Proteomic identification of 3-nitrotyrosine-containing rat cardiac proteins: Effects of biological aging

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 288, Issue 1 57-1, 2005, Pages

  Kanski, Jaroslaw ^a   Behring, Antje ^a   Pelling, Jill ^b,c   Schöneich, Christian ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Heart; Mitochondria

Indexed keywords

3 NITROTYROSINE; ACETYL COENZYME A ACETYLTRANSFERASE; ACETYL COENZYME A ACYLTRANSFERASE; ACONITATE HYDRATASE; ALPHA ALDOLASE; ALPHA ENOLASE; ANION CHANNEL; ANTIBODY; CREATINE KINASE; ELECTRON TRANSFERRING FLAVOPROTEIN; ENOLASE; FLAVOPROTEIN; FRUCTOSE BISPHOSPHATE ALDOLASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MALATE DEHYDROGENASE; MANGANESE SUPEROXIDE DISMUTASE; METHYLMALONATE SEMIALDEHYDE DEHYDROGENASE; OXIDOREDUCTASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

AGE; AGING; ANIMAL TISSUE; ARTICLE; ELECTROSPRAY MASS SPECTROMETRY; HEART DISEASE; HEART FUNCTION; HEART MITOCHONDRION; IMMUNOPRECIPITATION; NANOELECTROSPRAY MASS SPECTROMETRY; NITRATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; RAT; TANDEM MASS SPECTROMETRY; TISSUE HOMOGENATE; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

AGING; ANIMALS; BLOTTING, WESTERN; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MYOCARDIUM; NANOTECHNOLOGY; PROTEINS; PROTEOMICS; RATS; RATS, INBRED BN; RATS, INBRED F344; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TYROSINE;

EID: 11144318614     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.01030.2003     Document Type: Article

References (71)

