Specificity and regulation of casein kinase-mediated phosphorylation of α-synuclein

Journal of Neuropathology and Experimental Neurology

Volumn 67, Issue 5, 2008, Pages 402-416

  Waxman, Elisa A ^a   Giasson, Benoit I ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

synuclein; Casein kinase; Fibrillation; Parkinson disease; Phosphorylation; PP2C; Proteasome

Indexed keywords

ALPHA SYNUCLEIN; CASEIN KINASE; SERINE;

ACTIN POLYMERIZATION; ADULT; AGED; ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MOUSE; NERVE CELL CULTURE; NEUROFIBRILLARY TANGLE; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; TISSUE SECTION; TRANSGENIC MOUSE;

ADULT; AGED; AGED, 80 AND OVER; ALPHA-SYNUCLEIN; ANIMALS; BINDING SITES; CASEIN KINASE II; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; INCLUSION BODIES; MALE; MICE; MICE, TRANSGENIC; MIDDLE AGED; NEURONS; PARKINSON DISEASE; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; SERINE; SUBSTANTIA NIGRA; SUBSTRATE SPECIFICITY; UP-REGULATION;

EID: 43249108653     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3186fc995     Document Type: Article

References (64)

1. Goedert M. Alpha-synuclein and neurodegenerative diseases. Nat Rev Neurosci 2001;2:492-501
2. von Bohlen Und HO. Synucleins and their relationship to Parkinson's disease. Cell Tissue Res 2004;318:163-74
3. Lee VM, Trojanowski JQ. Mechanisms of Parkinson's disease linked to pathological alpha-synuclein: New targets for drug discovery. Neuron 2006;52:33-38
4. Sidhu A, Wersinger C, Vernier P. Does alpha-synuclein modulate dopaminergic synaptic content and tone at the synapse? FASEB J 2004;18:637-47
5. Forman MS, Lee VM, Trojanowski JQ. Nosology of Parkinson's disease: Looking for the way out of a quagmire. Neuron 2005;47:479-82
6. Polymeropoulos MH, Lavedan C, Leroy E, et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 1997;276:2045-47
7. Duda JE, Giasson BI, Gur TL, et al. Immunohistochemical and biochemical studies demonstrate a distinct profile of alpha-synuclein permutations in multiple system atrophy. J Neuropathol Exp Neurol 2000;59:830-41
8. Lippa CF, Schmidt ML, Lee VM, et al. Dementia with Lewy bodies. Neurology 1999;52:893
9. Spillantini MG, Schmidt ML, Lee VMY, et al. Alpha-synuclein in Lewy bodies. Nature 1997;388:839-40
10. Spillantini MG, Crowther RA, Jakes R, et al. Filamentous alpha-synuclein inclusions link multiple system atrophy with Parkinson's disease and dementia with Lewy bodies. Neurosci Lett 1998;251:205-8
11. Tu PH, Galvin JE, Baba M, et al. Glial cytoplasmic inclusions in white matter oligodendrocytes of multiple system atrophy brains contain insoluble alpha-synuclein. Ann Neurol 1998;44:415-22
12. Nakajo S, Tsukada K, Omata K, et al. A new brain-specific 14-kDa protein is a phosphoprotein. Its complete amino acid sequence and evidence for phosphorylation. Eur J Biochem 1993;217:1057-63
13. Nakajo S, Shioda S, Nakai Y, et al. Localization of phosphoneuroprotein 14 (PNP 14) and its mRNA expression in rat brain determined by immunocytochemistry and in situ hybridization. Brain Res Mol Brain Res 1994;27:81-86
14. Shibayama-Imazu T, Okahashi I, Omata K, et al. Cell and tissue distribution and developmental change of neuron specific 14 kDa protein (phosphoneuroprotein 14). Brain Res 1993;622:17-25
15. Okochi M, Walter J, Koyama A, et al. Constitutive phosphorylation of the Parkinson's disease associated alpha-synuclein. J Biol Chem 2000;275:390-97
16. Arawaka S, Wada M, Goto S, et al. The role of G-protein-coupled receptor kinase 5 in pathogenesis of sporadic Parkinson's disease. J Neurosci 2006;26:9227-38
17. Kim EJ, Sung JY, Lee HJ, et al. Dyrk1A phosphorylates alpha-synuclein and enhances intracellular inclusion formation. J Biol Chem 2006;281:33250-57
18. Pronin AN, Morris AJ, Surguchov A, et al. Synucleins are a novel class of substrates for G protein-coupled receptor kinases. J Biol Chem 2000;275:26515-22
19. Fujiwara H, Hasegawa M, Dohmae N, et al. α-Synuclein is phosphorylated in synucleinopathy lesions. Nat Cell Biol 2002;4:160-64
