Zn2+ dyshomeostasis caused by loss of ATP13A2/PARK9 leads to lysosomal dysfunction and alpha-synuclein accumulation

Human Molecular Genetics

Volumn 23, Issue 11, 2014, Pages 2791-2801

  Tsunemi, Taiji ^a   Krainc, Dimitri ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; CHELATING AGENT; CLIOQUINOL; GLUCOSYLCERAMIDASE; MUTANT PROTEIN; PARK9 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; ZINC ION; ZINC TRANSPORTER; ATP13A2 PROTEIN, HUMAN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; ZINC;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FIBROBLAST; HUMAN; HUMAN CELL; LYSOSOME; NERVE CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; WILD TYPE; ENZYMOLOGY; GENETICS; HOMEOSTASIS; METABOLISM; PARKINSONISM;

ALPHA-SYNUCLEIN; HOMEOSTASIS; HUMANS; LYSOSOMES; PARKINSONIAN DISORDERS; PROTON-TRANSLOCATING ATPASES; ZINC;

EID: 84899971096     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt572     Document Type: Article

References (57)

1. 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.
2. 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.
3. 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.
4. Podhajska, A., Musso, A., Trancikova, A., Stafa, K., Moser, R., Sonnay, S., Glauser, L. and Moore, D.J. (2012) Common pathogenic effects of missense mutations in the P-type ATPase ATP13A2 (PARK9) associated with early-onset parkinsonism. PLoS ONE, 7, e39942.
5. Ramonet, D., Podhajska, A., Stafa, K., Sonnay, S., Trancikova, A., Tsika, E., Pletnikova, O., Troncoso, J.C., Glauser, L. and Moore, D.J. (2012) PARK9-associated ATP13A2 localizes to intracellular acidic vesicles and regulates cation homeostasis and neuronal integrity. Hum. Mol. Genet., 21, 1725-1743.
6. Axelsen, K.B. and Palmgren, M.G. (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J. Mol. Evol., 46, 84-101.
7. 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.
8. Tan, J., Zhang, T., Jiang, L., Chi, J., Hu, D., Pan, Q., Wang, D. and Zhang, Z. (2011) Regulation of intracellular manganese homeostasis by Kufor-Rakeb syndrome-associatedATP13A2protein. J. Biol. Chem., 286, 29654-29662.
9. Usenovic, M., Tresse, E., Mazzulli, J.R., Taylor, J.P. and Krainc, D. (2012) Deficiency of ATP13A2 leads to lysosomal dysfunction, alpha-synuclein accumulation, and neurotoxicity. J. Neurosci., 32, 4240-4246.
10. Usenovic, M. and Krainc, D. (2012) Lysosomal dysfunction in neurodegeneration: the role of ATP13A2/PARK9. Autophagy, 8, 987-988.
11. Dehay, B., Ramirez, A., Martinez-Vicente, M., Perier, C., Canron, M.H., Doudnikoff, E., Vital, A., Vila, M., Klein, C. and Bezard, E. (2012) Loss of P-type ATPase ATP13A2/PARK9 function induces general lysosomal deficiency and leads to Parkinson disease neurodegeneration. Proc. Natl Acad. Sci. USA, 109, 9611-9616.
12. Hwang, J.J., Lee, S.J., Kim, T.Y., Cho, J.H. and Koh, J.Y. (2008) Zinc and 4-hydroxy-2-nonenal mediate lysosomal membrane permeabilization induced by H2O2 in cultured hippocampal neurons. J. Neurosci., 28, 3114-3122.
13. Varea, E., Alonso-Llosa, G., Molowny, A., Lopez-Garcia, C. and Ponsoda, X. (2006) Capture of extracellular zinc ions by astrocytes. Glia, 54, 304-315.
14. Fukada, T., Yamasaki, S., Nishida, K., Murakami, M. and Hirano, T. (2011) Zinc homeostasis and signaling in health and diseases: Zinc signaling. J. Biol. Inorg. Chem., 16, 1123-1134.
15. Liuzzi, J.P. and Cousins, R.J. (2004) Mammalian zinc transporters. Annu. Rev. Nutr., 24, 151-172.
16. Vasak, M. and Meloni, G. (2011) Chemistry and biology of mammalian metallothioneins. J. Biol. Inorg. Chem., 16, 1067-1078.
17. Jackson, K.A., Valentine, R.A., Coneyworth, L.J., Mathers, J.C. and Ford, D. (2008) Mechanisms of mammalian zinc-regulated gene expression. Biochem. Soc. Trans., 36, 1262-1266.
18. Kambe, T., Yamaguchi-Iwai, Y., Sasaki, R. and Nagao, M. (2004) Overview of mammalian zinc transporters. Cell. Mol. Life Sci., 61, 49-68.
