Identification, quantification, and functional aspects of skeletal muscle protein-carbonylation in vivo during acute oxidative stress

Journal of Proteome Research

Volumn 9, Issue 5, 2010, Pages 2516-2526

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

^a UNIVERSITY OF LEIPZIG   (Germany)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

Author keywords

Actin; Enzyme linked immunosorbent assay (ELISA); Myosin; Reactive oxygen species (ROS); Skeletal muscle proteins

Indexed keywords

MUSCLE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FUNCTIONAL PROTEOMICS; IN VIVO STUDY; LEG MUSCLE; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CARBONYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CARBOHYDRATE METABOLISM; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GAMMA RAYS; HYDRAZINES; MALE; MUSCLE PROTEINS; MUSCLE, SKELETAL; OXIDATIVE STRESS; PROTEIN CARBONYLATION; PROTEOME; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES;

RATTUS;

EID: 77952021866     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr901182r     Document Type: Article

References (45)

1. Pfeilschifter, J.; Eberhardt, W.; Huwiler, A. Nitric oxide and mechanisms of redox signalling: matrix and matrix-metabolizing enzymes as prime nitric oxide targets Eur. J. Pharmacol. 2001, 429 (1-3) 279-286
2. DAutreaux, B.; Toledano, M. B. ROS as Signalling Molecules: Mechanisms That Generate Specificity in ROS Homeostasis Nature Rev. Mol. Cell Biol. 2007, 8 (10) 813-824
3. Thannickal, V. J.; Fanburg, B. L. Reactive oxygen species in cell signaling Am. J. Physiol. Lung Cell Mol. Physiol. 2000, 279 (6) L1005-L1028
4. Moylan, J. S.; Reid, M. B. Oxidative stress, chronic disease, and muscle wasting Muscle Nerve 2007, 35 (4) 411-429
5. Chandel, N. S.; Budinger, G. R. The cellular basis for diverse responses to oxygen Free Radical Biol. Med. 2007, 42 (2) 165-174
6. Stadtman, E. R.; Levine, R. L. Protein oxidation Ann. N.Y. Acad. Sci. 2000, 899, 191-208
7. Dalle-Donne, I.; Giustarini, D.; Colombo, R.; Rossi, R.; Milzani, A. Protein carbonylation in human diseases Trends Mol. Med. 2003, 9 (4) 169-176
8. Goto, S.; Nakamura, A.; Radak, Z.; Nakamoto, H.; Takahashi, R.; Yasuda, K.; Sakurai, Y.; Ishii, N. Carbonylated proteins in aging and exercise: immunoblot approaches Mech. Ageing Dev. 1999, 107 (3) 245-253
9. Alamdari, D. H.; Kostidou, E.; Paletas, K.; Sarigianni, M.; Konstas, A. G.; Karapiperidou, A.; Koliakos, G. High sensitivity enzyme-linked immunosorbent assay (ELISA) method for measuring protein carbonyl in samples with low amounts of protein Free Radical Biol. Med. 2005, 39 (10) 1362-1367
10. Conrad, C. C.; Choi, J.; Malakowsky, C. A.; Talent, J. M.; Dai, R.; Marshall, P.; Gracy, R. W. Identification of protein carbonyls after two-dimensional electrophoresis Proteomics 2001, 1 (7) 829-834
11. Levine, R. L.; Wehr, N.; Williams, J. A.; Stadtman, E. R.; Shacter, E. Determination of carbonyl groups in oxidized proteins Methods Mol. Biol. 2000, 99, 15-24
12. Kumagai, A.; Nakayashiki, N.; Aoki, Y. Analysis of age-related carbonylation of human vitreous humor proteins as a tool for forensic diagnosis Legal Med. 2007, 9 (4) 175-180
13. Rabek, J. P.; Boylston III, W. H.; Papaconstantinou, J. Carbonylation of ER chaperone proteins in aged mouse liver Biochem. Biophys. Res. Commun. 2003, 305 (3) 566-572
