Caspase-3-dependent proteolytic cleavage of protein kinase Cδ is essential for oxidative stress-mediated dopaminergic cell death after exposure to methylcyclopentadienyl manganese tricarbonyl

Journal of Neuroscience

Volumn 22, Issue 5, 2002, Pages 1738-1751

  Anantharam, Vellareddy ^a   Kitazawa, Masashi ^a   Wagner, Jarrad ^b   Kaul, Siddharth ^a   Kanthasamy, Anumantha G ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; Dopaminergic degeneration; Environmental factors; Manganese; Oxidative stress; Parkinson's disease

Indexed keywords

BENZYLOXYCARBONYLASPARTYLGLUTAMYLVALYLASPARTYL FLUOROMETHYL KETONE; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3; CASPASE 8; CASPASE 9; CASPASE INHIBITOR; CYSTEINE PROTEINASE; CYTOCHROME C; DNA FRAGMENT; DOPAMINE; LACTATE DEHYDROGENASE; MANGANESE DERIVATIVE; METHYLCYCLOPENTADIENYLMANGANESE TRICARBONYL; NEUROTOXIN; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; ROTTLERIN;

APOPTOSIS; ARTICLE; CELL DEATH; CELL IMMORTALIZATION; CHROMATIN CONDENSATION; CONTROLLED STUDY; CYTOTOXICITY; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; DOSE RESPONSE; DOSE TIME EFFECT RELATION; ENVIRONMENTAL FACTOR; ENZYMATIC ASSAY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LIPID PEROXIDATION; MESENCEPHALON; MITOCHONDRION; NERVE DEGENERATION; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOGENESIS; PHEOCHROMOCYTOMA CELL; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN DEGRADATION; RISK FACTOR;

EID: 0036523088     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-05-01738.2002     Document Type: Article

References (71)