19. Palmiter, R.D., Findley, S.D., Whitmore, T.E. and Durnam, D.M. (1992) MT-III, a brain-specific member of the metallothionein gene family. Proc. Natl Acad. Sci. USA, 89, 6333-6337.
20. Mindell, J.A. (2012) Lysosomal acidification mechanisms. Annu. Rev. Physiol., 74, 69-86.
21. Mazzulli, J.R., Xu, Y.H., Sun, Y., Knight, A.L., McLean, P.J., Caldwell, G.A., Sidransky, E., Grabowski, G.A. and Krainc, D. (2011) Gaucher disease glucocerebrosidase and alpha-synuclein form a bidirectional pathogenic loop in synucleinopathies. Cell, 146, 37-52.
22. Schulze, H. and Sandhoff, K. (2011) Lysosomal lipid storage diseases. Cold Spring Harb. Perspect. Biol., 3, a004804.
23. Jenkins, R.W., Idkowiak-Baldys, J., Simbari, F., Canals, D., Roddy, P., Riner, C.D., Clarke, C.J. and Hannun, Y.A. (2011) A novel mechanism of lysosomal acid sphingomyelinase maturation: requirement for carboxyl-terminal proteolytic processing. J. Biol. Chem., 286, 3777-3788.
24. Tapiero, H. and Tew, K.D. (2003) Trace elements in human physiology and pathology: zinc and metallothioneins. Biomed. Pharmacother., 57, 399-411.
25. Andreini, C., Banci, L., Bertini, I. and Rosato, A. (2006) Counting the zinc-proteins encoded in the human genome. J. Proteome Res., 5, 196-201.
26. Vallee, B.L. and Auld, D.S. (1990) Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry, 29, 5647-5659.
27. Sensi, S.L., Paoletti, P., Bush, A.I. and Sekler, I. (2009) Zinc in the physiology and pathology of the CNS. Nat. Rev. Neurosci., 10, 780-791.
28. Religa, D., Strozyk, D., Cherny, R.A., Volitakis, I., Haroutunian, V., Winblad, B., Naslund, J. and Bush, A.I. (2006) Elevated cortical zinc in Alzheimer disease. Neurology, 67, 69-75.
29. Bush, A.I., Pettingell, W.H., Multhaup, G., dParadis, M., Vonsattel, J.P., Gusella, J.F., Beyreuther, K., Masters, C.L. and Tanzi, R.E. (1994) Rapid induction of Alzheimer A beta amyloid formation by zinc. Science, 265, 1464-1467.
30. Dexter, D.T., Jenner, P., Schapira, A.H. and Marsden, C.D. (1992) Alterations in levels of iron, ferritin, and other trace metals in neurodegenerative diseases affecting the basal ganglia. The Royal Kings and Queens Parkinson's Disease Research Group. Ann. Neurol., 32 (suppl.), S94-S100.
31. Dexter, D.T., Carayon, A., Javoy-Agid, F., Agid, Y., Wells, F.R., Daniel, S.E., Lees, A.J., Jenner, P. and Marsden, C.D. (1991) Alterations in the levels of iron, ferritin and other trace metals in Parkinson's disease and other neurodegenerative diseases affecting the basal ganglia. Brain, 114(Pt 4), 1953-1975.
32. Hozumi, I., Hasegawa, T., Honda, A., Ozawa, K., Hayashi, Y., Hashimoto, K., Yamada, M., Koumura, A., Sakurai, T., Kimura, A. et al. (2011) Patterns of levels of biological metals in CSF differ among neurodegenerative diseases. J. Neurol. Sci., 303, 95-99.
33. Frederickson, C.J., Koh, J.Y. and Bush, A.I. (2005) The neurobiology of zinc in health and disease. Nat. Rev. Neurosci., 6, 449-462.
34. Devirgiliis, C., Murgia, C., Danscher, G. and Perozzi, G. (2004) Exchangeable zinc ions transiently accumulate in a vesicular compartment in the yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun., 323, 58-64.
35. Roh, H.C., Collier, S., Guthrie, J., Robertson, J.D. and Kornfeld, K. (2012) Lysosome-related organelles in intestinal cells are a zinc storage site in C. elegans. Cell. Metab., 15, 88-99.
36. Palmiter, R.D., Cole, T.B. and Findley, S.D. (1996) ZnT-2, a mammalian protein that confers resistance to zinc by facilitating vesicular sequestration. EMBO J., 15, 1784-1791.
37. Falcon-Perez, J.M. and Dell'Angelica, E.C. (2007) Zinc transporter 2 (SLC30A2) can suppress the vesicular zinc defect of adaptor protein 3-depleted fibroblasts by promoting zinc accumulation in lysosomes. Exp. Cell Res., 313, 1473-1483.
38. Outten, C.E. and O'Halloran, T.V. (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science, 292, 2488-2492.
39. Lichten, L.A. and Cousins, R.J. (2009) Mammalian zinc transporters: nutritional and physiologic regulation. Annu. Rev. Nutr., 29, 153-176.