20. Anderson JP, Walker DE, Goldstein JM, et al. Phosphorylation of Ser-129 is the dominant pathological modification of alpha-synuclein in familial and sporadic Lewy body disease. J Biol Chem 2006;281:29739-52
21. Kahle PJ, Neumann M, Ozmen L, et al. Hyperphosphorylation and insolubility of alpha-synuclein in transgenic mouse oligodendrocytes. EMBO Rep 2002;3:583-88
22. Nishie M, Mori F, Fujiwara H, et al. Accumulation of phosphorylated alpha-synuclein in the brain and peripheral ganglia of patients with multiple system atrophy. Acta Neuropathol (Berl) 2004;107:292-98
23. Neumann M, Kahle PJ, Giasson BI, et al. Misfolded proteinase K-resistant hyperphosphorylated alpha-synuclein in aged transgenic mice with locomotor deterioration and in human alpha-synucleinopathies. J Clin Invest 2002;110:1429-39
24. Smith WW, Margolis RL, Li X, et al. Alpha-synuclein phosphorylation enhances eosinophilic cytoplasmic inclusion formation in SH-SY5Y cells. J Neurosci 2005;25:5544-52
25. Lee G, Tanaka M, Park K, et al. Casein kinase II-mediated phosphorylation regulates alpha-synuclein/synphilin-1 interaction and inclusion body formation. J Biol Chem 2004;279:6834-39
26. Chen L, Feany MB. Alpha-synuclein phosphorylation controls neurotoxicity and inclusion formation in a Drosophila model of Parkinson disease. Nat Neurosci 2005;8:657-63
27. Giasson BI, Jakes R, Goedert M, et al. A panel of epitope-specific antibodies detects protein domains distributed throughout human alpha-synuclein in Lewy bodies of Parkinson's disease. J Neurosci Res 2000;59:528-33
28. Giasson BI, Duda JE, Murray IV, et al. Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 2000;290:985-89
29. Duda JE, Giasson BI, Mabon ME, et al. Novel antibodies to synuclein show abundant striatal pathology in Lewy body diseases. Ann Neurol 2002;52:205-10
30. Otvos L Jr, Feiner L, Lang E, et al. Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404. J Neurosci Res 1994;39:669-73
31. Kosik KS, Orecchio LD, Binder L, et al. Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1988;1:817-25
32. Greenbaum EA, Graves CL, Mishizen-Eberz AJ, et al. The E46K mutation in alpha-synuclein increases amyloid fibril formation. J Biol Chem 2005;280:7800-7807
33. Giasson BI, Covy JP, Bonini NM, et al. Biochemical and pathological characterization of Lrrk2. Ann Neurol 2006;59:315-22
34. Giasson BI, Duda JE, Quinn SM, et al. Neuronal α-synucleinopathy with severe movement disorder in mice expressing A53T human α-synuclein. Neuron 2002;34:521-33
35. Giasson BI, Murray IVJ, Trojanowski JQ, et al. A hydrophobic stretch of 12 amino acid residues in the middle of alpha-synuclein is essential for filament assembly. J Biol Chem 2001;276:2380-86
36. Crystal AS, Giasson BI, Crowe A, et al. A comparison of amyloid fibrillogenesis using the novel fluorescent compound K114. J Neurochem 2003;86:1359-68
37. Mazzulli JR, Mishizen AJ, Giasson BI, et al. Cytosolic catechols inhibit alpha-synuclein aggregation and facilitate the formation of intracellular soluble oligomeric intermediates. J Neurosci 2006;26:10068-78
38. Pagano MA, Meggio F, Ruzzene M, et al. 2-Dimethylamino-4,5,6,7- tetrabromo-1H-benzimidazole: A novel powerful and selective inhibitor of protein kinase CK2. Biochem Biophys Res Commun 2004;321:1040-44
39. Pagano MA, Andrzejewska M, Ruzzene M, et al. Optimization of protein kinase CK2 inhibitors derived from 4,5,6,7-tetrabromobenzimidazole. J Med Chem 2004;47:6239-47
40. Pagano MA, Poletto G, DiMaira G, et al. Tetrabromocinnamic acid (TBCA) and related compounds represent a new class of specific protein kinase CK2 inhibitors. Chembiochem 2007;8:129-39
41. Baba M, Nakajo S, Tu PH, et al. Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am J Pathol 1998;152:879-84
42. Sampathu DM, Giasson BI, Pawlyk AC, et al. Ubiquitination of alpha-synuclein is not required for formation of pathological inclusions in alpha-synucleinopathies. Am J Pathol 2003;163:91-100
43. Liu F, Grundke-Iqbal I, Iqbal K, et al. Contributions of protein phosphatases PP1, PP2A, PP2B and PP5 to the regulation of tau phosphorylation. Eur J Neurosci 2005;22:1942-50