14. Vasilaki, A.; Mansouri, A.; Remmen, H.; van der Meulen, J. H.; Larkin, L.; Richardson, A. G.; McArdle, A.; Faulkner, J. A.; Jackson, M. J. Free radical generation by skeletal muscle of adult and old mice: effect of contractile activity Aging Cell 2006, 5 (2) 109-117
15. Gong, M. C.; Arbogast, S.; Guo, Z.; Mathenia, J.; Su, W.; Reid, M. B. Calcium-independent phospholipase A2 modulates cytosolic oxidant activity and contractile function in murine skeletal muscle cells J. Appl. Physiol. 2006, 100 (2) 399-405
16. Zuo, L.; Christofi, F. L.; Wright, V. P.; Bao, S.; Clanton, T. L. Lipoxygenase-dependent superoxide release in skeletal muscle J. Appl. Physiol. 2004, 97 (2) 661-668
17. Criswell, D.; Powers, S.; Dodd, S.; Lawler, J.; Edwards, W.; Renshler, K.; Grinton, S. High intensity training-induced changes in skeletal muscle antioxidant enzyme activity Med. Sci. Sports Exercise 1993, 25 (10) 1135-1140
18. Powers, S. K.; Criswell, D.; Lawler, J.; Ji, L. L.; Martin, D.; Herb, R. A.; Dudley, G. Influence of exercise and fiber type on antioxidant enzyme activity in rat skeletal muscle Am. J. Physiol. 1994, 266 (2 Pt 2) R375-R380
19. Powers, S. K.; Jackson, M. J. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production Physiol. Rev. 2008, 88 (4) 1243-1276
20. Powers, S. K.; Kavazis, A. N.; McClung, J. M. Oxidative stress and disuse muscle atrophy J. Appl. Physiol. 2007, 102 (6) 2389-2397
21. Wouters, E. F. Muscle wasting in chronic obstructive pulmonary disease: to bother and to measure Am. J. Respir. Crit. Care Med. 2006, 173 (1) 4-5
22. Barreiro, E.; Nowinski, A.; Gea, J.; Sliwinski, P. Oxidative stress in the external intercostal muscles of patients with obstructive sleep apnoea Thorax 2007, 62 (12) 1095-1101
23. Hasselgren, P. O.; Menconi, M. J.; Fareed, M. U.; Yang, H.; Wei, W.; Evenson, A. Novel aspects on the regulation of muscle wasting in sepsis Int. J. Biochem. Cell Biol. 2005, 37 (10) 2156-2168
24. Feng, J.; Xie, H.; Meany, D. L.; Thompson, L. V.; Arriaga, E. A.; Griffin, T. J. Quantitative proteomic profiling of muscle type-dependent and age-dependent protein carbonylation in rat skeletal muscle mitochondria J. Gerontol., Ser. A 2008, 63 (11) 1137-1152
25. Kuleva, N. V.; Fedorova, M. A.; Frolov, A. A. Dynamics of rat hepatocyte histone glycoxidation after general x-ray irradiation Tsitologyia 2006, 48 (6) 515-521
26. Fedorova, M.; Kuleva, N.; Hoffmann, R. Reversible and irreversible modifications of skeletal muscle proteins in a rat model of acute oxidative stress Biochim. Biophys. Acta 2009, 1792, 1185-1193
27. 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. 1976, 72, 248-254
28. Domingues, M. R.; Domingues, P.; Reis, A.; Fonseca, C.; Amado, F. M.; Ferrer-Correia, A. J. Identification of oxidation products and free radicals of tryptophan by mass spectrometry J. Am. Soc. Mass Spectrom. 2003, 14 (4) 406-16
29. Levine, R. L.; Garland, D.; Oliver, C. N.; Amici, A.; Climent, I.; Lenz, A. G.; Ahn, B. W.; Shaltiel, S.; Stadtman, E. R. Determination of carbonyl content in oxidatively modified proteins Methods Enzymol. 1990, 186, 464-78
30. Shevchenko, A.; Jensen, O. N.; Podtelejnikov, A. V.; Sagliocco, F.; Wilm, M.; Vorm, O.; Mortensen, P.; Boucherie, H.; 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. 1996, 93 (25) 14440-14445