1. 2+-ATPaSe function, and lowers tyrosine nitration in hypercholesterolemia and improves nitric oxide-induced relaxation. Circ Res 90: 1114-1121, 2002.
2. Aulak KS, Koeck T, Crabb JW, and Stuehr DJ. Dynamics of protein nitration in cells and mitochondria. Am J Physiol Heart Circ Physiol 286: H30-H38, 2004,
3. Aulak KS, Koeck T, Crabb JW, and Stuehr DJ. Proteomic method for identification of tyrosine-nitrated proteins. Methods Mol Biol 279: 151-166, 2004,
4. Aulak KS, Miyagi M, Yan L, West KA, Massillon D, Crabb JW, and Stuehr DJ. Proteomic method identifies proteins nitrated in vivo during inflammatory challenge. Proc Natl Acad Sci USA 98: 12056-12061, 2001.
5. S. Balligand J, Kelly RA, Marsden PA, Smith TW, and Michel T. Control of cardiac muscle cell function by endogenous nitric oxide signaling system. Proc Natl Acad Sci USA 90: 347-351, 1993.
6. Beal MF. Oxidatively modified proteins in aging and disease. Free Radic Biol Med 32: 797-803, 2002.
7. Beckman JS. Oxidative damage and tyrosine nitration from peroxynitrite. Chem Res Toxicol 9: 836-844, 1996.
8. Beckman JS and Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol Cell Physiol 271: C1424-C1427, 1996.
9. Cabiscol E, Piulats E, Echave P, Herrero P, and Ros J. Oxidative stress promotes specific protein damage in Saccharomyces cerisiae. J Biol Chem 275: 27393-27398, 2000.
10. lO. Castegna A, Aksenov M, Thongbookerd V, Klein JB, Pierce WM, Booze R, Markesbery WR, and Butterfield DA. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase- related protein 2, α-enolase and heat shock cognate 71. J Neurochem 82: 1524-1532, 2002.
11. Castro L, Rodrigues M, and Radi R. Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide. J Biol Chem 269: 29409-29415, 1994.
12. Choksi KB, Boylston WH, Rabek JP, Widger WR, and Papaconstantinou J. Oxidatively damaged proteins of heart mitochondrial electron transport complexes. Biochim Biophys Acta 1688: 95-101, 2004.
13. Conconi M and Friguet B. Proteasome inactivation upon aging and on oxidation-effects of HSP 90. Mol Biol Rep 24: 45-50, 1997.
14. Corman B, Duries M, Poitevin P, Heudes D, Bruneval P, Tedgui A, and Levy BI. Aminoguanidine prevents age-related arterial stiffening cardiac hyperthorphy. Proc Natl Acad Sci USA 95: 1301-1306, 1998.
15. DePinho RA. The age of cancer. Nature 408: 248-254, 2000.
16. Ducret A, Van Ooxtveen I, Eng JK, Yates JR III, and Aebersold R. High throughput protein characterization by automated reverse-phase chromatography/electrospray tandem mass spectrometry. Protein Sci 7: 706-719, 1998,
17. Eaton P, Jones ME, McGregor E, Dunn MJ, Leeds N, Byers HL, Leun KY, Ward MA, Pratt JR, and Shattock MJ. Reversible cysteine-targeted oxidation of proteins during renal oxidative stress. J Am Soc Nephrol 8: S290-S296, 2003.
18. Ebadi M, Govitrapong P, Sharma S, Muralikrishnan D, Shavali S, Pell L, Schafer R, Albano C, and Eken J. Ubiquinone (coenzyme q10) and mitochondria in oxidative stress of Parkinson disease. Biol Signals Recept 10: 224-253, 2001.
19. Elfering SI, Haynes VL, Traaseth NJ, Ettl A, and Giulivi C. Aspects, mechanism, and biological relevance of mitochondrial protein nitration sustained by mitochondrial nitric oxide synthase. Am J Physiol Heart Circ Physiol 286: H22-H29, 2004.
20. Fernandes G, Venkatraman JT, Turturro A, Attwood VG, and Hart RW. Effect of food restriction on life span and immune functions in long-lived Fisher-344 X Brown Norway F1 rats. J Clin Immunol 17: 85-95, 1997.
21. Gole MD, Souza JM, Choi I, Hertkorn C, Malcolm S, Foust RF III, Finkel B, Lanken PN, and Ischiropoulos H. Plasma proteins modified by tyrosine nitration in acute respiratory distress syndrome. Am J Physiol Lung Cell Mol Physiol 278: L961-L967, 2000.
22. 2 production and oxidative DNA damage in the heart of food-restricted rats. Microsc Res Tech 59: 273-277, 2002.
23. Greenacre SA and Ischiropoulos H. Tyrosine nitration: localization, quantification, consequences for protein function and signal transduction. Free Radic Res 34: 541-581, 2001.
24. Grune T, Reinheckel T, and Davies KS. Degradation of oxidized proteins in mammalian cells. FASEB J 11: 526-534, 1997.
