Protein targets for carbonylation by 4-hydroxy-2-nonenal in rat liver mitochondria

Journal of Proteomics

Volumn 74, Issue 11, 2011, Pages 2370-2379

  Guo, Jia ^a   Prokai Tatrai, Katalin ^a   Nguyen, Vien ^a   Rauniyar, Navin ^a,c   Ughy, Bettina ^a,b   Prokai, Laszlo ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

4 Hydroxy 2 nonenal; ATP synthase; Liver; Mitochondria; Protein carbonylation; Redox proteomics

Indexed keywords

4 HYDROXYNONENAL; ACETYL COENZYME A ACYLTRANSFERASE; ACYL COENZYME A DEHYDROGENASE; CARBAMOYL PHOSPHATE SYNTHASE; CATALASE; GLUTAMATE DEHYDROGENASE; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN 70; HYDRAZINE; HYDROXYACYLGLUTATHIONE HYDROLASE; METHYLMALONATE SEMIALDEHYDE DEHYDROGENASE (ACYLATING); MITOCHONDRIAL PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRUVATE CARBOXYLASE; SULFITE OXIDASE; THIOSULFATE SULFURTRANSFERASE; TRANSKETOLASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEATH; DRUG METABOLISM; IMMUNOBLOTTING; LIQUID CHROMATOGRAPHY; LIVER MITOCHONDRION; MALE; MASS SPECTROMETRY; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CARBONYLATION; PROTEIN INTERACTION; PROTEIN MODIFICATION; PROTEIN TARGETING; RAT;

ALDEHYDES; AMINO ACID SEQUENCE; ANIMALS; DRUG DELIVERY SYSTEMS; LIVER; MALE; METABOLIC NETWORKS AND PATHWAYS; MITOCHONDRIA, LIVER; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; PEPTIDE FRAGMENTS; PROTEIN CARBONYLATION; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES;

RATTUS;

EID: 80054874658     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.07.009     Document Type: Article

References (57)

