Parkin deficiency disrupts calcium homeostasis by modulating phospholipase C signalling

FEBS Journal

Volumn 276, Issue 18, 2009, Pages 5041-5052

  Sandebring, Anna ^a,b   Dehvari, Nodi ^a   Perez Manso, Monica ^a   Thomas, Kelly Jean ^b   Karpilovski, Elena ^a   Cookson, Mark R ^b   Cowburn, Richard F ^a,c   Cedazo Mínguez, Angel ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c ASTRAZENECA R AND D   (Sweden)

Author keywords

Autosomal recessive juvenile Parkinsonism; Calcium; Parkin; Parkinson's disease; Phospholipase C

Indexed keywords

CALCIUM ION; DANTROLENE; MUTANT PROTEIN; NEOMYCIN; OXIDOPAMINE; PARKIN; PHOSPHATIDYLINOSITIDE; PHOSPHOLIPASE C; PROTEIN KINASE C ALPHA; RYANODINE RECEPTOR; SMALL INTERFERING RNA;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; HYDROLYSIS; KNOCKOUT GENE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; SIGNAL TRANSDUCTION; WILD TYPE;

CALCIUM; CELL LINE, TUMOR; DANTROLENE; HOMEOSTASIS; HUMANS; OXIDOPAMINE; PHOSPHATIDYLINOSITOLS; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE C-ALPHA; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES;

EID: 69449103790     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07201.x     Document Type: Article

References (53)

1. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN Braak E (2003) Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 24, 197 211.
2. Hasegawa T, Treis A, Patenge N, Fiesel FC, Springer W Kahle PJ (2008) Parkin protects against tyrosinase-mediated dopamine neurotoxicity by suppressing stress-activated protein kinase pathways. J Neurochem 105, 1700 1715.
3. Fallon L, Belanger CM, Corera AT, Kontogiannea M, Regan-Klapisz E, Moreau F, Voortman J, Haber M, Rouleau G, Thorarinsdottir T et al. (2006) A regulated interaction with the UIM protein Eps15 implicates parkin in EGF receptor trafficking and PI(3)K-Akt signalling. Nat Cell Biol 8, 834 842.
4. Dehvari N, Sandebring A, Flores-Morales A, Mateos L, Chuan YC, Goldberg MS, Cookson MR, Cowburn RF Cedazo-Minguez A (2008) Parkin-mediated ubiquitination regulates phospholipase C-gamma1. J Cell Mol Med, doi :.
5. Jiang H, Ren Y, Zhao J Feng J (2004) Parkin protects human dopaminergic neuroblastoma cells against dopamine-induced apoptosis. Hum Mol Genet 13, 1745 1754.
6. Darios F, Corti O, Lucking CB, Hampe C, Muriel MP, Abbas N, Gu WJ, Hirsch EC, Rooney T, Ruberg M et al. (2003) Parkin prevents mitochondrial swelling and cytochrome c release in mitochondria-dependent cell death. Hum Mol Genet 12, 517 526.
7. Petrucelli L, O'Farrell C, Lockhart PJ, Baptista M, Kehoe K, Vink L, Choi P, Wolozin B, Farrer M, Hardy J et al. (2002) Parkin protects against the toxicity associated with mutant alpha-synuclein: proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 36, 1007 1019.
8. Moore DJ, West AB, Dikeman DA, Dawson VL Dawson TM (2008) Parkin mediates the degradation-independent ubiquitination of Hsp70. J Neurochem 105, 1806 1819.
9. Dodson MW Guo M (2007) Pink1, Parkin, DJ-1 and mitochondrial dysfunction in Parkinson's disease. Curr Opin Neurobiol 17, 331 337.
10. Imai Y, Soda M Takahashi R (2000) Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitin-protein ligase activity. J Biol Chem 275, 35661 35664.
11. Imai Y, Soda M, Inoue H, Hattori N, Mizuno Y Takahashi R (2001) An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell 105, 891 902.
12. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA Nicotera P (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961 973.
13. Paschen W (2004) Endoplasmic reticulum dysfunction in brain pathology: critical role of protein synthesis. Curr Neurovasc Res 1, 173 181.
14. + channels regulate pacemaker activity in nigral dopamine neurons. Neuroreport 7, 809 814.
15. Wilson CJ Callaway JC (2000) Coupled oscillator model of the dopaminergic neuron of the substantia nigra. J Neurophysiol 83, 3084 3100.
16. Paschen W (2003) Mechanisms of neuronal cell death: diverse roles of calcium in the various subcellular compartments. Cell Calcium 34, 305 310.
17. Mattson MP (2007) Calcium and neurodegeneration. Aging Cell 6, 337 350.
18. Surmeier DJ (2007) Calcium, ageing, and neuronal vulnerability in Parkinson's disease. Lancet Neurol 6, 933 938.
19. Becker C, Jick SS Meier CR (2008) Use of antihypertensives and the risk of Parkinson disease. Neurology 70, 1438 1444.
20. Goldman RS, Finkbeiner SM Smith SJ (1991) Endothelin induces a sustained rise in intracellular calcium in hippocampal astrocytes. Neurosci Lett 123, 4 8.
21. Terzioglu M Galter D (2008) Parkinson's disease: genetic versus toxin-induced rodent models. Febs J 275, 1384 1391.
22. Wahl MI, Nishibe S, Kim JW, Kim H, Rhee SG Carpenter G (1990) Identification of two epidermal growth factor-sensitive tyrosine phosphorylation sites of phospholipase C-gamma in intact HSC-1 cells. J Biol Chem 265, 3944 3948.
23. Berridge MJ, Heslop JP, Irvine RF Brown KD (1984) Inositol trisphosphate formation and calcium mobilization in Swiss 3T3 cells in response to platelet-derived growth factor. Biochem J 222, 195 201.
24. Tvorogov D Carpenter G (2002) EGF-dependent association of phospholipase C-gamma1 with c-Cbl. Exp Cell Res 277, 86 94.
25. Parekh AB Penner R (1997) Store depletion and calcium influx. Physiol Rev 77, 901 930.
26. Steinberg SF (2008) Structural basis of protein kinase C isoform function. Physiol Rev 88, 1341 1378.
27. Cedazo-Minguez A, Bonecchi L, Winblad B, Post C, Wong EH, Cowburn RF Benatti L (1999) Nicergoline stimulates protein kinase C mediated alpha-secretase processing of the amyloid precursor protein in cultured human neuroblastoma SH-SY5Y cells. Neurochem Int 35, 307 315.