25. Harman D. Aging, a theory based on free radicals and radiation chemistry. J Gerontol A Biol Sci Med Sci 2: 298-300, 1956.
26. Hauslanden A and Fridovich I. Superoxide and peroxynitite inactivate aconitases, but nitric acid does not. J Biol Chem 269: 29405-29409, 1994.
27. Heukenshoven J and Dernick R. Simplified method for silver staining of proteins in polyacrylamide gels and the mechanisms of silver staining. Electrophoresis 6: 103-112, 1985.
28. Imran NM, Gros R, You X, Pirani A, Azad A, Csond T, Schulz T, Butany J, Duncan J, and Steward MH. Cardiomyocyte overexpression of iNOS in mice results in peroxynitrite generation, heart block and sudden death. J Clin Invest 109: 735-743, 2002.
29. Ischiropoulos H. Biological selectivity and functional aspects of protein tyrosine nitration. Biochem Biophys Res Commun 305: 776-783, 2003.
30. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, and Snyder SH. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3: 193-197, 2001.
31. Ji LL, Dillon D, and Wu E. Myocardial aging: antioxidant enzyme systems and related biochemical properties. Am J Physiol Regul Integr Comp Physiol 261: R386-R392, 1991.
32. Kanski J, Alterman M, and Schöneich C. Proteomic identification of age-dependent protein nitration in rat skeletal muscle. Free Radic Biol Med 35: 1229-1239, 2003.
33. Kato H, Miyazaki T, Yoshikawa M, Nakajima M, Fukai Y, Tajima K, Masuda N, Tsutsumi S, Tsukada K, Nakajima T, and Kuwano H. Nitrotyrosine in esophageal squamous cell carcinoma and relevance to p53 expression. Cancer Lett 153: 121-127, 2000.
34. Kmita II, Budzinska M, and Stobienia O. Modulation of the voltage dependent anion channel by cytoplasmic proteins. Acta Biochim Pol 50: 415-424, 2003.
35. Koeck T, Fu X, Hazen SL, Crabb JW, Stuehr DJ, and Aulak KS. Rapid and selective oxygen-regulated protein tyrosine denitration and nitration in mitochondria. J Biol Chem 279: 27257-27262, 2004.
36. 1-ATPase (Review). Mol Membr Biol 20: 27-33, 2003.
37. Liang-Yun Y, Levine R, and Sohal RS. Oxidative damage during aging targets mitochondrial aconitase. Proc Natl Acad Sci USA 94: 11168-11172, 1997.
38. Miyagi M, Skaguchi H, Darrow RM, Yan L, West KA, Aulak K, Stuehr DJ, Hollyfield JG, Organisciak DT, and Crabb JW. Evidence that light modulates protein nitration in rat retina. Mol Cell Proteomics 4: 293-302, 2002.
39. Molloy MP. Two-dimensional electrophoresis of membrane proteins using immobilized pH gradients. Anal Biochem 280: 1-10, 2000.
40. Murray J, Taylor SW, Zhang B, Gosh SS, and Capaldi RA. Oxidative damage to mitochondrial complex I due to peroxynitrite; identification of reactive tyrosines by mass spectrometry. J Biol Chem 278: 37223-37230, 2003.
41. Nauser T and Koppenol WH. The rate constant of the reaction of superoxide with nitrogen monoxide: approaching the diffusion limit. J Phys Chem A 106: 4084-4086, 2002.
42. Nohl H, Breuninger V, and Hegner D. Influence of radical formation on energy-linked respiration. Eur J Biochem 90: 385-390, 1978.
43. Nohl H and Hegner D. Evidence for existence of catalase in the matrix space of rat-heart mitochondria. FEBS Lett 89: 155-169, 1978.
44. Ochi H, Horiuchi I, Araki N, Toda T, Araki T, Sato K, Murai H, Osoegawa M, Yamada T, Okamura K, Ogino T, Mizumoto K, Yamashita H, Saya H, and Kira J. Proteomic analysis of human brain identifies α-enolase as a novel autoantigen in Hashimoto's encephalopathy. FEBS Lett 528: 197-202, 2002.
45. Oxenham H and Sharpe N. Cardiovascular aging and heart failure. Eur J Heart Fail 5: 427-434, 2003.
46. Pamplona R, Portero-Otin M, Bellmun MJ, Gredilla R, and Barja G. Aging increases Nε-(carboxymethyl)lysine and caloric restriction decreases Nε-(carboxyethyl)lysine and Nε-(melondialdehyde)lysine in rat heart mitochondrial proteins. Free Radic Res 26: 47-54, 2002.
47. Pamplona R, Portero-Otin M, Requena J, Gredilla R, and Barja G. Oxidative, glycoxidative, and lipoxidative damage to rat heart mitochondrial proteins is lower after 4 mo of caloric restriction than in age-matched controls. Mech Ageing Dev 123: 1437-1436, 2002.
