Reversible and irreversible modifications of skeletal muscle proteins in a rat model of acute oxidative stress

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1792, Issue 12, 2009, Pages 1185-1193

  Fedorova, Maria ^a   Kuleva, Nadezhda ^b   Hoffmann, Ralf ^a  

^a Faculty of Chemistry and Mineralogy   (Germany)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

Author keywords

Carbonylation; Cysteine residue; Diagonal redox SDS PAGE; Mass spectrometry (MS); Protein oxidation; Reactive oxygen species (ROS)

Indexed keywords

ACTIN; CREATINE KINASE; MUSCLE PROTEIN; MYOSIN LIGHT CHAIN; REACTIVE OXYGEN METABOLITE;

ACTIN POLYMERIZATION; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN DEPLETION; PROTEIN MODIFICATION; RAT; SKELETAL MUSCLE; WESTERN BLOTTING; X IRRADIATION;

ACUTE DISEASE; ANIMALS; DISEASE MODELS, ANIMAL; DISULFIDES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; LIPID PEROXIDATION; MALE; MUSCLE PROTEINS; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; WHOLE-BODY IRRADIATION; X-RAYS;

RATTUS;

EID: 71849118358     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2009.09.011     Document Type: Article

References (72)

1. Thannickal V.J., and Fanburg B.L. Reactive oxygen species in cell signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 279 (2000) L1005-L1028
2. Moldovan L., and Moldovan N.I. Oxygen free radicals and redox biology of organelles. Histochem. Cell Biol. 122 (2004) 395-412
3. 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
4. Pfeilschifter J., Eberhardt W., and Huwiler A. Nitric oxide and mechanisms of redox signalling: matrix and matrix-metabolizing enzymes as prime nitric oxide targets. Eur. J. Pharmacol. 429 (2001) 279-286
5. Droge W. Free radicals in the physiological control of cell function. Physiol. Rev. 82 (2002) 47-95
6. Maulik N. Redox signaling of angiogenesis. Antioxid. Redox Signal. 4 (2002) 805-815
7. Forman H.J., Fukuto J.M., and Torres M. Redox signaling: thiol chemistry defines which reactive oxygen and nitrogen species can act as second messengers. Am. J. Physiol. Cell Physiol. 287 (2004) C246-C256
8. Cadenas E. Biochemistry of oxygen toxicity. Annu. Rev. Biochem. 58 (1989) 79-110
9. Dalle-Donne I., Scaloni A., Giustarini D., Cavarra E., Tell G., Lungarella G., Colombo R., Rossi R., and Milzani A. Proteins as biomarkers of oxidative/nitrosative stress in diseases: the contribution of redox proteomics. Mass. Spectrom. Rev. 24 (2005) 55-99
10. Chandel N.S., and Budinger G.R. The cellular basis for diverse responses to oxygen. Free Radic. Biol. Med. 42 (2007) 165-174
11. Stadtman E.R., and Levine R.L. Protein oxidation. Ann. N. Y. Acad. Sci. 899 (2000) 191-208
12. Uchida K. Histidine and lysine as targets of oxidative modification. Amino Acids 25 (2003) 249-257
13. Chang T.C., Chou W.Y., and Chang G.G. Protein oxidation and turnover. J. Biomed. Sci. 7 (2000) 357-363
14. Louie J.L., Kapphahn R.J., and Ferrington D.A. Proteasome function and protein oxidation in the aged retina. Exp. Eye Res. 75 (2002) 271-284
15. Squier T.C. Oxidative stress and protein aggregation during biological aging. Exp. Gerontol. Mol. Aging 36 (2001) 1539-1550
16. Butterfield D.A. Oxidative stress in neurodegenerative disorders. Antioxid. Redox Signal. 8 (2006) 1971-1973
17. Beckman K.B., and Ames B.N. The free radical theory of aging matures. Physiol. Rev. 78 (1998) 547-581
18. Sayre L.M., Perry G., and Smith M.A. Oxidative stress and neurotoxicity. Chem. Res. Toxicol. 21 (2008) 172-188
19. Hsiai T., and Berliner J.A. Oxidative stress as a regulator of murine atherosclerosis. Curr. Drug Targets 8 (2007) 1222-1229
20. Hamblin M., Friedman D.B., Hill S., Caprioli R.M., Smith H.M., and Hill M.F. Alterations in the diabetic myocardial proteome coupled with increased myocardial oxidative stress underlies diabetic cardiomyopathy. J. Mol. Cell. Cardiol. 42 (2007) 884-895
21. Firdaus W.J., Wyttenbach A., Diaz-Latoud C., Currie R.W., and Arrigo A.P. Analysis of oxidative events induced by expanded polyglutamine huntingtin exon 1 that are differentially restored by expression of heat shock proteins or treatment with an antioxidant. Febs. J. 273 (2006) 3076-3093
22. Norris E.H., and Giasson B.I. Role of oxidative damage in protein aggregation associated with Parkinson's disease and related disorders. Antioxid. Redox Signal. 7 (2005) 672-684