1. Shacter E. Quantification and significance of protein oxidation in biological sample. Drug Metabol Rev 2000, 32:307-326.
2. Porter N.A., Caldwell S.E., Mills K.A. Mechanisms of free radical oxidation of unsaturated lipids. Lipids 1995, 30:277-290.
3. Catala A. Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions. Chem Phys Lipids 2009, 157:1-11.
4. Pamplona R. Membrane phospholipids, lipoxidative damage and molecular integrity: a causal role in aging and longevity. Biochim Biophys Acta 2008, 1777:1249-1262.
5. Grimsrud P.A., Xie H., Griffin T.J., Bernlohr D.A. Oxidative stress and covalent modification of protein with bioactive aldehydes. J Biol Chem 2008, 283:21837-21841.
6. Carini M., Aldini G., Facino R.M. Mass spectrometry for detection of 4-hydroxy-trans-2-nonenal (HNE) adducts with peptides and proteins. Mass Spectrom Rev 2004, 23:281-305.
7. Navarro A., Boveris A. Rat brain and liver mitochondria develop oxidative stress and lose enzymatic activities on aging. Am J Physiol Regul Integr Comp Physiol 2004, 287:R1244-R1249.
8. Marques C., Pereira P., Taylor A., Liang J.N., Reddy V.N., Szweda L.I., et al. Ubiquitin-dependent lysosomal degradation of the HNE-modified proteins in lens epithelial cells. FASEB J 2004, 18:1424-1426.
9. Cecarini V., Gee J., Fioretti E., Amici M., Angeletti M., Eleuteri A., et al. Protein oxidation and cellular homeostasis: emphasis on metabolism. Biochim Biophys Acta 2007, 1773:93-104.
10. Negre-Salvayre A., Coatrieux C., Ingueneau C., Salvayre R. Advanced lipid peroxidation end products in oxidative damage to proteins. Potential role in diseases and therapeutic prospects for the inhibitors. Br J Pharmacol 2008, 153:6-20.
11. Maier C.S., Chavez J., Wang J., Wu J. Protein adducts of aldehydic lipid peroxidation products: identification and characterization of protein adducts using an aldehyde/keto-reactive probe in combination with mass spectrometry. Methods in Enzymology, vol 473: thiol redox transitions in cell signaling, Part A: chemistry and biochemistry of low molecular weight and protein thiols 2010, 305-330. Academic Press/Elsevier Inc, San Diego. E. Cadenas, L. Packer (Eds.).
12. Xu G.Z., Liu Y., Sayre L.M. Independent synthesis, solution behavior, and studies on the mechanism of formation of a primary amine-derived fluorophore representing cross-linking of proteins by (E)-4-hydroxy-2-nonenal. J Org Chem 1999, 64:5732-5745.
13. Poli G., Biasia F., Leonarduzzi G. 4-Hydroxynonenal-protein adducts: a reliable biomarker of lipid oxidation in liver diseases. Mol Aspects Med 2008, 29:67-71.
14. Schneider C., Porter N.A., Brash A.R. Routes to 4-hydroxynonenal: fundamental issues in the mechanisms of lipid peroxidation. J Biol Chem 2008, 283:15539-15543.
15. Petersen D.R., Doorn J.A. Reactions of 4-hydroxynonenal with proteins and cellular targets. Free Radic Biol Med 2004, 37:937-945.
16. Newton B.W., Russell W.K., Russell D.H., Ramaiah S.K., Jayaraman A. Liver proteome analysis in a rodent model of alcoholic steatosis. J Proteome Res 2009, 8:1663-1671.
17. Carbone D.L., Doorn J.A., Kiebler Z., Ickes B.R., Petersen D.R. Modification of heat shock protein 90 by 4-hydroxynonenal in a rat model of chronic alcoholic liver disease. J Pharmacol Exp Ther 2005, 315:8-15.
18. Dalle-Donne I., Aldini G., Carini M., Colombo R., Rossi R., Milzani A. Protein carbonylation, cellular dysfunction, and disease progression. J Cell Mol Med 2006, 10:389-406.
19. Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991, 11:81-128.
20. Bruenner B.A., Jones A.D., German J.B. Direct characterization of protein adducts of the lipid peroxidation product 4-hydroxy-2-nonenal using electrospray mass spectrometry. Chem Res Toxicol 1995, 8:552-559.
21. 3 acquisition: method evaluation through an in vitro study on cytochrome c oxidase modifications. Proteomics 2009, 9:5188-5193.
22. Rauniyar N., Stevens S.M., Prokai L. Fourier transform ion cyclotron resonance mass spectrometry of covalent adducts of protein and 4-hydroxy-2-nonenal, a reactive end-product of lipid peroxidation. Anal Bioanal Chem 2007, 389:1421-1428.
23. 3 acquisition. J Mass Spectrom 2007, 42:1599-1605.
24. Prokai L., Yan L.J., Vera-Serrano J.L., Stevens S.M., Forster M.J. Mass spectrometry-based survey of age-associated protein carbonylation in rat brain mitochondria. J Mass Spectrom 2007, 42:1583-1589.
25. Uto H., Kanmura S., Takami Y., Tsubouchi H. Clinical proteomics for liver disease: a promising approach for discovery of novel biomarkers. Proteome Sci 2010, 8:70.
26. Young T.A., Cunningham C.C., Bailey S.M. Reactive oxygen species production by the mitochondrial respiratory chain in isolated rat hepatocytes and liver mitochondria: studies using myxothiazol. Arch Biochem Biophys 2002, 405:65-72.
27. Venkatraman A., Landar A., Davis A.J., Ulasova E., Page G., Murphy M.P., et al. Oxidative modification of hepatic mitochondria protein thiols: effect of chronic alcohol consumption. Am J Physiol Gastrointest Liver Physiol 2004, 286:G521-G527.
28. Sharma R., Nakamura A., Takahashi R., Nakamoto H., Goto S. Carbonyl modification in rat liver histones: decrease with age and increase by dietary restriction. Free Radic Biol Med 2006, 40:1179-1184.
29. Arnaiz S., Llesuy S., Cutrin J., Boveris A. Oxidative stress by acute acetaminophen administration in mouse liver. Free Radic Biol Med 1995, 19:303-310.