48. Patel M and Li QY. Age dependence of seizure-induced oxidative stress. Neuroscience 118: 431-437, 2003.
49. Powell CS and Jackson RM. Mitochondrial complex I, aconitase, and succinate dehydrogenase during hypoxia-reoxygenation: modulation of enzyme activities by MnSOD. Am J Physiol Lung Cell Mol Physiol 285: L189-L198, 2003.
50. Reid MB, Khawli FA, and Moody MR. Reactive oxygen in skeletal muscle. III. Contractility of unfatigued muscle. J Appl Physiol 75: 1081-1087, 1993.
51. Roberts DL, Frank EF, and Jung-Ja PK. Three-dimensional structure of human electron transfer flavoprotein to 2.1-Å resolution. Proc Natl Acad Sci USA 93: 14355-14360, 1996.
52. Rockstein M and Sussman M. Biology of Aging. Belmond, CA: Wadsworth, 1979, p. 73-87.
53. Rosen P, Nawroth PP, King G, Moller W, Tritschler HJ, and Packer L. The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCO-MCBN, the American Diabetes Association, and the German Diabetes Society. Diabetes Metab Res Rev 17: 189-212, 2001.
54. Salazar D, Zhang L, deGala GD, and Frerman FE. Expression and characterization of two pathogenic mutations in human electron transfer flavoprotein. J Biol Chem 272: 26425-26433, 1997.
55. Sawada M and Carlson JC. Changes in superoxide radical and lipid peroxide formation in the brain, heart, and liver during the lifetime of the rat. Mech Ageing Dev 41: 125-137, 1987.
56. Shevchenko A, Wilm M, Vorm O, and Mann M. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem 68: 850-858, 1996.
57. Sohal RS. Role of oxidative stress and protein oxidation in the aging process. Free Radic Biol Med 33: 37-44, 2002.
58. Sohal RS, Arnold LA, and Sohal BH. Age-related changes in antioxidant enzymes and prooxidant generation in tissues of the rat with special reference to parameters in two insect species. Free Radic Biol Med 9: 495-500, 1990.
59. Souza JM, Choi JM, Chen Q, Weisse M, Daikhin E, Yudkoff MO, Ara J, Horwitz J, and Ischiropoulos H. Proteolytic degradation of tyrosine nitrated proteins. Arch Biochem Biophys 380: 360-366, 2000.
60. Souza JM, Daikhin E, Yudkoff M, Raman CS, and Ischiropoulos H. Factors determining the selectivity of protein tyrosine nitration. Arch Biochem Biophys 371: 169-178, 1999.
61. Stadtman ER. Protein oxidation and aging. Science 257: 1220-1224, 1992.
62. Szweda LI and Lucas DT. Cardiac reperfusion injury: aging, lipid peroxidation, and mitochondrial dysfunction. Proc Natl Acad Sci USA 95: 510-514, 1998.
63. Tamarit J, Cabiscol E, and Ros J. Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J Biol Chem 273: 3027-3032, 1998.
64. Turko IV, Li L, Aulak KS, Stuehr DJ, Chang JY, and Murad F. Protein tyrosine nitration in the mitochondria from diabetic mouse heart. Implications to dysfunctional mitochondria in diabetes. J Biol Chem 278: 33972-33977, 2003.
65. Turko IV and Murad F. Quantitative protein profiling in heart mitochondria from diabetic rats. J Biol Chem 278: 35844-35849, 2003.
66. Vadseth C, Souza JM, Thompon L, Seagraves A, Nagaswami C, Scheiner T, Torbet J, Vilaire G, Bennett JS, Murciano JC, Muzynkantov V, Penn MS, Hazen SL, Weisel JW, and Ischiropoulos H. Pro-thrombotic state induced by post-translational modification of fibrinogen by reactive nitrogen species. J Biol Chem 279: 8820-8826, 2004.
67. Viner RI, Ferrington DA, Williams TD, Bigelow DJ, and Schöneich C. Protein modification during biological aging: selective tyrosine nitration of the SERCA2 isoform of the sarcoplasmic reticulum Ca-ATPase in skeletal muscle. Biochem J 340: 657-669, 1999.
68. Wang X, Osinska H, Gerdes AM, and Bobbins J. Desmin filaments and cardiac disease: establishing causality. J Card Fail 8: S287-S292, 2002.
69. Xu KY, Huso DL, Dawson TM, Bredt LC, and Becker LC. Nitric oxide synthase in cardiac sarcoplasmic reticulum. Proc Natl Acad Sci USA 96: 657-662, 1999.
70. Yates JR III, Eng JK, McCormack AL, and Schleitz D. Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 67:1426-1436, 1995.
71. Ye YZ, Strong M, Huang ZQ, and Beckman JS. Antibodies that recognize nitrotyrosine. Methods Enzymol 269:201-209, 1996.