LEWY BODIES; MEMBRANE PROTEINS; MICE; MITOCHONDRIA; NEURITES; NEURONS; PARKINSON DISEASE; PROTON-TRANSLOCATING ATPASES; PYRAMIDAL CELLS; RATS; RNA INTERFERENCE; SUBSTANTIA NIGRA;

MAMMALIA;

EID: 84859246513     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr606     Document Type: Article

References (41)

1. Gasser, T. (2009) Mendelian forms of Parkinson's disease. Biochim. Biophys. Acta, 1792, 587-596.
2. Hardy, J., Cai, H., Cookson, M.R., Gwinn-Hardy, K. and Singleton, A. (2006) Genetics of Parkinson's disease and parkinsonism. Ann. Neurol., 60, 389-398.
3. Moore, D.J., West, A.B., Dawson, V.L. and Dawson, T.M. (2005) Molecular pathophysiology of Parkinson's disease. Annu. Rev. Neurosci., 28, 57-87.
4. Behrens, M.I., Bruggemann, N., Chana, P., Venegas, P., Kagi, M., Parrao, T., Orellana, P., Garrido, C., Rojas, C.V., Hauke, J. et al. (2010) Clinical spectrum of Kufor-Rakeb syndrome in the Chilean kindred with ATP13A2 mutations. Mov. Disord., 25, 1929-1937.
5. Najim Al-Din, A.S., Wriekat, A., Mubaidin, A., Dasouki, M. and Hiari, M. (1994) Pallido-pyramidal degeneration, supranuclear upgaze paresis and dementia: Kufor-Rakeb syndrome. Acta Neurol. Scand., 89, 347-352.
6. 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.
7. Williams, D.R., Hadeed, A., al-Din, A.S., Wreikat, A.L. and Lees, A.J. (2005) Kufor Rakeb disease: autosomal recessive, levodopa-responsive parkinsonism with pyramidal degeneration, supranuclear gaze palsy, and dementia. Mov. Disord., 20, 1264-1271.
8. Ugolino, J., Fang, S., Kubisch, C. and Monteiro, M.J. (2011) Mutant Atp13a2 proteins involved in parkinsonism are degraded by ER-associated degradation and sensitize cells to ER-stress induced cell death. Hum. Mol. Genet., 20, 3565-3577.
9. Park, J.S., Mehta, P., Cooper, A.A., Veivers, D., Heimbach, A., Stiller, B., Kubisch, C., Fung, V.S., Krainc, D., Mackay-Sim, A. et al. (2011) Pathogenic effects of novel mutations in the P-type ATPase ATP13A2 (PARK9) causing Kufor-Rakeb syndrome, a form of early-onset parkinsonism. Hum. Mutat., 32, 956-964.
10. Crosiers, D., Ceulemans, B., Meeus, B., Nuytemans, K., Pals, P., Van Broeckhoven, C., Cras, P. and Theuns, J. (2011) Juvenile dystonia-parkinsonism and dementia caused by a novel ATP13A2 frameshift mutation. Parkinsonism Relat. Disord., 17, 135-138.
11. Djarmati, A., Hagenah, J., Reetz, K., Winkler, S., Behrens, M.I., Pawlack, H., Lohmann, K., Ramirez, A., Tadic, V., Bruggemann, N. et al. (2009) ATP13A2 variants in early-onset Parkinson's disease patients and controls. Mov. Disord., 24, 2104-2111.
12. Lin, C.H., Tan, E.K., Chen, M.L., Tan, L.C., Lim, H.Q., Chen, G.S. and Wu, R.M. (2008) Novel ATP13A2 variant associated with Parkinson disease in Taiwan and Singapore. Neurology, 71, 1727-1732.
13. Ning, Y.P., Kanai, K., Tomiyama, H., Li, Y., Funayama, M., Yoshino, H., Sato, S., Asahina, M., Kuwabara, S., Takeda, A. et al. (2008) PARK9-linked parkinsonism in eastern Asia: mutation detection in ATP13A2 and clinical phenotype. Neurology, 70, 1491-1493.
14. Santoro, L., Breedveld, G.J., Manganelli, F., Iodice, R., Pisciotta, C., Nolano, M., Punzo, F., Quarantelli, M., Pappata, S., Di Fonzo, A. et al. (2011) Novel ATP13A2 (PARK9) homozygous mutation in a family with marked phenotype variability. Neurogenetics, 12, 33-39.
15. Schultheis, P.J., Hagen, T.T., O'Toole, K.K., Tachibana, A., Burke, C.R., McGill, D.L., Okunade, G.W. and Shull, G.E. (2004) Characterization of the P5 subfamily of P-type transport ATPases in mice. Biochem. Biophys. Res. Commun., 323, 731-738.
16. Gitler, A.D., Chesi, A., Geddie, M.L., Strathearn, K.E., Hamamichi, S., Hill, K.J., Caldwell, K.A., Caldwell, G.A., Cooper, A.A., Rochet, J.C. et al. (2009) Alpha-synuclein is part of a diverse and highly conserved interaction network that includes PARK9 and manganese toxicity. Nat. Genet., 41, 308-315.
17. Schmidt, K., Wolfe, D.M., Stiller, B. and Pearce, D.A. (2009) Cd2+, Mn2+, Ni2+ and Se2+ toxicity to Saccharomyces cerevisiae lacking YPK9p the orthologue of human ATP13A2. Biochem. Biophys. Res. Commun., 383, 198-202.