30. Niemela O. Distribution of ethanol-induced protein adducts in vivo: relationship to tissue injury. Free Radic Biol Med 2001, 31:1533-1538.
31. Traverso N., Menini S., Odetti P., Pronzato M.A., Cottalasso D., Marinari U.M. Lipoperoxidation in hepatic subcellular compartments of diabetic rats. Free Radic Biol Med 1999, 26:538-547.
32. Chen J.J., Schenker S., Henderson G.I. 4-hydroxynonenal levels are enhanced in fetal liver mitochondria by in utero ethanol exposure. Hepatology 1997, 25:142-147.
33. Mendez D., Hernaez M.L., Diez A., Puyet A., Bautista J.M. Combined proteomic approaches for the identification of specific amino acid residues modified by 4-hydroxy-2-nonenal under physiological conditions. J Proteome Res 2010, 9:5770-5781.
34. Brunet S., Thibault P., Gagnon E., Kearney P., Bergeron J.J.M., Desjardins M. Organelle proteomics: looking at less to see more. Trends Cell Biol 2003, 13:629-638.
35. 3 versus neutral loss-driven electron capture dissociation. Anal Chem 2009, 81:782-789.
36. Rauniyar N., Prokai-Tatrai K., Prokai L. Identification of carbonylation sites in apomyoglobin after exposure to 4-hydroxy-2-nonenal by solid-phase enrichment and liquid chromatography-electrospray ionization tandem mass spectrometry. J Mass Spectrom 2009, 45:398-410.
37. Uchida K., Stadtman E.R. Modification of histidine residues in proteins by reaction with 4-hydroxynonenal. Proc Natl Acad Sci USA 1992, 89:4544-4548.
38. Uchida K., Stadtman E.R. Selective cleavage of thioether linkage in proteins modified with 4-hydroxynonenal. Proc Natl Acad Sci USA 1992, 89:5611-5615.
39. Uchida K. 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res 2003, 42:318-343.
40. Roe M.R., McGowan T.F., Thomas F., Thompson L.V., Griffin T.J. Targeted O-18-labeling for improved proteomic analysis of carbonylated peptides by mass spectrometry. J Am Soc Mass Spectrom 2010, 21:1190-1203.
41. Doorn J.A., Petersen D.R. Covalent adduction of nucleophilic amino acids by 4-hydroxynonenal and 4-oxononenal. Chem Biol Interact 2003, 143-144:93-100.
42. Roe M.R., Xie H., Bandhakavi S., Griffin T.J. Proteomic mapping of 4-hydroxynonenal protein modification sites by solid-phase hydrazide chemistry and mass spectrometry. Anal Chem 2007, 79:3747-3756.
43. Lopachin R.M., Geohagen B.C., Gavin T. Synaptosomal toxicity and nucleophilic targets of 4-hydroxy-2-nonenal. Toxicol Sci 2009, 107:171-181.
44. Ohta S., Kagawa Y. Human F1-ATPase: molecular cloning of cDNA for the beta subunit. J Biochem 1968, 99:135-141.
45. Del Rio P., Montiel T., Chagoya V., Massieu L. Exacerbation of excitotoxic neuronal death induced during mitochondrial inhibition in vivo: relation to energy imbalance or ATP depletion?. Neuroscience 2007, 146:1561-1570.
46. Mastorodemos V., Kotzamani D., Zaganas I., Arianoglou G., Latsoudis H., Plaitakis A. Human GLUD1 and GLUD2 glutamate dehydrogenase localize to mitochondria and endoplasmic reticulum. Biochem Cell Biol 2009, 87:505-516.
47. Fang J., Hsu B.Y.L., Macmullen C.M., Poncz M., Smith T.J., Stanley C.A. Expression, purification and characterization of human glutamate dehydrogenase (GDH) allosteric regulatory mutations. Biochem J 2002, 363:81-87.
48. Crouser E.D., Julian M.W., Huff J.E., Struck J., Cook C.H. Carbamoyl phosphate synthase-1: a marker of mitochondrial damage and depletion in the liver during sepsis. Crit Care Med 2006, 34:2439-2446.
49. Radi R., Turrens J.F., Chang L.Y., Bush K.M., Crapo J.D., Freeman B.A. Detection of catalase in rat heart mitochondria. J Biol Chem 1991, 266:22028-22034.
50. Jiang X.S., Dai J., Sheng Q.H., Zhang L., Xia Q.C., Wu J.R., et al. A comparative proteomic strategy for subcellular proteome research: ICAT approach coupled with bioinformatics prediction to ascertain rat liver mitochondrial proteins and indication of mitochondrial localization for catalase. Mol Cell Proteomics 2005, 4:12-34.
51. Semsei I., Rao G., Richardson A. Changes in the expression of superoxide dismutase and catalase as a function of age and dietary restriction. Biochem Biophys Res Commun 1989, 164:620-625.
52. D'Souza A., Kurien B., Rodgers R., Shenoi J., Kurono S., Matsumoto H., et al. Detection of catalase as a major protein target of the lipid peroxidation product 4-HNE and the lack of its genetic association as a risk factor in SLE. BMC Med Genet 2008, 9:62.
53. Schuler A.M., Wood P.A. Mouse models for disorders of mitochondrial fatty acid beta-oxidation. ILAR J 2002, 43:57-65.
54. Mi J., Garcia-Arcos I., Alvarez R., Cristobal S. Age-related subproteomic analysis of mouse liver and kidney peroxisomes. Proteome Sci 2007, 5:19-34.
55. Marquez A., Villa-Treviño S., Guéraud F. The LEC rat: a useful model for studying liver carcinogenesis related to oxidative stress and inflammation. Redox Rep 2007, 12:35-39.
56. Reed T., Perluigi M., Sultana R., Pierce W.M., Klein J.B., Turner D.M., et al. Redox proteomic identification of 4-hydroxy-2-nonenal-modified brain proteins in amnestic mild cognitive impairment: insight into the role of lipid peroxidation in the progression and pathogenesis of Alzheimer's disease. Neurobiol Dis 2008, 30:107-120.
57. Mailman R.B. Toxicant-receptor interactions: fundamental principles. Molecular and biochemical toxicology 2008, 359-390. John Wiley & Sons, Inc, Chichester. 4th Edition. R.C. Smart, E. Hodgson (Eds.).