1. Ajiro K (2000) Histone H2B phosphorylation in mammanan apoptotic cells. An association with DNA fragmentation. J Biol Chem 275:439-443.
2. Aschner M (2000) Manganese brain transport and emerging research needs. Environ Health Perspect 108 [Suppl 3]:429-432.
3. Autissier N, Dumas P, Brosseau J, Loireau A (1977) Effects of methylcyclopentadienyl manganese tricarbonyl (MMT) of rat liver mitochondria. I. Effects, in vitro, on the oxidative phosphorylation. Toxicology 7:115-122.
4. Barbeau A (1984) Manganese and extrapyramidal disorders (a critical review and tribute to Dr. George C Cotzias). Neurotoxicology 5:13-35.
5. Basu A, Woolard MD, Johnson CL (2001) Involvement of protein kinase C-delta in DNA damage-induced apoptosis. Cell Death Differ 8:899-908.
6. Bharti A, Kraeft SK, Gounder M, Pandey P, Jin S, Yuan ZM, Lees-Miller SP, Weichselbaum R, Weaver D, Chen LB, Kufe D, Kharbanda S (1998) Inactivation of DNA-dependent protein kinase by protein kinase C delta: Implications for apoptosis. Mol Cell Biol 18:6719-6728.
7. Blackstone NW, Green DR (1999) The evolution of a mechanism of cell suicide. Bioessays 21:84-88.
8. Cassarino DS, Parks JK, Parker Jr WD, Bennett Jr JP (1999) The parkinsonian neurotoxin MPP+ opens the mitochondrial permeability transition pore and releases cytochrome c in isolated mitochondria via an oxidative mechanism. Biochim Biophys Acta 1453:49-62.
9. Chen N, Ma W, Huang C, Dong Z (1999) Translocation of protein kinase Cepsilon and protein kinase C delta to membrane is required for ultraviolet B-induced activation of mitogen-activated protein kinases and apoptosis. J Biol Chem 274:15389-15394.
10. Cohen GM (1997) Caspases: The executioners of apoptosis. Biochem J 326:1-16.
11. Crompton M (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem J 341:233-249.
12. Cross T, Griffiths G, Deacon E, Sallis R, Gough M, Watters D, Lord JM (2000) PKC-delta is an apoptotic lamin kinase. Oncogene 19:2331-2337.
13. Dal Pra I, Whitfield JF, Chiarini A, Armato U (1999) Changes in nuclear protein kinase C-delta holoenzyme, its catalytic fragments, and its activity in polyomavirus-transformed pyF111 rat fibroblasts while proliferating and following exposure to apoptogenic topoisomerase-II inhibitors. Exp Cell Res 249:147-160.
14. Davies PS, Reddy H, Caivano M, Cohen P (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105.
15. Davis JM (1998) Methylcyclopentadienyl manganese tricarbonyl: Health risk uncertainties and research directions. Environ Health Perspect 106 [Suppl 1]:191-201.
16. Dempsey EC, Newton AC, Mochly-Rosen D, Fields AP, Reyland ME, Insel PA, Messing RO (2000) Protein kinase C isozymes and the regulation of diverse cell responses. Am J Physiol Lung Cell Mol Physiol 279:L429-L438.
17. Dodel RC, Du Y, Bales KR, Ling Z, Carvey PM, Paul SM (1999) Caspase-3-like proteases and 6-hydroxydopamine induced neuronal cell death. Brain Res Mol Brain Res 64:141-148.
18. Donaldson J (1987) The physiopathologic significance of manganese in brain: Its relation to schizophrenia and neurodegenerative disorders. Neurotoxicology 8:451-462.
19. Du Y, Dodel RC, Bales KR, Jemmerson R, Hamilton-Byrd E, Paul SM (1997) Involvement of a caspase-3-like cysteine protease in 1-methyl-4-phenylpyridinium-mediated apoptosis of cultured cerebellar granule neurons. J Neurochem 69:1382-1388.
20. Earnshaw WC, Martins LM, Kaufmann SH (1999) Mammalian caspases: Structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68:383-424.
21. Ferraz HB, Bertolucci PH, Pereira JS, Lima JG, Andrade LA (1988) Chronic exposure to the fungicide MANEB may produce symptoms and signs of CNS manganese intoxication. Neurology 38:550-553.
22. Fishman BE, McGinley PA, Gianutsos G (1987) Neurotoxic effects of methylcyclopentadienyl manganese tricarbonyl (MMT) in the mouse: Basis of MMT-induced seizure activity. Toxicology 45:193-201.
23. Frasch SC, Henson PM, Kailey JM, Richter DA, Janes MS, Fadok VA, Bratton DL (2000) Regulation of phospholipid scramblase activity during apoptosis and cell activation by protein kinase Cdelta. J Biol Chem 275:23065-23073.
24. Frumkin H, Solomon G (1997) Manganese in the U.S. gasoline supply. Am J Ind Med 31:107-115.
25. Gianutsos G, Murray MT (1982) Alterations in brain dopamine and GABA following inorganic or organic manganese administration. Neurotoxicology 3:75-81.
