The Ca 2+ /Mn 2+ ion-pump PMR1 links elevation of cytosolic Ca 2+ levels to -synuclein toxicity in Parkinson's disease models

Cell Death and Differentiation

Volumn 20, Issue 3, 2013, Pages 465-477

  Buttner S ^a   Faes, L ^b,c   Reichelt, W N ^a   Broeskamp, F ^a   Habernig, L ^a   Benke, S ^a   Kourtis, N ^d   Ruli, D ^a   Carmona Gutierrez, D ^a   Eisenberg, T ^a   D'Hooge, P ^b   Ghillebert, R ^c   Franssens, V ^c   Harger, A ^c   Pieber, T R ^c   Freudenberger, P ^a   Kroemer, G ^e,f,g,h,i   Sigrist, S J ^j   Winderickx, J ^c   Callewaert, G ^b   Tavernarakis, N ^d   Madeo, F ^a   more..

^a UNIVERSITY OF GRAZ   (Austria)

^b Research Group Neurodegeneration   (Belgium)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d INSTITUTE OF COMPUTER SCIENCE   (Greece)

^e INSERM   (France)

^f INSTITUT GUSTAVE ROUSSY   (France)

^g CENTRE DE RECHERCHE DES CORDELIERS   (France)

^h HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

ⁱ UNIVERSITÉ PARIS DESCARTES   (France)

^j FREIE UNIVERSITÄT BERLIN   (Germany)

more..

Author keywords

a synuclein; Ca2+ homeostasis; dopaminergic neuron loss; Parkinson's disease models; PMR1; yeast cell death

Indexed keywords

ALPHA SYNUCLEIN; CALCIUM ION; MANGANESE; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATASE (CALCIUM); CAENORHABDITIS ELEGANS PROTEIN; CALCIUM; PMR1 PROTEIN, C ELEGANS; PMR1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SMALL INTERFERING RNA;

ARTICLE; CAENORHABDITIS ELEGANS; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CELL DEATH; CYTOTOXICITY; DOPAMINERGIC NERVE CELL; DROSOPHILA MELANOGASTER; GOLGI COMPLEX; ION TRANSPORT; NEMATODE; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; SURVIVAL; ANIMAL; APOPTOSIS; BIOLOGICAL MODEL; DRUG EFFECT; GENETICS; HUMAN; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; PHOSPHORYLATION; PROMOTER REGION; RNA INTERFERENCE;

NEMATODA;

ACETYLCYSTEINE; ALPHA-SYNUCLEIN; ANIMALS; APOPTOSIS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM; CALCIUM-TRANSPORTING ATPASES; HUMANS; MANGANESE; MODELS, BIOLOGICAL; OXIDATIVE STRESS; PARKINSON DISEASE; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; RNA, SMALL INTERFERING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84873703372     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2012.142     Document Type: Article

References (61)

1. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M. Alpha-synuclein in Lewy bodies. Nature 1997; 388: 839-840.
2. Kruger R, Kuhn W, Mu ller T, Woitalla D, Graeber M, Ko sel S et al. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat.Genet 1998; 18: 106-108.
3. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J et al. alpha-Synuclein locus triplication causes Parkinson's disease. Science 2003; 302: 841.
4. Zarranz JJ, Alegre J, Gomez-Esteban JC, Lezcano E, Ros R, Ampuero I et al. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann.Neurol. 2004; 55: 164-173.
5. Farrer M, Kachergus J, Forno L, Lincoln S, Wang DS, Hulihan M et al. Comparison of kindreds with parkinsonism and alpha-synuclein genomic multiplications. Ann. Neurol 2004; 55: 174-179.
6. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 1997; 276: 2045-2047.
7. Chan CS, Guzman JN, Ilijic E, Mercer JN, Rick C, Tkatch T et al. 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature 2007; 447: 1081-1086.
8. Cal? T, Ottolini D, Brini M. Mitochondria, calcium, and endoplasmic reticulum stress in Parkinson's disease. Biofactors 2011; 37: 228-240.
9. Lowe R, Pountney DL, Jensen PH, Gai WP, Voelcker NH. Calcium(II) selectively induces alpha-synuclein annular oligomers via interaction with the C-terminal domain. Protein Sci 2004; 13: 3245-3252.
10. Adamczyk A, Strosznajder JB. Alpha-synuclein potentiates Ca2 influx through voltagedependent Ca2 channels. Neuroreport 2006; 17: 1883-1886.
11. Hettiarachchi NT, Parker A, Dallas ML, Pennington K, Hung CC, Pearson HA et al. alpha-Synuclein modulation of Ca2 signaling in human neuroblastoma (SH-SY5Y) cells. J Neurochem 2009; 111: 1192-1201.
12. Danzer KM, Haasen D, Karow AR, Moussaud S, Habeck M, Giese A et al. Different species of alpha-synuclein oligomers induce calcium influx and seeding. J Neurosci 2007; 27: 9220-9232.
13. Khurana V, Lindquist S. Modelling neurodegeneration in Saccharomyces cerevisiae: why cook with baker's yeast? Nat Rev Neurosci 2010; 11: 436-449.
14. Bu ttner S, Bitto A, Ring J, Augsten M, Zabrocki P, Eisenberg T et al. Functional mitochondria are required for alpha-synuclein toxicity in aging yeast. J Biol Chem 2008; 283: 7554-7560.
15. Outeiro TF, Lindquist S. Yeast cells provide insight into alpha-synuclein biology and pathobiology. Science 2003; 302: 1772-1775.
16. Cooper AA, Gitler AD, Cashikar A, Haynes CM, Hill KJ, Bhullar B et al. Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 2006; 313: 324-328.
17. Zabrocki P, Bastiaens I, Delay C, Bammens T, Ghillebert R, Pellens K et al. Phosphorylation, lipid raft interaction and traffic of alpha-synuclein in a yeast model for Parkinson. Biochim Biophys Acta 2008; 1783: 1767-1780.
18. Ton V-K, Rao R. Functional expression of heterologous proteins in yeast: insights into Ca2 signaling and Ca2-transporting ATPases. Am J Physiol Cell Physiol 2004; 287: C580-C589.
19. Cronin SR, Rao R, Hampton RY. Cod1p/Spf1p is a P-type ATPase involved in ER function and Ca2 homeostasis. J Cell Biol 2002; 157: 1017-1028.
20. Cui J, Kaandorp JA, Sloot PMA, Lloyd CM, Filatov MV. Calcium homeostasis and signaling in yeast cells and cardiac myocytes. FEMS Yeast Res 2009; 9: 1137-1147.
21. Abou-Sleiman PM, Muqit MM, Wood NW. Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat Rev Neurosci 2006; 7: 207-219.
22. Jenner P. Oxidative stress in Parkinson's disease. Ann Neurol 2003; 53(Suppl 3): S26-S36; discussion S36-8., S26-S36.
23. Jomova K, Vondrakova D, Lawson M, Valko M. Metals, oxidative stress and neurodegenerative disorders. Mol Cell Biochem 2010; 345: 91-104.
24. Sun L, Gu L, Wang S, Yuan J, Yang H, Zhu J et al. N-acetylcysteine protects against apoptosis through modulation of group I metabotropic glutamate receptor activity. PLoS ONE 2012; 7: e32503.
25. Berman AE, Chan WY, Brennan AM, Reyes RC, Adler BL, Suh SW et al. N-acetylcysteine prevents loss of dopaminergic neurons in the EAAC1-/- mouse. Ann Neurol 2011; 69: 509-520.
26. Clark J, Clore EL, Zheng K, Adame A, Masliah E, Simon DK. Oral N-acetyl-cysteine attenuates loss of dopaminergic terminals in alpha-synuclein overexpressing mice. PLoS ONE 2010; 5: e12333.
27. Bagh MB, Maiti AK, Jana S, Banerjee K, Roy A, Chakrabarti S. Quinone and oxyradical scavenging properties of N-acetylcysteine prevent dopamine mediated inhibition of Na, K-ATPase and mitochondrial electron transport chain activity in rat brain: implications in the neuroprotective therapy of Parkinson's disease. Free Radic Res 2008; 42: 574-581.
28. Yen K, Gitsham P,Wishart J, Oliver SG, Zhang N. An improved tetO promoter replacement system for regulating the expression of yeast genes. Yeast 2003; 20: 1255-1262.
29. Bonilla M, Nastase KK, Cunningham KW. Essential role of calcineurin in response to endoplasmic reticulum stress. EMBO J 2002; 21: 2343-2353.
30. Miseta A, Fu L, Kellermayer R, Buckley J, Bedwell DM. The Golgi apparatus plays a significant role in the maintenance of Ca2 homeostasis in the vps33Delta vacuolar biogenesis mutant of Saccharomyces cerevisiae. J Biol Chem 1999; 274: 5939-5947.
