Effects of age and calorie restriction on tryptophan nitration, protein content, and activity of succinyl-CoA:3-ketoacid CoA transferase in rat kidney mitochondria

Free Radical Biology and Medicine

Volumn 48, Issue 4, 2010, Pages 609-618

  Brégère, Catherine ^a,b   Rebrin, Igor ^a   Gallaher, Timothy K ^a   Sohal, Rajindar S ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Aging; Caloric restriction; Free radicals; Mitochondrial enzymes; Protein nitration; Succinyl CoA transferase; Tryptophan nitration

Indexed keywords

3 NITROTYROSINE; 3 OXOACID COENZYME A TRANSFERASE; ANTIBODY; HYDROXYL GROUP; KETONE BODY; MITOCHONDRIAL PROTEIN; PROTEIN; TRYPTOPHAN; TYROSINE;

AGE; AMINO ACID ANALYSIS; ANIMAL TISSUE; ARTICLE; CALORIC RESTRICTION; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME ACTIVITY; KIDNEY PARENCHYMA; MALE; MASS SPECTROMETRY; MITOCHONDRIAL RESPIRATION; NITRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN TARGETING; RAT;

AGE FACTORS; AGING; ANIMALS; CALORIC RESTRICTION; CATALYTIC DOMAIN; COENZYME A-TRANSFERASES; KETONES; KIDNEY; MALE; MASS SPECTROMETRY; MITOCHONDRIA; NITROGEN; RATS; RATS, INBRED F344; TRYPTOPHAN;

RATTUS;

EID: 74149093964     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.12.009     Document Type: Article

References (47)