26. Gorell JM, Rybicki BA, Cole Johnson C, Peterson EL (1999) Occupational metal exposures and the risk of Parkinson's disease. Neuroepidemiology 18:303-308.
27. Gschwendt M, Muller HJ, Kielbassa K, Zang R, Kittstein W, Rincke G, Marks F (1994) Rottlerin, a novel protein kinase inhibitor. Biochem Biophys Res Commun 199:93-98.
28. Hartmann A, Hunot S, Michel PP, Muriel MP, Vyas S, Faucheux BA, Mouatt-Prigent A, Turmel H, Srinivasan A, Ruberg M, Evan GI, Agid Y, Hirsch EC (2000) Caspase-3: A vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson's disease. Proc Natl Acad Sci USA 97:2875-2880.
29. Hollensworth SB, Shen C, Sim JE, Spitz DR, Wilson GL, LeDoux SP (2000) Glial cell type-specific responses to menadione-induced oxidative stress. Free Radic Biol Med 28:1161-1174.
30. Jain N, Zhang T, Kee WH, Li W, Cao X (1999) Protein kinase C delta associates with and phosphorylates Stat3 in an interleukin-6-dependent manner. J Biol Chem 274:24392-24400.
31. Jellinger KA (2000) Cell death mechanisms in Parkinson's disease. J Neural Transm 107:1-29.
32. 2+ in catecholamine release and lethality in PC12 cells. Toxicol Lett 81:151-157.
33. Kitazawa M, Anantharam V, Kanthasamy AG (2001) Dieldrin-induced oxidative stress and neurochemical changes contribute to apoptotic cell death in dopaminergic cells. Free Radic Biol Med 31:1473-1485.
34. Kovanen PE, Junttila I, Takaluoma K, Saharinen P, Valmu L, Li W, Silvennoinen O (2000) Regulation of Jak2 tyrosine kinase by protein kinase C during macrophage differentiation of IL-3-dependent myeloid progenitor cells. Blood 95:1626-1632.
35. Langsten R, Hill K (1998) The accuracy of mothers' reports of child vaccination: Evidence from rural Egypt. Soc Sci Med 46:1205-1212.
36. Lee HC, Wei YH (2000) Mitochondrial role in life and death of the cell. J Biomed Sci 7:2-15.
37. Leist M, Volbracht C, Fava E, Nicotera P (1998) 1-Methyl-4-phenylpyridinium induces autocrine excitotoxicity, protease activation, and neuronal apoptosis. Mol Pharmacol 54:789-801.
38. Li L, Lorenzo PS, Bogi K, Blumberg PM, Yuspa SH (1999) Protein kinase Cdelta targets mitochondria, alters mitochondrial membrane potential, and induces apoptosis in normal and neoplastic keratinocytes when overexpressed by an adenoviral vector. Mol Cell Biol 19:8547-8558.
39. Liou HH, Tsai MC, Chen CJ, Jeng JS, Chang YC, Chen SY, Chen RC (1997) Environmental risk factors and Parkinson's disease: A case-control study in Taiwan. Neurology 48:1583-1588.
40. Liu X, Kim CN, Yang J, Jemmerson R, Wang. X (1996) Induction of apoptotic program in cell-free extracts: Requirement for dATP and cytochrome c. Cell 86:147-157.
41. Lynam DR, Roos JW, Pfeifer GD, Fort BF, Pullin TG (1999) Environmental effects and exposures to manganese from use of methylcyclopentadienyl manganese tricarbonyl (MMT) in gasoline. Neurotoxicology 20:145-150.
42. Maizels ET, Peters CA, Kline M, Cutler Jr RE, Shanmugam M, Hunzicker-Dunn M (1998) Heat-shock protein-25/27 phosphorylation by the delta isoform of protein kinase C. Biochem J 332:703-712.
43. Majumder PK, Pandey P, Sun X, Cheng K, Datta R, Saxena S, Kharbanda S, Kufe D (2000) Mitochondrial translocation of protein kinase C delta in phorbol ester-induced cytochrome c release and apoptosis. J Biol Chem 275:21793-21796.
44. Mena I, Marin O, Fuenzalida S, Cotzias GC (1967) Chronic manganese poisoning. Clinical picture and manganese turnover. Neurology 17:128-136.
45. Muller-Hocker J (1992) Mitochondria and ageing. Brain Pathol 2:149-158.
46. Narayanan PK, Goodwin EH, Lehnert BE (1997) Alpha particles initiate biological production of superoxide anions and hydrogen peroxide in human cells. Cancer Res 57:3963-3971.
47. Oertel WH, Kupsch A (1993) Pathogenesis and animal studies of Parkinson's disease. Curr Opin Neurol Neurosurg 6:323-332.
48. Petit PX, Susin SA, Zamzami N, Mignotte B, Kroemer G (1996) Mitochondria and programmed cell death: Back to the future. FEBS Lett 396:7-13.
49. Pongracz J, Webb P, Wang K, Deacon E, Lunn OJ, Lord JM (1999) Spontaneous neutrophil apoptosis involves caspase 3-mediated activation of protein kinase C-delta. J Biol Chem 274:37329-37334.
