Protein carbonylation and aggregation precede neuronal apoptosis induced by partial glutathione depletion

ASN Neuro

Volumn 4, Issue 3, 2012, Pages 161-174

  Dasgupta, Anushka ^a   Zheng, Jianzheng ^a   Bizzozero, Oscar A ^a  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

Author keywords

Apoptosis; Cell death; Glutathione depletion; Proteasome; Protein aggregation; Protein carbonylation

Indexed keywords

CALPAIN; CARBONYL DERIVATIVE; CASPASE INHIBITOR; CYCLOSPORIN A; GLUTATHIONE; HISTIDINE; HISTIDINE HYDRAZIDE; HYDRALAZINE; MALEIC ACID DIETHYL ESTER; METHOXYAMINE; PROTEASOME; PROTEIN CARBONYL; SCAVENGER; UNCLASSIFIED DRUG; ZVAD FMK;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL STRAIN; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; ENZYME DEGRADATION; IMMUNOCYTOCHEMISTRY; LIPID PEROXIDATION; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NONHUMAN; OXIDATIVE STRESS; PROTEIN AGGREGATION; PROTEIN CARBONYLATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; RAT; ANIMAL; CELL INCLUSION; DRUG EFFECT; METABOLISM; MOUSE; NERVE DEGENERATION; PATHOLOGY; PC12 CELL; PHYSIOLOGY; PRIMARY CELL CULTURE;

ANIMALS; APOPTOSIS; GLUTATHIONE; INCLUSION BODIES; MICE; NERVE DEGENERATION; PC12 CELLS; PRIMARY CELL CULTURE; PROTEIN CARBONYLATION; RATS;

EID: 84860576100     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1042/AN20110064     Document Type: Article

References (55)