40. McMahon, R.J. and Cousins, R.J. (1998) Regulation of the zinc transporter ZnT-1 by dietary zinc. Proc. Natl Acad. Sci. USA, 95, 4841-4846.
41. Jou, M.Y., Philipps, A.F., Kelleher, S.L. and Lonnerdal, B. (2010) Effects of zinc exposure on zinc transporter expression in human intestinal cells of varying maturity. J. Pediatr. Gastroenterol. Nutr., 50, 587-595.
42. Palmiter, R.D. and Findley, S.D. (1995) Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zinc. EMBO J., 14, 639-649.
43. 2+ inhibits alpha-ketoglutarate-stimulated mitochondrial respiration and the isolated alpha-ketoglutarate dehydrogenase complex. J. Biol. Chem., 275, 13441-13447.
44. Link, T.A. and von Jagow,G. (1995) Zinc ions inhibit theQPcenter of bovine heart mitochondrial bc1 complex by blocking a protonatable group. J. Biol. Chem., 270, 25001-25006.
45. Wudarczyk, J., Debska, G. and Lenartowicz, E. (1999) Zinc as an inducer of the membrane permeability transition in rat liver mitochondria. Arch. Biochem. Biophys., 363, 1-8.
46. Dineley, K.E., Richards, L.L., Votyakova, T.V. and Reynolds, I.J. (2005) Zinc causes loss of membrane potential and elevates reactive oxygen species in rat brain mitochondria. Mitochondrion, 5, 55-65.
47. Gusdon, A.M., Zhu, J., Van Houten, B. and Chu, C.T. (2012) ATP13A2 regulates mitochondrial bioenergetics through macroautophagy. Neurobiol. Dis., 45, 962-972.
48. Grunewald, A., Arns, B., Seibler, P., Rakovic, A.,Munchau, A., Ramirez, A., Sue, C.M. and Klein, C. (2012) ATP13A2 mutations impair mitochondrial function in fibroblasts from patients with Kufor-Rakeb syndrome. Neurobiol. Aging, 33, 1843 e1841-1847.
49. Schultheis, P.J., Fleming, S.M., Clippinger, A.K., Lewis, J., Tsunemi, T., Giasson, B., Dickson, D.W., Mazzulli, J.R., Bardgett, M.E., Haik, K.L. et al. (2013) Atp13a2-deficient mice exhibit neuronal ceroid lipofuscinosis, limited alpha-synuclein accumulation and age-dependent sensorimotor deficits. Hum. Mol. Genet., 22, 2067-2082.
50. Devine, M.J., Gwinn, K., Singleton, A. and Hardy, J. (2011) Parkinson's disease and alpha-synuclein expression. Mov. Disord., 26, 2160-2168.
51. Esteves, A.R., Arduino, D.M., Swerdlow, R.H., Oliveira, C.R. and Cardoso, S.M. (2009) Oxidative stress involvement in alpha-synuclein oligomerization in Parkinson's disease cybrids. Antioxid. Redox Signal., 11, 439-448.
52. Li, W., Jiang, H., Song, N. and Xie, J. (2011) Oxidative stress partially contributes to iron-induced alpha-synuclein aggregation in SK-N-SH cells. Neurotox. Res., 19, 435-442.
53. Freeman, D., Cedillos, R., Choyke, S., Lukic, Z., McGuire, K., Marvin, S., Burrage, A.M., Sudholt, S., Rana, A., O'Connor, C. et al. (2013) Alpha-synuclein induces lysosomal rupture and cathepsin dependent reactive oxygen species following endocytosis. PLoS ONE, 8, e62143.
54. Schissel, S.L., Keesler, G.A., Schuchman, E.H., Williams, K.J. and Tabas, I. (1998) The cellular trafficking and zinc dependence of secretory and lysosomal sphingomyelinase, two products of the acid sphingomyelinase gene. J. Biol. Chem., 273, 18250-18259.
55. Macauley, S.L., Sidman, R.L., Schuchman, E.H., Taksir, T. and Stewart, G.R. (2008) Neuropathology of the acid sphingomyelinase knockout mouse model of Niemann-Pick A disease including structure-function studies associated with cerebellar Purkinje cell degeneration. Exp. Neurol., 214, 181-192.
56. Jeong, H., Then, F., Melia, T.J. Jr, Mazzulli, J.R., Cui, L., Savas, J.N., Voisine, C., Paganetti, P., Tanese, N., Hart, A.C. et al. (2009) Acetylation targets mutant huntingtin to autophagosomes for degradation. Cell, 137, 60-72.
57. Tsunemi, T., Ashe, T.D., Morrison, B.E., Soriano, K.R., Au, J., Roque, R.A., Lazarowski, E.R., Damian, V.A., Masliah, E. and La Spada, A.R. (2012) PGC-1alpha rescues Huntington's disease proteotoxicity by preventing oxidative stress and promoting TFEB function. Sci. Transl. Med., 4, 142ra197.