Proteomic identification of carbonylated proteins in the monkey hippocampus after ischemia-reperfusion

Free Radical Biology and Medicine

Volumn 46, Issue 11, 2009, Pages 1472-1477

  Oikawa, Shinji ^a   Yamada, Tomoko ^a   Minohata, Toshikazu ^b   Kobayashi, Hatasu ^a,c   Furukawa, Ayako ^d   Tada Oikawa, Saeko ^a,c   Hiraku, Yusuke ^a   Murata, Mariko ^a   Kikuchi, Mitsuru ^d   Yamashima, Tetsumori ^a  

^a MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b SHIMADZU CORPORATION   (Japan)

^c Aichi Human Service Center ^*

^d KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

Author keywords

CA1; Carbonylation; Free radicals; Hsp70; Ischemia reperfusion; Proteomics; Reactive oxygen species

Indexed keywords

ARGININE; BETA ACTIN; CALPAIN; CARBONYL DERIVATIVE; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 70 1; ISOPROTEIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CARBONYLATION; CONTROLLED STUDY; HIPPOCAMPUS; LYSOSOME; MACACA; NERVE CELL NECROSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN MODIFICATION; REPERFUSION INJURY; TWO DIMENSIONAL ELECTROPHORESIS;

ACTINS; ANIMALS; CALPAIN; CELL DEATH; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; HSP72 HEAT-SHOCK PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MACACA; NERVE TISSUE PROTEINS; NEURONS; PROTEIN CARBONYLATION; PROTEIN ISOFORMS; PROTEOMICS; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY;

EID: 67349091434     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.02.029     Document Type: Article

References (45)