1. Altman SA, Randers L, Rao G (1993) Comparison of trypan blue dye exclusion and fluorometric assays for mammalian cell viability determinations. Biotechnol Prog 9:671-674.
2. Armstrong JS, Jones DP (2002) Glutathione depletion enforces the mitochondrial permeability transition and causes cell death in Bcl-2-overexpressing HL60 cells. FASEB J 16:1263-1265.
3. Aksenov MY, Aksenova MV, Butterfield DA, Geddes JW, Markesbery WR (2001) Protein oxidation in the brain in Alzheimer's disease. Neuroscience 103:373-383.
4. Bizzozero OA (2009) Protein carbonylation in neurodegenerative and demyelinating CNS diseases. In Handbook of Neurochemistry and Molecular Neurobiology (Lajtha A, Banik N, Ray S, eds), pp. 543-562, Springer, New York, NY.
5. Bizzozero OA, Dejesus G, Callahan K, Pastuszyn A (2005) Elevated protein carbonylation in the brain white matter and gray matter of patients with multiple sclerosis. J Neurosci Res 81:687-695.
6. Bizzozero OA, Ziegler JL, De Jesus G, Bolognani F (2006) Acute depletion of reduced glutathione causes extensive carbonylation of rat brain proteins. J Neurosci Res 83:656-667.
7. Bota DA, Davies KJ (2002) Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat Cell Biol 4:674-680.
8. Buchmüller-Rouiller Y, Corrandin SB, Smith J, Schneider P, Ransijn A, Jongeneel CV, Mauel J (1995) Role of glutathione in macrophage activation: effect of cellular glutathione depletion on nitrite production and leishmanicidal activity. Cell Immunol 164:73-80.
9. Cahuana GM, Tejedo JR, Jiménez J, Rami{dotless}írez R, Sobrino F, Bedoya FJ (2004) Nitric oxide-induced carbonylation of Bcl-2, GAPDH and ANT precedes apoptotic events in insulin-secreting RINm5F cells. Exp Cell Res 293: 22-30.
10. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ (2003) Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278:36027-36031.
11. Dalle-Donne I, Rossi R, Giustarini D, Gagliano N, Lusini L, Milzani A, Di Simplicio P, Colombo R. (2001) Actin carbonylation: from a simple marker of protein oxidation to relevant signs of severe functional impairment. Free Radical Biol Med 31:1075-1083.
12. Dasgupta A, Bizzozero OA (2011) Positive correlation between protein carbonylation and apoptosis in EAE. Trans Am Soc Neurochem 42: PSM08-01.
13. Davies MJ (2005) The oxidative environment and protein damage. Biochim Biophys Acta 1703:93-109.
14. Demasi M, Davies KJ (2003) Proteasome inhibitors induce intracellular protein aggregation and cell death by an oxygen-dependent mechanism. FEBS Lett 542:89-94.
15. Divald A, Powell SR (2006) Proteasome mediates removal of proteins oxidized during myocardial ischemia. Free Radical Biol Med 40:156-164.
16. Eguchi Y, Shimizu S, Tsujimoto Y (1997) Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res 57:1835-1840.
17. England K, O'Driscoll C, Cotter TG (2004) Carbonylation of glycolytic proteins is a key response to drug-induced oxidative stress and apoptosis. Cell Death Differ 11:252-260.
18. Ferrante RJ, Browne SE, Shinobu LA, Bowling AC, Baik MJ, MacGarvey U, Kowall NW, Brown RH, Beal MF (1997) Evidence of increased oxidative damage in both sporadic and familial amyotrophic lateral sclerosis. J Neurochem 69:2064-2074.
19. Ferrington DA, Husom AD, Thompson LV (2005) Altered proteasome structure, function and oxidation in aged muscle. FASEB J 19:644-646.
20. Floor E, Wetzel MG (1998) Increased protein oxidation in human sustantia nigra pars compacta in comparison with basal ganglia and prefrontal cortex measured with an improved dinitrophenylhydrazine assay. J Neurochem 70:268-275.
21. Freeman ML, Meredith MJ (1988) Subcellular localization of glutathione and thermal sensitivity. Radiat Res 115:461-471.
22. Fucci L, Oliver CN, Coon MJ, Stadtman ER (1983) Inactivation of key metabolic enzymes by mixed-function oxidation reactions: possible implication in protein turnover and ageing. Proc Natl Acad Sci USA 80:1521-1525.
23. Gao G, Xing J, Xiao X, Liou AF, Gao Y, Yin XM, Clark RS, Graham SH, Chen J (2007) Critical role of calpain I in mitochondrial release of apoptosis-inducing factor in ischemic neuronal injury. J Neurosci 27: 9278-9293.
24. Grune T, Reinheckel T, Davies KJ (1997) Degradation of oxidized proteins in mammalian cells. FASEB J 11:526-534.
25. Gupta A, Datta M, Shukla GS (2000) Cerebral antioxidant status and free radical generation following glutathione depletion and subsequent recovery. Mol Cell Biochem 209:55-61.
26. Guyton MK, Wingrave JM, Yallapragada AV, Wilford GG, Sribnick EA, Matzelle DD, Tyor WR, Ray SK, Banik NL (2005) Upregulation of calpain correlates with increased neurodegeneration in acute experimental autoimmune encephalomyelitis. J Neurosci Res 81:53-61.
27. Harms KM, Li L, Cunningham LA (2010) Murine neural stem/progenitor cells protect neurons against ischemia by HIF-1a-Regulated VEGF signaling. PLoS ONE 5:e9767.