50. Prasad KN, Clarkson ED, La Rosa FG, Edwards-Prasad J, Freed CR (1998) Efficacy of grafted immortalized dopamine neurons in an animal model of parkinsonism: A review. Mol Genet Metab 65:1-9.
51. Pulliam L, Stubblebine M, Hyun W (1998) Quantification of neurotoxicity and identification of cellular subsets in a three-dimensional brain model. Cytometry 32:66-69.
52. Reyland ME, Anderson SM, Matassa AA, Barzen KA, Quissell DO (1999) Protein kinase C delta is essential for etoposide-induced apoptosis in salivary gland acinar cells. J Biol Chem 274:19115-19123.
53. Roels H, Lauwerys R, Buchet JP, Genet P, Sarhan MJ, Hanotiau I, de Fays M, Bernard A, Stanescu D (1987) Epidemiological survey among workers exposed to manganese: Effects on lung, central nervous system, and some biological indices. Am J Ind Med [Erratum (1987) 12:119-120] 11:307-327.
54. Sawai H, Okazaki T, Takeda Y, Tashima M, Sawada H, Okuma M, Kishi S, Umehara H, Domae N (1997) Ceramide-induced translocation of protein kinase C-delta and -epsilon to the cytosol. Implications in apoptosis. J Biol Chem 272:2452-2458.
55. Schultz SK, Andreasen NC (1999) Schizophrenia. Lancet 353:1425-1430.
56. Seidler A, Hellenbrand W, Robra BP, Vieregge P, Nischan P, Joerg J, Oertel WH, Ulm G, Schneider E (1996) Possible environmental, occupational, and other etiologic factors for Parkinson's disease: A case-control study in Germany. Neurology 46:1275-1284.
57. Shimizu S, Eguchi Y, Kamiike W, Waguri S, Uchiyama Y, Matsuda H, Tsujimoto Y (1996) Retardation of chemical hypoxia-induced necrotic cell death by Bcl-2 and ICE inhibitors: Possible involvement of common mediators in apoptotic and necrotic signal transductions. Oncogene 12:2045-2050.
58. Simon DK, Mayeux R, Marder K, Kowall NW, Beal MF, Johns DR (2000) Mitochondrial DNA mutations in complex I, tRNA genes in Parkinson's disease. Neurology 54:703-709.
59. Tan S, Wood M, Maher P (1998) Oxidative stress induces a form of programmed cell death with characteristics of both apoptosis and necrosis in neuronal cells. J Neurochem 71:95-105.
60. Tanner CM, Ottman R, Goldman SM, Ellenberg J, Chan P, Mayeux R, Langston JW (1999) Parkinson disease in twins: An etiologic study. JAMA 281:341-346.
61. Thiruchelvam M, Richfield EK, Baggs RB, Tank AW, Cory-Slechta DA (2000) The nigrostriatal dopaminergic system as a preferential target of repeated exposures to combined paraquat and maneb: Implications for Parkinson's disease. J Neurosci 20:9207-9214.
62. Vancurova I, Miskolci V, Davidson D (2001) NF-kappa B activation in tumor necrosis factor alpha-stimulated neutrophils is mediated by protein kinase Cdelta correlation to nuclear Ikappa Balpha. J Biol Chem 276:19746-19752.
63. Vassault A (1983) Lactate dehydrogenase. In: Methods of Enzymatic Analysis (Bergmeyer, ed), pp 118-126. New York: Academic.
64. Villalba M (1998) A possible role for PKC delta in cerebellar granule cells apoptosis, NeuroReport 9:2381-2385.
65. Wagner JR, Anantharam V, Gunasekar PG, Kanthasamy AG (2000) Free radical mediated mechanisms of MMT-induced dopaminergic toxicity in PC12 cells. Toxicol Sci 54:167.
66. Wang JD, Huang CC, Hwang YH, Chiang JR, Lin JM, Chen JS (1989) Manganese induced parkinsonism: An outbreak due to an unrepaired ventilation control system in a ferromanganese smelter. Br J Ind Med 46:856-859.
67. Way KJ, Chou E, King GL (2000) Identification of PKC-isoform-specific biological actions using pharmacological approaches. Trends Pharmacol Sci 21:181-187.
68. Yoshimura S, Banno Y, Nakashima S, Takenaka K, Sakai H, Nishimura Y, Sakai N, Shimizu S, Eguchi Y, Tsujimoto Y, Nozawa Y (1998) Ceramide formation leads to caspase-3 activation during hypoxic PC12 cell death. Inhibitory effects of Bcl-2 on ceramide formation and caspase-3 activation. J Biol Chem 273:6921-6927.
69. Zayed J, Thibault C, Gareau L, Kennedy G (1999) Airborne manganese particulates and methylcyclopentadienyl manganese tricarbonyl (MMT) at selected outdoor sites in Montreal. Neurotoxicology 20:151-157.
70. Zelphati O, Wang Y, Kitada S, Reed JC, Felgner PL, Corbeil J (2001) Intracellular delivery of proteins with a new lipid-mediated delivery system. J Biol Chem 276:35103-35110.
71. Zheng W, Kim H, Zhao Q (2000) Comparative toxicokinetics of manganese chloride and methylcyclopentadienyl manganese tricarbonyl (MMT) in Sprague-Dawley rats. Toxicol Sci 54:295-301.