44. Yamamoto H, Hasegawa M, Ono T, et al. Dephosphorylation of fetal-tau and paired helical filaments-tau by protein phosphatases 1 and 2A and calcineurin. J Biochem (Tokyo) 1995;118:1224-31
45. Gong CX, Grundke-Iqbal I, Iqbal K. Dephosphorylation of Alzheimer's disease abnormally phosphorylated tau by protein phosphatase-2A. Neuroscience 1994;61:765-72
46. Gong CX, Grundke-Iqbal I, Damuni Z, et al. Dephosphorylation of microtubule-associated protein tau by protein phosphatase-1 and -2C and its implication in Alzheimer disease. FEBS Lett 1994;341:94-98
47. Gong CX, Singh TJ, Grundke-Iqbal I, et al. Alzheimer's disease abnormally phosphorylated tau is dephosphorylated by protein phosphatase-2B (calcineurin). J Neurochem 1994;62:803-6
48. Zhang C, Vilk G, Canton DA, et al. Phosphorylation regulates the stability of the regulatory CK2beta subunit. Oncogene 2002;21:3754-64
49. DeVore RF, Corbett AH, Osheroff N. Phosphorylation of topoisomerase II by casein kinase II and protein kinase C: Effects on enzyme-mediated DNA cleavage/religation and sensitivity to the antineoplastic drugs etoposide and 4′-(9-acridinylamino)methane-sulfon-m-anisidide. Cancer Res 1992;52:2156-61
50. DiMaira G, Brustolon F, Bertacchini J, et al. Pharmacological inhibition of protein kinase CK2 reverts the multidrug resistance phenotype of a CEM cell line characterized by high CK2 level. Oncogene 2007;26:6915-26
51. Franck N, Le SJ, Guguen-Guillouzo C, et al. Hepatitis C virus NS2 protein is phosphorylated by the protein kinase CK2 and targeted for degradation to the proteasome. J Virol 2005;79:2700-2708
52. Kim YS, Lee JY, Son MY, et al. Phosphorylation of threonine 10 on CKBBP1/SAG/ROC2/Rbx2 by protein kinase CKII promotes the degradation of IkappaBalpha and p27Kip1. J Biol Chem 2003;278:28462-69
53. Yamada M, Iwatsubo T, Mizuno Y, et al. Overexpression of alpha-synuclein in rat substantia nigra results in loss of dopaminergic neurons, phosphorylation of alpha-synuclein and activation of caspase-9: Resemblance to pathogenetic changes in Parkinson's disease. J Neurochem 2004;91:451-61
54. Ishii A, Nonaka T, Taniguchi S, et al. Casein kinase 2 is the major enzyme in brain that phosphorylates Ser129 of human alpha-synuclein: Implication for alpha-synucleinopathies. FEBS Lett 2007;581:4711-17
55. Takahashi M, Ko LW, Kulathingal J, et al. Oxidative stress-induced phosphorylation, degradation and aggregation of alpha-synuclein are linked to upregulated CK2 and cathepsin D. Eur J Neurosci 2007;26:863-74
56. McNaught KS, Jenner P. Proteasomal function is impaired in substantia nigra in Parkinson's disease. Neurosci Lett 2001;297:191-94
57. McNaught KS, Belizaire R, Jenner P, et al. Selective loss of 20S proteasome alpha-subunits in the substantia nigra pars compacta in Parkinson's disease. Neurosci Lett 2002;326:155-58
58. McNaught KS, Jackson T, JnoBaptiste R, et al. Proteasomal dysfunction in sporadic Parkinson's disease. Neurology 2006;66:S37-S49
59. Tofaris GK, Razzaq A, Ghetti B, et al. Ubiquitination of alpha-synuclein in Lewy bodies is a pathological event not associated with impairment of proteasome function. J Biol Chem 2003;278:44405-11
60. Tofaris GK, Layfield R, Spillantini MG. Alpha-synuclein metabolism and aggregation is linked to ubiquitin-independent degradation by the proteasome. FEBS Lett 2001;509:22-26
61. Mytilineou C, McNaught KS, Shashidharan P, et al. Inhibition of proteasome activity sensitizes dopamine neurons to protein alterations and oxidative stress. J Neural Transm 2004;111:1237-51
62. Snyder H, Mensah K, Theisler C, et al. Aggregated and monomeric α-synuclein bind to the S6′ proteasomal protein and inhibit proteasomal function. J Biol Chem 2003;278:11753-59
63. Tanaka Y, Engelender S, Igarashi S, et al. Inducible expression of mutant alpha-synuclein decreases proteasome activity and increases sensitivity to mitochondria-dependent apoptosis. Hum Mol Genet 2001;10:919-26
64. Lindersson E, Beedholm R, Hojrup P, et al. Proteasomal inhibition by alpha-synuclein filaments and oligomers. J Biol Chem 2004;279:12924-34