28. Lee CS, Park WJ, Ko HH Han ES (2006) Differential involvement of mitochondrial permeability transition in cytotoxicity of 1-methyl-4- phenylpyridinium and 6-hydroxydopamine. Mol Cell Biochem 289, 193 200.
29. Fujita H, Ogino T, Kobuchi H, Fujiwara T, Yano H, Akiyama J, Utsumi K Sasaki J (2006) Cell-permeable cAMP analog suppresses 6-hydroxydopamine-induced apoptosis in PC12 cells through the activation of the Akt pathway. Brain Res 1113, 10 23.
30. Rebecchi MJ Pentyala SN (2000) Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev 80, 1291 1335.
31. Kim HK, Kim JW, Zilberstein A, Margolis B, Kim JG, Schlessinger J Rhee SG (1991) PDGF stimulation of inositol phospholipid hydrolysis requires PLC-gamma 1 phosphorylation on tyrosine residues 783 and 1254. Cell 65, 435 441.
32. Bird GS, Aziz O, Lievremont JP, Wedel BJ, Trebak M, Vazquez G Putney JW Jr. (2004) Mechanisms of phospholipase C-regulated calcium entry. Curr Mol Med 4, 291 301.
33. 2+ entry. Cell 111, 529 541.
34. Caligiuri MA, Briesewitz R, Yu J, Wang L, Wei M, Arnoczky KJ, Marburger TB, Wen J, Perrotti D, Bloomfield CD et al. (2007) Novel c-CBL and CBL-b ubiquitin ligase mutations in human acute myeloid leukemia. Blood 110, 1022 1024.
35. Dunbar AJ, Gondek LP, O'Keefe CL, Makishima H, Rataul MS, Szpurka H, Sekeres MA, Wang XF, McDevitt MA Maciejewski JP (2008) 250K single nucleotide polymorphism array karyotyping identifies acquired uniparental disomy and homozygous mutations, including novel missense substitutions of c-Cbl, in myeloid malignancies. Cancer Res 68, 10349 10357.
36. Foster TC (2007) Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell 6, 319 325.
37. Bojarski L, Herms J Kuznicki J (2008) Calcium dysregulation in Alzheimer's disease. Neurochem Int 52, 621 633.
38. Marongiu R, Spencer B, Crews L, Adame A, Patrick C, Trejo M, Dallapiccola B, Valente EM Masliah E (2009) Mutant Pink1 induces mitochondrial dysfunction in a neuronal cell model of Parkinson's disease by disturbing calcium flux. J Neurochem 108, 1561 1574.
39. Chan SL Mattson MP (1999) Caspase and calpain substrates: roles in synaptic plasticity and cell death. J Neurosci Res 58, 167 190.
40. Nixon RA (2003) The calpains in aging and aging-related diseases. Ageing Res Rev 2, 407 418.
41. Lafon-Cazal M, Pietri S, Culcasi M Bockaert J (1993) NMDA-dependent superoxide production and neurotoxicity. Nature 364, 535 537.
42. Mattson MP Chan SL (2003) Calcium orchestrates apoptosis. Nat Cell Biol 5, 1041 1043.
43. 2+) signaling: old guests, new functions. Pflugers Arch 455, 375 396.
44. Lipton SA, Singel DJ Stamler JS (1994) Nitric oxide in the central nervous system. Prog Brain Res 103, 359 364.
45. Mattson MP (1998) Modification of ion homeostasis by lipid peroxidation: roles in neuronal degeneration and adaptive plasticity. Trends Neurosci 21, 53 57.
46. Dehvari N, Cedazo-Minguez A, Isacsson O, Nilsson T, Winblad B, Karlstrom H, Benedikz E Cowburn RF (2007) Presenilin dependence of phospholipase C and protein kinase C signaling. J Neurochem 102, 848 857.
47. 2-terminal kinase. J Biol Chem 283, 35783 35788.
48. Henn IH, Bouman L, Schlehe JS, Schlierf A, Schramm JE, Wegener E, Nakaso K, Culmsee C, Berninger B, Krappmann D et al. (2007) Parkin mediates neuroprotection through activation of IkappaB kinase/nuclear factor-kappaB signaling. J Neurosci 27, 1868 1878.
49. Unschuld PG, Dachsel J, Darios F, Kohlmann A, Casademunt E, Lehmann-Horn K, Dichgans M, Ruberg M, Brice A, Gasser T et al. (2006) Parkin modulates gene expression in control and ceramide-treated PC12 cells. Mol Biol Rep 33, 13 32.
50. Cookson MR (2003) Parkin's substrates and the pathways leading to neuronal damage. Neuromolecular Med 3, 1 13.
51. Ambar I Sokolovsky M (1993) Endothelin receptors stimulate both phospholipase C and phospholipase D activities in different cell lines. Eur J Pharmacol 245, 31 41.
52. Cedazo-Minguez A, Popescu BO, Ankarcrona M, Nishimura T Cowburn RF (2002) The presenilin 1 deltaE9 mutation gives enhanced basal phospholipase C activity and a resultant increase in intracellular calcium concentrations. J Biol Chem 277, 36646 36655.
53. Popescu BO, Cedazo-Minguez A, Benedikz E, Nishimura T, Winblad B, Ankarcrona M Cowburn RF (2004) Gamma-secretase activity of presenilin 1 regulates acetylcholine muscarinic receptor-mediated signal transduction. J Biol Chem 279, 6455 6464.