31. Avigad, G. Dansyl hydrazine as a fluorimetric reagent for thin-layer chromatographic analysis of reducing sugars J. Chromatogr. 1977, 139 (2) 343-347
32. Dalle-Donne, I.; Carini, M.; Orioli, M.; Vistoli, G.; Regazzoni, L.; Colombo, G.; Rossi, R.; Milzani, A.; Aldini, G. Protein carbonylation: 2,4-dinitrophenylhydrazine reacts with both aldehydes/ketones and sulfenic acids Free Radical Biol. Med. 2009, 46 (10) 1411-1419
33. Baldwin, K. M.; Klinkerfuss, G. H.; Terjung, R. L.; Mole, P. A.; Holloszy, J. O. Respiratory capacity of white, red, and intermediate muscle: adaptative response to exercise Am. J. Physiol. 1972, 222 (2) 373-378
34. Doran, P.; Donoghue, P.; OConnell, K.; Gannon, J.; Ohlendieck, K. Proteomics of skeletal muscle aging Proteomics 2009, 9 (4) 989-1003
35. Lombardi, A.; Silvestri, E.; Cioffi, F.; Senese, R.; Lanni, A.; Goglia, F.; de Lange, P.; Moreno, M. Defining the transcriptomic and proteomic profiles of rat ageing skeletal muscle by the use of a cDNA array, 2D- and Blue native-PAGE approach J. Proteomics 2009, 72 (4) 708-721
36. Doran, P.; OConnell, K.; Gannon, J.; Kavanagh, M.; Ohlendieck, K. Opposite pathobiochemical fate of pyruvate kinase and adenylate kinase in aged rat skeletal muscle as revealed by proteomic DIGE analysis Proteomics 2008, 8 (2) 364-77
37. Doran, P.; Donoghue, P.; OConnell, K.; Gannon, J.; Ohlendieck, K. Proteomic profiling of pathological and aged skeletal muscle fibres by peptide mass fingerprinting (review) Int. J. Mol. Med. 2007, 19 (4) 547-564
38. Anderson, E. J.; Neufer, P. D. Type II skeletal myofibers possess unique properties that potentiate mitochondrial H(2)O(2) generation Am. J. Physiol. Cell Physiol. 2006, 290 (3) C844-C851
39. Barreiro, E.; Gea, J.; Di Falco, M.; Kriazhev, L.; James, S.; Hussain, S. N. Protein carbonyl formation in the diaphragm Am. J. Respir. Cell Mol. Biol. 2005, 32 (1) 9-17
40. Coirault, C.; Guellich, A.; Barbry, T.; Samuel, J. L.; Riou, B.; Lecarpentier, Y. Oxidative stress of myosin contributes to skeletal muscle dysfunction in rats with chronic heart failure Am. J. Physiol. Heart Circ. Physiol. 2007, 292 (2) H1009-H1017
41. Yamada, T.; Mishima, T.; Sakamoto, M.; Sugiyama, M.; Matsunaga, S.; Wada, M. Myofibrillar protein oxidation and contractile dysfunction in hyperthyroid rat diaphragm J. Appl. Physiol. 2007, 102 (5) 1850-1855
42. Luo, J.; Hill, B. G.; Gu, Y.; Cai, J.; Srivastava, S.; Bhatnagar, A.; Prabhu, S. D. Mechanisms of acrolein-induced myocardial dysfunction: implications for environmental and endogenous aldehyde exposure Am. J. Physiol. Heart Circ. Physiol. 2007, 293 (6) H3673-H3684
43. Rao, V. S.; La Bonte, L. R.; Xu, Y.; Yang, Z.; French, B. A.; Guilford, W. H. Alterations to myofibrillar protein function in nonischemic regions of the heart early after myocardial infarction Am. J. Physiol. Heart Circ. Physiol. 2007, 293 (1) H654-H659
44. Kjaersgard, I. V.; Norrelykke, M. R.; Baron, C. P.; Jessen, F. Identification of carbonylated protein in frozen rainbow trout (Oncorhynchus mykiss) fillets and development of protein oxidation during frozen storage J. Agric. Food Chem. 2006, 54 (25) 9437-9446
45. Barreiro, E.; Comtois, A. S.; Mohammed, S.; Lands, L. C.; Hussain, S. N. Role of heme oxygenases in sepsis-induced diaphragmatic contractile dysfunction and oxidative stress Am. J. Physiol. Lung Cell Mol. Physiol. 2002, 283 (2) L476-L484