18. Tan, J., Zhang, T., Jiang, L., Chi, J., Hu, D., Pan, Q., Wang, D. and Zhang, Z. (2011) Regulation of intracellular manganese hemeostasis by kufor-rakeb syndrome associated ATP13A2. J. Biol. Chem., 286, 29654-29662.
19. Wong, E. and Cuervo, A.M. (2010) Autophagy gone awry in neurodegenerative diseases. Nat. Neurosci., 13, 805-811.
20. Cuervo, A.M., Stefanis, L., Fredenburg, R., Lansbury, P.T. and Sulzer, D. (2004) Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science, 305, 1292-1295.
21. Martinez-Vicente, M., Talloczy, Z., Kaushik, S., Massey, A.C., Mazzulli, J., Mosharov, E.V., Hodara, R., Fredenburg, R., Wu, D.C., Follenzi, A. et al. (2008) Dopamine-modified alpha-synuclein blocks chaperone-mediated autophagy. J. Clin. Invest., 118, 777-788.
22. Ravikumar, B., Sarkar, S., Davies, J.E., Futter, M., Garcia-Arencibia, M., Green-Thompson, Z.W., Jimenez-Sanchez, M., Korolchuk, V.I., Lichtenberg, M., Luo, S. et al. (2010) Regulation of mammalian autophagy in physiology and pathophysiology. Physiol. Rev., 90, 1383-1435.
23. Winslow, A.R., Chen, C.W., Corrochano, S., Acevedo-Arozena, A., Gordon, D.E., Peden, A.A., Lichtenberg, M., Menzies, F.M., Ravikumar, B., Imarisio, S. et al. (2010) alpha-Synuclein impairs macroautophagy: implications for Parkinson's disease. J. Cell Biol., 190, 1023-1037.
24. Mizushima, N. and Yoshimori, T. (2007) How to interpret LC3 immunoblotting. Autophagy, 3, 542-545.
25. Vallipuram, J., Grenville, J. and Crawford, D.A. (2010) The E646D-ATP13A4 mutation associated with autism reveals a defect in calcium regulation. Cell. Mol. Neurobiol., 30, 233-246.
26. Li, Z., Okamoto, K., Hayashi, Y. and Sheng, M. (2004) The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell, 119, 873-887.
27. Detmer, S.A. and Chan, D.C. (2007) Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol., 8, 870-879.
28. Schneider, S.A., Paisan-Ruiz, C., Quinn, N.P., Lees, A.J., Houlden, H., Hardy, J. and Bhatia, K.P. (2010) ATP13A2 mutations (PARK9) cause neurodegeneration with brain iron accumulation. Mov. Disord., 25, 979-984.
29. Higashi, S., Moore, D.J., Minegishi, M., Kasanuki, K., Fujishiro, H., Kabuta, T., Togo, T., Katsuse, O., Uchikado, H., Furukawa, Y. et al. (2011) Localization of MAP1-LC3 in vulnerable neurons and Lewy bodies in brains of patients with dementia with Lewy bodies. J. Neuropathol. Exp. Neurol., 70, 264-280.
30. Strack, R.L., Strongin, D.E., Bhattacharyya, D., Tao, W., Berman, A., Broxmeyer, H.E., Keenan, R.J. and Glick, B.S. (2008) A noncytotoxic DsRed variant for whole-cell labeling. Nat. Methods, 5, 955-957.
31. Jackson, W.T., Giddings, T.H., Jr, Taylor, M.P., Mulinyawe, S., Rabinovitch, M., Kopito, R.R. and Kirkegaard, K. (2005) Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol., 3, e156.
32. Vonderheit, A. and Helenius, A. (2005) Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol., 3, e233.
33. Choudhury, A., Dominguez, M., Puri, V., Sharma, D.K., Narita, K., Wheatley, C.L., Marks, D.L. and Pagano, R.E. (2002) Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J. Clin. Invest., 109, 1541-1550.
34. Sherer, N.M., Lehmann, M.J., Jimenez-Soto, L.F., Ingmundson, A., Horner, S.M., Cicchetti, G., Allen, P.G., Pypaert, M., Cunningham, J.M. and Mothes, W. (2003) Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic, 4, 785-801.
35. 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.
36. Moore, D.J., Zhang, L., Dawson, T.M. and Dawson, V.L. (2003) A missense mutation (L166P) in DJ-1, linked to familial Parkinson's disease, confers reduced protein stability and impairs homo-oligomerization. J. Neurochem., 87, 1558-1567.
37. 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.
38. 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.
39. Hallett, P.J., Collins, T.L., Standaert, D.G. and Dunah, A.W. (2008) Biochemical fractionation of brain tissue for studies of receptor distribution and trafficking. Curr. Protoc. Neurosci., Chapter 1, Unit 1.16.
40. 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.
41. Nakamura, K., Nemani, V.M., Azarbal, F., Skibinski, G., Levy, J.M., Egami, K., Munishkina, L., Zhang, J., Gardner, B., Wakabayashi, J. et al. (2011) Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein alpha-synuclein. J. Biol. Chem., 286, 20710-20726.