1. White B.C., Sullivan J.M., DeGracia D.J., O'Neil B.J., Neumar R.W., Grossman L.I., Rafols J.A., and Krause G.S. Brain ischemia and reperfusion: molecular mechanisms of neuronal injury. J. Neurol. Sci. 179 (2000) 1-33
2. Neumar R.W. Molecular mechanisms of ischemic neuronal injury. Ann. Emerg. Med. 36 (2000) 483-506
3. Di Loreto S., Zimmitti V., Sebastiani P., Cervelli C., Falone S., and Amicarelli F. Methylglyoxal causes strong weakening of detoxifying capacity and apoptotic cell death in rat hippocampal neurons. Int. J. Biochem. Cell Biol. 40 (2008) 245-257
4. Serrano F., and Klann E. Reactive oxygen species and synaptic plasticity in the aging hippocampus. Ageing Res. Rev. 3 (2004) 431-443
5. Wang X., Pal R., Chen X.W., Limpeanchob N., Kumar K.N., and Michaelis E.K. High intrinsic oxidative stress may underlie selective vulnerability of the hippocampal CA1 region. Brain Res. Mol. Brain Res. 140 (2005) 120-126
6. Vornov J.J., Park J., and Thomas A.G. Regional vulnerability to endogenous and exogenous oxidative stress in organotypic hippocampal culture. Exp. Neurol. 149 (1998) 109-122
7. Chan P.H. Oxygen radicals in focal cerebral ischemia. Brain Pathol 4 (1994) 59-65
8. Coyle J.T., and Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science 262 (1993) 689-695
9. Nakabeppu Y., Tsuchimoto D., Furuichi M., and Sakumi K. The defense mechanisms in mammalian cells against oxidative damage in nucleic acids and their involvement in the suppression of mutagenesis and cell death. Free Radic. Res. 38 (2004) 423-429
10. Castegna A., Aksenov M., Thongboonkerd V., Klein J.B., Pierce W.M., Booze R., Markesbery W.R., and Butterfield D.A. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II. Dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71. J. Neurochem. 82 (2002) 1524-1532
11. Stadtman E.R., and Berlett B.S. Reactive oxygen-mediated protein oxidation in aging and disease. Chem. Res. Toxicol. 10 (1997) 485-494
12. Kwon Y.S., Ann H.S., Nabeshima T., Shin E.J., Kim W.K., Jhoo J.H., Jhoo W.K., Wie M.B., Kim Y.S., Jang K.J., and Kim H.C. Selegiline potentiates the effects of EGb 761 in response to ischemic brain injury. Neurochem. Int. 45 (2004) 157-170
13. Yamashima T., Tonchev A.B., and Borlongan C.V. Differential response to ischemia in adjacent hippocampal sectors: neuronal death in CA1 versus neurogenesis in dentate gyrus. Biotechnol. J. 2 (2007) 596-607
14. Yamashima T. Implication of cysteine proteases calpain, cathepsin and caspase in ischemic neuronal death of primates. Prog. Neurobiol. 62 (2000) 273-295
15. Yamashima T., Kohda Y., Tsuchiya K., Ueno T., Yamashita J., Yoshioka T., and Kominami E. Inhibition of ischaemic hippocampal neuronal death in primates with cathepsin B inhibitor CA-074: a novel strategy for neuroprotection based on 'calpain-cathepsin hypothesis'. Eur. J. Neurosci. 10 (1998) 1723-1733
16. 2+, PIP2 and calpain responses prior to delayed neuronal death in monkeys. Eur. J. Neurosci. 8 (1996) 1932-1944
17. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
18. Nakamura A., and Goto S. Analysis of protein carbonyls with 2,4-dinitrophenyl hydrazine and its antibodies by immunoblot in two-dimensional gel electrophoresis. J. Biochem 119 (1996) 768-774
19. Nabeshi H., Oikawa S., Inoue S., Nishino K., and Kawanishi S. Proteomic analysis for protein carbonyl as an indicator of oxidative damage in senescence-accelerated mice. Free Radic. Res. 40 (2006) 1173-1181
20. Kondo T., and Hirohashi S. Application of highly sensitive fluorescent dyes (CyDye DIGE Fluor saturation dyes) to laser microdissection and two-dimensional difference gel electrophoresis (2D-DIGE) for cancer proteomics. Nat. Protoc 1 (2006) 2940-2956
21. Toda T., and Kimura N. Standardization of protocol for Immobiline 2-D PAGE and construction of 2-D PAGE protein database on world wide web home page. Jpn. J. Electrophor. 41 (1997) 13-19
22. Butterfield D.A., Perluigi M., and Sultana R. Oxidative stress in Alzheimer's disease brain: new insights from redox proteomics. Eur. J. Pharmacol. 545 (2006) 39-50
23. Tonchev A.B., Yamashima T., Zhao L., and Okano H. Differential proliferative response in the postischemic hippocampus, temporal cortex, and olfactory bulb of young adult macaque monkeys. Glia 42 (2003) 209-224