28. Hassen GW, Feliberti J, Kesner L, Stracher A, Mokhtarian F (2006) A novel calpain inhibitor for the treatment of acute experimental autoimmune encephalomyelitis. J Neuroimmunol 180:135-146.
29. Jomova K, Vondrakova D, Lawson M, Valko M (2010) Msetals, oxidative stress and neurodegenerative disorders. Mol Cell Biochem 345:91-104.
30. Kisselev AF, Goldberg AL (2001) Proteasome inhibitors: from research tools to drug candidates. Chem Biol 8:739-758.
31. Lambert AJ, Brand MD (2004) Superoxide production by NADH:ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane. Biochem J 382:511-517.
32. Lewerenz J, Maher P (2011) Control of redox state and redox signaling by neural antioxidant systems. Antiox Redox Signal 14:1449-1465.
33. Lin S, Lisi L, Russo CD, Polak PE, Sharp A, Weinberg G, Kalinin S, Feinstein DL (2011) The anti-inflammatory effects of dimethyl fumarate in astrocytes involve glutathione and haem oxygenase-1. ASN NEURO 3(2):art:e00055. doi:10.1042/AN20100033.
34. Luo S, Wehr NN (2009) Protein carbonylation: avoiding pitfalls in the 2,4-dinitrophenylhydrazine assay. Redox Rep 14:159-166.
35. Magi B, Ettorre A, Liberatori S, Bini L, Andreassi M, Frosali S, Neri P, Pallini V (2004) Selectivity of protein carbonylation in the apoptotic response to oxidative stress associated with photodynamic therapy: a cell biochemical and proteomic investigation. Cell Death Differ 11: 842-852.
36. Maisonneuve E, Ezraty B, Dukan S (2008) Protein aggregates: an aging factor involved in cell death. J Bacteriol 190:6070-6075.
37. Mirzaei H, Regnier F (2008) Protein:protein aggregation induced by protein oxidation. J Chromatogr 873:8-14.
38. Nagai H, Matsumaru K, Feng G, Kaplowitz N (2002) Sensitization to tumor necrosis factor-a-induced apoptosis in cultured mouse hepatocytes. Hepatology 36:55-64.
39. Namura S, Zhu J, Fink K, Endres M, Srinivasan A, Tomaselli K, Yuan J, Moskowitz MA (1998) Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J Neurosci 18:3659-3668.
40. Nyström T (2005) Role of oxidative carbonylation in protein quality control and senescence. EMBO J 24:1311-1317.
41. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351-358.
42. Olzscha H, Schermann SM, Woerner AC, Pinket S, Hecht MH, Tartaglia GG, Vendruscolo M, Hayer-Hartl M, Hartl FU, Vabulas RM (2011) Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 144:67-78.
43. Petronilli V, Costantini P, Scorrano L, Colonna R, Passamonti S, Bernardi P (1994) The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction state of vicinal thiols. Increase of the gating potential by oxidants and its reversal by reducing agents. J Biol Chem 269:16638-16642.
44. Pickering AM, Koop AL, Teoh CY, Ermak G, Grune T, Davies KJ (2010) The immunoproteasome, the 20S proteasome and the PA28ab proteasome regulator are oxidative-stress-adaptive proteolytic complexes. Biochem J 432:585-594.
45. Reynolds A, Laurie C, Mosley RL, Gendelman HE (2007) Oxidative stress and the pathogenesis of neurodegenerative disorders. Int Rev Neurobiol 82:297-325.
46. Rinaudo MT, Piccinini M (2007) Immunoproteasome activity in the nervous system. In Handbook of Neurochemistry and Molecular Neurobiology: Neuroimmunology, Vol. 12 (Lajtha A, Galoya A, Besedorsky H, eds), pp. 223-235, Springer, New York, NY.
47. Rodgers KJ, Dean RT (2003) Assessment of proteasome activity in cell lysates and tissue homogenates using peptide substrates. Int J Biochem Cell Biol 35:716-727.
48. Shaik IH, Mehvar R (2006) Rapid determination of reduced and oxidized glutathione levels using a new thiol-masking reagent and the enzymatic recycling method: application to the rat liver and bile samples. Anal Bioanal Chem 385:105-113.
49. Shen D, Dalton TP, Nebert DW, Shertzer HG (2005) Glutathione redox state regulates mitochondrial reactive oxygen production. J Biol Chem 280:25305-25312.
50. Shringarpure R, Grune T, Mehlhase J, Davies KJ (2003) Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J Biol Chem 278:311-318.
51. Smerjac SM, Bizzozero OA (2008) Cytoskeletal protein carbonylation and degradation in experimental autoimmune encephalomyelitis. J Neurochem 105:763-772.
52. Starke PE, Oliver CN, Stadtman ER (1987) Modification of hepatic proteins in rats exposed to high oxygen concentration. FASEB J 1:36-39.
53. 2+-induced permeabilization promotes free radical release from rat brain mitochondria with partially inhibited complex I. J Neurochem 93:526-537.
54. Zheng J, Bizzozero OA (2010a) Traditional reactive carbonyl scavengers do not prevent the carbonylation of brain proteins induced by acute glutathione depletion. Free Radical Res 44:258-266.
55. Zheng J, Bizzozero OA (2010b) Accumulation of protein carbonyls within cerebellar astrocytes in murine experimental autoimmune encephalomyelitis. J Neurosci Res 88:3376-3385.