31. Martin DC, Kim H, Mackin NA, Maldonado-Baez L, Evangelista CC Jr, Beaudry VG et al. New regulators of a high affinity Ca2 influx system revealed through a genome-wide screen in yeast. J Biol Chem 2011; 286: 10744-10754.
32. Locke EG, Bonilla M, Liang L, Takita Y, Cunningham KW. A homolog of voltage-gated Ca(2) channels stimulated by depletion of secretory Ca(2) in yeast. Mol Cell Biol 2000; 20: 6686-6694.
33. Du rr G, Strayle J, Plemper R, Elbs S, Klee SK, Catty P et al. The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca2 and Mn2 required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation. Mol Biol Cell 1998; 9: 1149-1162.
34. Cunningham KW. Acidic calcium stores of Saccharomyces cerevisiae. Cell Calcium 2011; 50: 129-138.
35. Ton V-K, Mandal D, Vahadji C, Rao R. Functional expression in yeast of the human secretory pathway Ca(2), Mn(2)-ATPase defective in Hailey-Hailey disease. J Biol Chem 2002; 277: 6422-6427.
36. Mandal D, Woolf TB, Rao R
37. Residue Asp778 is essential for cation transport. J Biol Chem 2000; 275: 23933-23938.
38. Olanow CW. Manganese-induced parkinsonism and Parkinson's disease. Ann N Y Acad Sci 2004; 1012: 209-223.
39. Pal PK, Samii A, Calne DB. Manganese neurotoxicity: a review of clinical features, imaging and pathology. Neurotoxicology 1999; 20: 227-238.
40. Gitler AD, Chesi A, Geddie ML, Strathearn KE, Hamamichi S, Hill KJ et al. Alpha-synuclein is part of a diverse and highly conserved interaction network that includes PARK9 and manganese toxicity. Nat Genet 2009; 41: 308-315.
41. Covy JP, Giasson BI. a-Synuclein, leucine-rich repeat kinase-2, and manganese in the pathogenesis of Parkinson disease. Neurotoxicology 2011; 32: 622-629.
42. Covy JP, Waxman EA, Giasson BI. Characterization of cellular protective effects of ATP13A2/PARK9 expression and alterations resulting from pathogenic mutants. J Neurosci Res 2012; 90: 2306-2316.
43. Tan J, Zhang T, Jiang L, Chi J, Hu D, Pan Q et al. Regulation of intracellular manganese homeostasis by Kufor-Rakeb syndrome-associated ATP13A2 protein. J Biol Chem 2011; 286: 29654-29662.
44. Settivari R, Levora J, Nass R. The divalent metal transporter homologues SMF-1/2 mediate dopamine neuron sensitivity in caenorhabditis elegans models of manganism and parkinson disease. J Biol Chem 2009; 284: 35758-35768.
45. Wei Y, Marchi V, Wang R, Rao R. An N-terminal EF hand-like motif modulates ion transport by Pmr1, the yeast Golgi Ca(2)/Mn(2)-ATPase. Biochemistry 1999; 38: 14534-14541.
46. Nakai J, Ohkura M, Imoto K. A high signal-to-noise Ca(2) probe composed of a single green fluorescent protein. Nat Biotechnol 2001; 19: 137-141.
47. Feany MB, Bender WW. A Drosophila model of Parkinson's disease. Nature 2000; 404: 394-398.
48. Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 2003; 4: 552-565.
49. Wojda U, Salinska E, Kuznicki J. Calcium ions in neuronal degeneration. IUBMB Life 2008; 60: 575-590.
50. Schapira AHV, Gegg M. Mitochondrial contribution to Parkinson's disease pathogenesis. Parkinsons Dis 2011; 2011: 159160.
51. Protter D, Lang C, Cooper AA. aSynuclein and mitochondrial dysfunction: a pathogenic partnership in Parkinson's disease? Parkinsons Dis 2012; 2012: 829207.
52. Kamp F, Exner N, Lutz AK, Wender N, Hegermann J, Brunner B et al. Inhibition of mitochondrial fusion by a-synuclein is rescued by PINK1, Parkin and DJ-1. EMBO J 2010; 29: 3571-3589.
53. Niedenthal RK, Riles L, Johnston M, Hegemann JH. Green fluorescent protein as a marker for gene expression and subcellular localization in budding yeast. Yeast 1996; 12: 773-786.
54. Madeo F, Herker E, Maldener C, Wissing S, La chelt S, Herlan M et al. A caspase-related protease regulates apoptosis in yeast. Mol Cell 2002; 9: 911-917.
55. Herker E, Jungwirth H, Lehmann KA, Maldener C, Fro hlich KU, Wissing S et al. Chronological aging leads to apoptosis in yeast. J Cell Biol 2004; 164: 501-507.
56. Bu ttner S, Eisenberg T, Carmona-Gutierrez D, Ruli D, Knauer H, Ruckenstuhl C et al. Endonuclease G regulates budding yeast life and death. Mol Cell 2007; 25: 233-246.
57. Kellermayer R, Szigeti R, Kellermayer M, Miseta A. The intracellular dissipation of cytosolic calcium following glucose re-addition to carbohydrate depleted Saccharomyces cerevisiae. FEBS Lett 2004; 571: 55-60.
58. Gupta SS, Ton VK, Beaudry V, Rulli S, Cunningham K, Rao R. Antifungal activity of amiodarone is mediated by disruption of calcium homeostasis. J Biol Chem 2003; 278: 28831-28839.
59. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974; 77: 71-94.
60. Qiao L, Hamamichi S, Caldwell KA, Caldwell GA, Yacoubian TA, Wilson S et al. Lysosomal enzyme cathepsin D protects against alpha-synuclein aggregation and toxicity. Mol Brain 2008; 1: 17.
61. Owald D, Fouquet W, Schmidt M, Wichmann C, Mertel S, Depner H et al. A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila. J Cell Biol 2010; 188: 565-579.