24. Yamagata A., Kristensen D.B., Takeda Y., Miyamoto Y., Okada K., Inamatsu M., and Yoshizato K. Mapping of phosphorylated proteins on two-dimensional polyacrylamide gels using protein phosphatase. Proteomics 2 (2002) 1267-1276
25. Daugaard M., Kirkegaard-Sørensen T., Ostenfeld M.S., Aaboe M., H.yer-Hansen M., Ørntoft T.F., Rohde M., and Jäättelä M. Lens epithelium-derived growth factor is an Hsp70-2 regulated guardian of lysosomal stability in human cancer. Cancer Res. 67 (2007) 2559-2567
26. Nylandsted J., Gyrd-Hansen M., Danielewicz A., Fehrenbacher N., Lademann U., Hoyer-Hansen M., Weber E., Multhoff G., Rohde M., and Jaattela M. Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J. Exp. Med. 200 (2004) 425-435
27. Rokutan K. Role of heat shock proteins in gastric mucosal protection. J. Gastroenterol. Hepatol. 15 Suppl. (2000) D12-19
28. Yenari M.A., Giffard R.G., Sapolsky R.M., and Steinberg G.K. The neuroprotective potential of heat shock protein 70 (HSP70). Mol. Med. Today 5 (1999) 525-531
29. Dalle-Donne I., Aldini G., Carini M., Colombo R., Rossi R., and Milzani A. Protein carbonylation, cellular dysfunction, and disease progression. J. Cell. Mol. Med. 10 (2006) 389-406
30. Nystrom T. Role of oxidative carbonylation in protein quality control and senescence. EMBO J. 24 (2005) 1311-1317
31. Mirzaei H., and Regnier F. Affinity chromatographic selection of carbonylated proteins followed by identification of oxidation sites using tandem mass spectrometry. Anal. Chem. 77 (2005) 2386-2392
32. Wilmarth P.A., Tanner S., Dasari S., Nagalla S.R., Riviere M.A., Bafna V., Pevzner P.A., and David L.L. Age-related changes in human crystallins determined from comparative analysis of post-translational modifications in young and aged lens: does deamidation contribute to crystallin insolubility?. J. Proteome Res. 5 (2006) 2554-2566
33. Bizzozero O.A., Reyes S., Ziegler J., and Smerjac S. Lipid peroxidation scavengers prevent the carbonylation of cytoskeletal brain proteins induced by glutathione depletion. Neurochem. Res. 32 (2007) 2114-2122
34. Aksenov M.Y., Aksenova M.V., Butterfield D.A., Geddes J.W., and Markesbery W.R. Protein oxidation in the brain in Alzheimer's disease. Neuroscience 103 (2001) 373-383
35. Chang T.C., Hsiao C.D., Wu S.J., and Wang C. The effect of mutating arginine-469 on the substrate binding and refolding activities of 70-kDa heat shock cognate protein. Arch. Biochem. Biophys. 386 (2001) 30-36
36. Rami A. Ischemic neuronal death in the rat hippocampus: the calpain-calpastatin-caspase hypothesis. Neurobiol. Dis. 13 (2003) 75-88
37. Poon H.F., Vaishnav R.A., Getchell T.V., Getchell M.L., and Butterfield D.A. Quantitative proteomics analysis of differential protein expression and oxidative modification of specific proteins in the brains of old mice. Neurobiol. Aging 27 (2006) 1010-1019
38. Lubec G., Nonaka M., Krapfenbauer K., Gratzer M., Cairns N., and Fountoulakis M. Expression of the dihydropyrimidinase related protein 2 (DRP-2) in Down syndrome and Alzheimer's disease brain is downregulated at the mRNA and dysregulated at the protein level. J. Neural Transm. Suppl. 57 (1999) 161-177
39. Johnston-Wilson N.L., Sims C.D., Hofmann J.P., Anderson L., Shore A.D., Torrey E.F., and Yolken R.H. Disease-specific alterations in frontal cortex brain proteins in schizophrenia, bipolar disorder, and major depressive disorder: the Stanley Neuropathology Consortium. Mol. Psychiatry 5 (2000) 142-149
40. Choi J., Forster M.J., McDonald S.R., Weintraub S.T., Carroll C.A., and Gracy R.W. Proteomic identification of specific oxidized proteins in ApoE-knockout mice: relevance to Alzheimer's disease. Free Radic. Biol. Med. 36 (2004) 1155-1162
41. Allison D.W., Gelfand V.I., Spector I., and Craig A.M. Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J. Neurosci. 18 (1998) 2423-2436
42. Christensen R.N., Ha B.K., Sun F., Bresnahan J.C., and Beattie M.S. Kainate induces rapid redistribution of the actin cytoskeleton in ameboid microglia. J. Neurosci. Res. 84 (2006) 170-181
43. Tsukada T., Watanabe M., and Yamashima T. Implications of CAD and DNase II in ischemic neuronal necrosis specific for the primate hippocampus. J. Neurochem. 79 (2001) 1196-1206
44. Shaham S. Glia-neuron interactions in nervous system function and development. Curr. Top. Dev. Biol. 69 (2005) 39-66
45. Levine R.L. Carbonyl modified proteins in cellular regulation, aging, and disease. Free Radic. Biol. Med. 32 (2002) 790-796