23. Menon S.G., and Goswami P.C. A redox cycle within the cell cycle: ring in the old with the new. Oncogene 26 (2007) 1101-1109
24. Barford D. The role of cysteine residues as redox-sensitive regulatory switches. Curr. Opin. Struct. Biol. 14 (2004) 679-686
25. Cooper C.E., Patel R.P., Brookes P.S., and Darley-Usmar V.M. Nanotransducers in cellular redox signaling: modification of thiols by reactive oxygen and nitrogen species. Trends Biochem. Sci. 27 (2002) 489-492
26. Ying J., Clavreul N., Sethuraman M., Adachi T., and Cohen R.A. Thiol oxidation in signaling and response to stress: detection and quantification of physiological and pathophysiological thiol modifications. Free Radic. Biol. Med. 43 (2007) 1099-1108
27. Leichert L.I., and Jakob U. Global methods to monitor the thiol-disulfide state of proteins in vivo. Antioxid. Redox Signal. 8 (2006) 763-772
28. Eaton P. Protein thiol oxidation in health and disease: techniques for measuring disulfides and related modifications in complex protein mixtures. Free Radic. Biol. Med. 40 (2006) 1889-1899
29. Biteau B., Labarre J., and Toledano M.B. ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425 (2003) 980-984
30. Shelton M.D., Chock P.B., and Mieyal J.J. Glutaredoxin: role in reversible protein s-glutathionylation and regulation of redox signal transduction and protein translocation. Antioxid. Redox Signal. 7 (2005) 348-366
31. Gallogly M.M., and Mieyal J.J. Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress. Curr. Opin. Pharmacol. 7 (2007) 381-391
32. Chrestensen C.A., Starke D.W., and Mieyal J.J. Acute cadmium exposure inactivates thioltransferase (Glutaredoxin), inhibits intracellular reduction of protein-glutathionyl-mixed disulfides, and initiates apoptosis. J. Biol. Chem. 275 (2000) 26556-26565
33. Dalle-Donne I., Rossi R., Colombo G., Giustarini D., and Milzani A. Protein S-glutathionylation: a regulatory device from bacteria to humans. Trends Biochem. Sci. 34 (2009) 85-96
34. Brosnan J.T., and Brosnan M.E. The sulfur-containing amino acids: an overview. J. Nutr. 136 (2006) 1636S-1640S
35. Otten E. Concepts and models of functional architecture in skeletal muscle. Exerc. Sport Sci. Rev. 16 (1988) 89-137
36. Schiaffino S., and Reggiani C. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol. Rev. 76 (1996) 371-423
37. Shishkin S.S., Kovalyov L.I., and Kovalyova M.A. Proteomic studies of human and other vertebrate muscle proteins. Biochemistry. (Mosc.) 69 (2004) 1283-1298
38. Geeves M.A., and Holmes K.C. Structural mechanism of muscle contraction. Annu. Rev. Biochem. 68 (1999) 687-728
39. Moylan J.S., and Reid M.B. Oxidative stress, chronic disease, and muscle wasting. Muscle Nerve. 35 (2007) 411-429
40. Sellers J.R., Goodson H.V., and Wang F. A myosin family reunion. J. Muscle Res. Cell Motil. 17 (1996) 7-22
41. Kuleva N.V., Fedorova M.A., and Frolov A.A. Dynamics of rat hepatocyte histone glycoxidation after general x-ray irradiation. Tsitologyia 48 (2006) 515-521
42. Janero D.R. Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic. Biol. Med. 9 (1990) 515-540
43. Levine R.L., Garland D., Oliver C.N., Amici A., Climent I., Lenz A.G., Ahn B.W., Shaltiel S., and Stadtman E.R. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 186 (1990) 464-478
44. Davies K. Protein damage and degradation by oxygen radicals, I, general aspects. J. Biol. Chem. 262 (1987) 9895-9901
45. Sommer A., and Traut R.R. Diagonal polyacrylamide-dodecyl sulfate gel electrophoresis for the identification of ribosomal proteins crosslinked with methyl-4-mercaptobutyrimidate. Proc. Natl. Acad. Sci. U. S. A. 71 (1974) 3946-3950
46. Brennan J.P., Wait R., Begum S., Bell J.R., Dunn M.J., and Eaton P. Detection and mapping of widespread intermolecular protein disulfide formation during cardiac oxidative stress using proteomics with diagonal electrophoresis. J. Biol. Chem. 279 (2004) 41352-41360
47. Shevchenko A., Jensen O.N., Podtelejnikov A.V., Sagliocco F., Wilm M., Vorm O., Mortensen P., Boucherie H., and Mann M. Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 14440-14445
48. Matsumoto K.-i., Okajo A., Kobayashi T., Mitchell J.B., Krishna M.C., and Endo K. Estimation of free radical formation by [beta]-ray irradiation in rat liver. J. Biochem. Biophys. Methods 63 (2005) 79-90
49. Riley P.A. Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int. J. Radiat. Biol. 65 (1994) 27-33