1. Koeck T., Willard B., Crabb J.W., Kinter M., Stuehr D.J., and Aulak K.S. Glucose-mediated tyrosine nitration in adipocytes: targets and consequences. Free Radic. Biol. Med. 46 (2009) 884-892
2. Parastatidis I., Thomson L., Burke A., Chernysh I., Nagaswami C., Visser J., Stamer S., Liebler D.C., Koliakos G., Heijnen H.F., Fitzgerald G.A., Weisel J.W., and Ischiropoulos H. Fibrinogen beta-chain tyrosine nitration is a prothrombotic risk factor. J. Biol. Chem. 283 (2008) 33846-33853
3. Gokulrangan G., Zaidi A., Michaelis M.L., and Schoneich C. Proteomic analysis of protein nitration in rat cerebellum: effect of biological aging. J. Neurochem. 100 (2007) 1494-1504
4. Sharov V.S., Galeva N.A., Kanski J., Williams T.D., and Schoneich C. Age-associated tyrosine nitration of rat skeletal muscle glycogen phosphorylase b: characterization by HPLC-nanoelectrospray-tandem mass spectrometry. Exp. Gerontol. 41 (2006) 407-416
5. Kanski J., Hong S.J., and Schoneich C. Proteomic analysis of protein nitration in aging skeletal muscle and identification of nitrotyrosine-containing sequences in vivo by nanoelectrospray ionization tandem mass spectrometry. J. Biol. Chem. 280 (2005) 24261-24266
6. Kanski J., Behring A., Pelling J., and Schoneich C. Proteomic identification of 3-nitrotyrosine-containing rat cardiac proteins: effects of biological aging. Am. J. Physiol. Heart Circ. Physiol. 288 (2005) H371-H381
7. Kanski J., Alterman M.A., and Schoneich C. Proteomic identification of age-dependent protein nitration in rat skeletal muscle. Free Radic. Biol. Med. 35 (2003) 1229-1239
8. Shishehbor M.H., Aviles R.J., Brennan M.L., Fu X., Goormastic M., Pearce G.L., Gokce N., Keaney Jr. J.F., Penn M.S., Sprecher D.L., Vita J.A., and Hazen S.L. Association of nitrotyrosine levels with cardiovascular disease and modulation by statin therapy. JAMA 289 (2003) 1675-1680
9. Turko I.V., Li L., Aulak K.S., Stuehr D.J., Chang J.Y., and Murad F. Protein tyrosine nitration in the mitochondria from diabetic mouse heart: implications to dysfunctional mitochondria in diabetes. J. Biol. Chem. 278 (2003) 33972-33977
10. Giasson B.I., Duda J.E., Murray I.V., Chen Q., Souza J.M., Hurtig H.I., Ischiropoulos H., Trojanowski J.Q., and Lee V.M. Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 290 (2000) 985-989
11. 2+-ATPase in skeletal muscle. Biochem. J. 340 Pt 3 (1999) 657-669
12. Gow A.J., Farkouh C.R., Munson D.A., Posencheg M.A., and Ischiropoulos H. Biological significance of nitric oxide-mediated protein modifications. Am. J. Physiol. Lung Cell Mol. Physiol. 287 (2004) L262-268
13. Souza J.M., Daikhin E., Yudkoff M., Raman C.S., and Ischiropoulos H. Factors determining the selectivity of protein tyrosine nitration. Arch. Biochem. Biophys. 371 (1999) 169-178
14. Rebrin I., Bregere C., Kamzalov S., Gallaher T.K., and Sohal R.S. Nitration of tryptophan 372 in succinyl-CoA:3-ketoacid CoA transferase during aging in rat heart mitochondria. Biochemistry 46 (2007) 10130-10144
15. Ji Y., Neverova I., Van Eyk J.E., and Bennett B.M. Nitration of tyrosine 92 mediates the activation of rat microsomal glutathione S-transferase by peroxynitrite. J. Biol. Chem. 281 (2006) 1986-1991
16. Soulere L., Claparols C., Perie J., and Hoffmann P. Peroxynitrite-induced nitration of tyrosine-34 does not inhibit Escherichia coli iron superoxide dismutase. Biochem. J. 360 (2001) 563-567
17. Yamakura F., Taka H., Fujimura T., and Murayama K. Inactivation of human manganese-superoxide dismutase by peroxynitrite is caused by exclusive nitration of tyrosine 34 to 3-nitrotyrosine. J. Biol. Chem. 273 (1998) 14085-14089
18. MacMillan-Crow L.A., Crow J.P., Kerby J.D., Beckman J.S., and Thompson J.A. Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc. Natl. Acad. Sci. USA 93 (1996) 11853-11858
19. Schoneich C., Viner R.I., Ferrington D.A., and Bigelow D.J. Age-related chemical modification of the skeletal muscle sarcoplasmic reticulum Ca-ATPase of the rat. Mech. Ageing Dev. 107 (1999) 221-231
20. Sharov V.S., Dremina E.S., Galeva N.A., Williams T.D., and Schoneich C. Quantitative mapping of oxidation-sensitive cysteine residues in SERCA in vivo and in vitro by HPLC-electrospray-tandem MS: selective protein oxidation during biological aging. Biochem. J. 394 (2006) 605-615
21. Sharov V.S., Galeva N.A., Dremina E.S., Williams T.D., and Schoneich C. Inactivation of rabbit muscle glycogen phosphorylase b by peroxynitrite revisited: does the nitration of Tyr613 in the allosteric inhibition site control enzymatic function?. Arch. Biochem. Biophys. 484 (2008) 155-166
22. Sohal R.S., and Weindruch R. Oxidative stress, caloric restriction, and aging. Science 273 (1996) 59-63
23. Dunbar B.S., and Schwoebel E.D. Preparation of polyclonal antibodies. Methods Enzymol. 182 (1990) 663-670