50. da Silva L.d.B., Leipnitz G., Seminotti B., Fernandes C.G., Beskow A.P., Amaral A.U., and Wajner M. D-Serine induces lipid and protein oxidative damage and decreases glutathione levels in brain cortex of rats. Brain Res. 1256 (2009) 34-42
51. Esterbauer H., and Cheeseman K.H. Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal, methods in enzymology. In: Glazer L.P.a.A.N. (Ed). Oxygen Radicals in Biological Systems Part B: Oxygen Radicals and Antioxidants (1990), Academic Press 407-421
52. Nourooz-Zadeh J., Cooper M.B., Ziegler D., and Betteridge D.J. Urinary 8-epi-PGF2[alpha] and its endogenous [beta]-oxidation products (2,3-dinor and 2,3-dinor-5,6-dihydro) as biomarkers of total body oxidative stress. Biochem. Biophys. Res. Commun. 330 (2005) 731-736
53. Dalle-Donne I., Rossi R., Milzani A., Di Simplicio P., and Colombo R. The actin cytoskeleton response to oxidants: from small heat shock protein phosphorylation to changes in the redox state of actin itself. Free Radic. Biol. Med. 31 (2001) 1624-1632
54. England K., and Cotter T. Identification of carbonylated proteins by MALDI-TOF mass spectroscopy reveals susceptibility of ER. Biochem. Biophys. Res. Commun. 320 (2004) 123-130
55. Dalle-Donne I., Giustarini D., Colombo R., Rossi R., and Milzani A. Protein carbonylation in human diseases. Trends Mol. Med. 9 (2003) 169-176
56. O'Neill C.A., Stebbins C.L., Bonigut S., Halliwell B., and Longhurst J.C. Production of hydroxyl radicals in contracting skeletal muscle of cats. J. Appl. Physiol. 81 (1996) 1197-1206
57. Kobzik L., Reid M.B., Bredt D.S., and Stamler J.S. Nitric Oxide Skelet. muscle 372 (1994) 546-548
58. Kolbeck R.C., She Z.W., and Callahan L.A. Increased superoxide production during fatigue in the perfused rat diaphragm. Am. J. Respir. Crit. Care Med. 156 (1997) 140-145
59. Tidball J.G., and Wehling-Henricks M. The role of free radicals in the pathophysiology of muscular dystrophy. J. Appl. Physiol. 102 (2007) 1677-1686
60. Canton M., Skyschally A., Menabo R., Boengler K., Gres P., Schulz R., Haude M., Erbel R., Di Lisa F., and Heusch G. Oxidative modification of tropomyosin and myocardial dysfunction following coronary microembolization. Eur. Heart J. 27 (2006) 875-881
61. Kudriashov Iu B., and Goncharenko E.N. Current problems of chemical radiation protection of organisms. Radiat. Biol. Radioecol. 39 (1999) 197-211
62. Grune T., Reinheckel T., and Davies K.J. Degradation of oxidized proteins in mammalian cells. Faseb. J. 11 (1997) 526-534
63. Putkey J.A., Dotson D.G., and Mouawad P. Formation of inter- and intramolecular disulfide bonds can activate cardiac troponin C. J. Biol. Chem. 268 (1993) 6827-6830
64. Lowe D.A., Warren G.L., Snow L.M., Thompson L.V., and Thomas D.D. Muscle activity and aging affect myosin structural distribution and force generation in rat fibers. J. Appl. Physiol. 96 (2004) 498-506
65. Feng J., Xie H., Meany D.L., Thompson L.V., Arriaga E.A., and Griffin T.J. Quantitative proteomic profiling of muscle type-dependent and age-dependent protein carbonylation in rat skeletal muscle mitochondria. J. Gerontol. A Biol. Sci. Med. Sci. 63 (2008) 1137-1152
66. 2 generation. Am. J. Physiol. Cell Physiol. 290 (2006) C844-C851
67. Thompson L.V. Skeletal muscle adaptations with age, inactivity, and therapeutic exercise. J. Orthop. Sports Phys. Ther. 32 (2002) 44-57
68. Shartava A., Monteiro C.A., Bencsath F.A., Schneider K., Chait B.T., Gussio R., Casoria-Scott L.A., Shah A.K., Heuerman C.A., and Goodman S.R. A posttranslational modification of beta-actin contributes to the slow dissociation of the spectrin-protein 4.1-actin complex of irreversibly sickled cells. J. Cell. Biol. 128 (1995) 805-818
69. Farah M.E., and Amberg D.C. Conserved actin cysteine residues are oxidative stress sensors that can regulate cell death in yeast. Mol. Biol. Cell. 18 (2007) 1359-1365
70. Prochniewicz E., Spakowicz D., and Thomas D.D. Changes in actin structural transitions associated with oxidative inhibition of muscle contraction. Biochemistry 47 (2008) 11811-11817
71. Koffer A., and Sleep J. Activation of myosin ATPase by actin isolated from cultured BHK cells and the effect of gelsolin. J. Muscle Res. Cell. Motil. 8 (1987) 541-547
72. Kuleva N.V., and Kovalenko Z.S. Change in the functional properties of actin by its glycation in vitro. Biochemistry. (Mosc.) 62 (1997) 1119-1123