24. Howard J.B., Zieske L., Clarkson J., and Rathe L. Mechanism-based fragmentation of coenzyme A transferase: comparison of alpha 2-macroglobulin and coenzyme A transferase thiol ester reactions. J. Biol. Chem. 261 (1986) 60-65
25. Bregere C., Rebrin I., and Sohal R.S. Detection and characterization of in vivo nitration and oxidation of tryptophan residues in proteins. Methods Enzymol. 441 (2008) 339-349
26. Yarian C.S., Rebrin I., and Sohal R.S. Aconitase and ATP synthase are targets of malondialdehyde modification and undergo an age-related decrease in activity in mouse heart mitochondria. Biochem. Biophys. Res. Commun. 330 (2005) 151-156
27. Schagger H., and von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166 (1987) 368-379
28. Williamson D.H., Bates M.W., Page M.A., and Krebs H.A. Activities of enzymes involved in acetoacetate utilization in adult mammalian tissues. Biochem. J. 121 (1971) 41-47
29. Rebrin I., Bregere C., Gallaher T.K., and Sohal R.S. Detection and characterization of peroxynitrite-induced modifications of tyrosine, tryptophan, and methionine residues by tandem mass spectrometry. Methods Enzymol. 441 (2008) 283-294
30. Souza J.M., Choi I., Chen Q., Weisse M., Daikhin E., Yudkoff M., Obin M., Ara J., Horwitz J., and Ischiropoulos H. Proteolytic degradation of tyrosine nitrated proteins. Arch. Biochem. Biophys. 380 (2000) 360-366
31. Grune T., Blasig I.E., Sitte N., Roloff B., Haseloff R., and Davies K.J. Peroxynitrite increases the degradation of aconitase and other cellular proteins by proteasome. J. Biol. Chem. 273 (1998) 10857-10862
32. Koppen M., and Langer T. Protein degradation within mitochondria: versatile activities of AAA proteases and other peptidases. Crit. Rev. Biochem. Mol. Biol. 42 (2007) 221-242
33. Rochet J.C., Brownie E.R., Oikawa K., Hicks L.D., Fraser M.E., James M.N., Kay C.M., Bridger W.A., and Wolodko W.T. Pig heart CoA transferase exists as two oligomeric forms separated by a large kinetic barrier. Biochemistry 39 (2000) 11291-11302
34. Rochet J.C., and Bridger W.A. Identification of glutamate 344 as the catalytic residue in the active site of pig heart CoA transferase. Protein Sci. 3 (1994) 975-981
35. Lin T.W., and Bridger W.A. Sequence of a cDNA clone encoding pig heart mitochondrial CoA transferase. J. Biol. Chem. 267 (1992) 975-978
36. Turko I.V., Marcondes S., and Murad F. Diabetes-associated nitration of tyrosine and inactivation of succinyl-CoA:3-oxoacid CoA-transferase. Am. J. Physiol. Heart Circ. Physiol. 281 (2001) H2289-H2294
37. Marcondes S., Turko I.V., and Murad F. Nitration of succinyl-CoA:3-oxoacid CoA-transferase in rats after endotoxin administration. Proc. Natl. Acad. Sci. USA 98 (2001) 7146-7151
38. - or peroxynitrite and bicarbonate: role of intramolecular electron transfer mechanism. Arch. Biochem. Biophys. 484 (2008) 134-145
39. Prokai L. Misidentification of nitrated peptides: comments on Hong, S.J., Gokulrangan, G., Schoneich, C., 2007. Proteomic analysis of age-dependent nitration of rat cardiac proteins by solution isoelectric focusing coupled to nanoHPLC tandem mass spectrometry. Exp. Gerontol. 42, 639-651. Exp. Gerontol. 44 (2009) 367-369
40. Stevens Jr. S.M., Prokai-Tatrai K., and Prokai L. Factors that contribute to the misidentification of tyrosine nitration by shotgun proteomics. Mol. Cell. Proteomics 7 (2008) 2442-2451
41. Nuriel T., Deeb R.S., Hajjar D.P., and Gross S.S. Protein 3-nitrotyrosine in complex biological samples: quantification by high-pressure liquid chromatography/electrochemical detection and emergence of proteomic approaches for unbiased identification of modification sites. Methods Enzymol. 441 (2008) 1-17
42. Sung B., Jung K.J., Song H.S., Son M.J., Yu B.P., and Chung H.Y. cDNA representational difference analysis used in the identification of genes related to the aging process in rat kidney. Mech. Ageing Dev. 126 (2005) 882-891
43. Sato T., and Tauchi H. Age changes of mitochondria of rat kidney. Mech. Ageing Dev. 20 (1982) 111-126
44. Chakravarti B., Seshi B., Ratanaprayul W., Dalal N., Lin L., Raval A., and Chakravarti D.N. Proteome profiling of aging in mouse models: differential expression of proteins involved in metabolism, transport, and stress response in kidney. Proteomics 9 (2009) 580-597
45. Baylis C., and Corman B. The aging kidney: insights from experimental studies. J. Am. Soc. Nephrol. 9 (1998) 699-709
46. Johnson D.T., Harris R.A., Blair P.V., and Balaban R.S. Functional consequences of mitochondrial proteome heterogeneity. Am. J. Physiol. Cell Physiol. 292 (2007) C698-C707
47. Johnson D.T., Harris R.A., French S., Blair P.V., You J., Bemis K.G., Wang M., and Balaban R.S. Tissue heterogeneity of the mammalian mitochondrial proteome. Am. J. Physiol. Cell Physiol. 292 (2007) C689-C697