Differential expression and glycative damage affect specific mitochondrial proteins with aging in rat liver

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 12, 2013, Pages 2057-2067

  Bakala, Hilaire ^a,b   Ladouce, Romain ^b   Baraibar, Martin A ^b   Friguet, Bertrand ^b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

2D DIGE; Aging; Glycation; Mitochondria; Protein expression; Proteomics

Indexed keywords

(S) 2 HYDROXY ACID OXIDASE; 2 METHYLACYL COENZYME A RACEMASE; ACYL COENZYME A DEHYDROGENASE; ADVANCED GLYCATION END PRODUCT; BETAINE HOMOCYSTEINE METHYLTRANSFERASE; CATALASE; COENZYME A; ENOYL COENZYME A HYDRATASE; FERREDOXIN NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE REDUCTASE; GLYCINE HYDROXYMETHYLTRANSFERASE; GLYCOSYLATED PROTEIN; MATRIX PROTEIN; MEDIUM CHAIN ACYL COENZYME A DEHYDROGENASE; MITOCHONDRIAL ENZYME; MITOCHONDRIAL PROTEIN; ORNITHINE OXOACID AMINOTRANSFERASE; PROTEOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRUVATE CARBOXYLASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SULFITE OXIDASE; SUPEROXIDE DISMUTASE;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; DOWN REGULATION; ENERGY YIELD; ENZYME ACTIVITY; ENZYME MECHANISM; FATTY ACID OXIDATION; FEMALE; GEL ELECTROPHORESIS; GLUCONEOGENESIS; GLYCATION; IMMUNODETECTION; LIVER MITOCHONDRION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; RAT; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UREA CYCLE; WESTERN BLOTTING;

EID: 84882753352     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.07.015     Document Type: Article

References (61)

1. Suh J.H., Heath S.H., Hagen T.M. Two subpopulations of mitochondria in the aging rat heart display heterogenous levels of oxidative stress. Free Radic. Biol. Med. 2003, 35(9):1064-1072.
2. Hayflick L. How and why we age. Exp. Gerontol. 1998, 33:639-653.
3. Berlett B.S., Stadtman E.R. Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 1997, 272(33):20313-20316.
4. Dencher N.A., Frenzel M., Reifschneider N.H., Sugawa M., Krause F. Proteome alterations in rat mitochondria caused by aging. Ann. N. Y. Acad. Sci. 2007, 1100:291-298.
5. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001, 292:727-730.
6. Duchen M.R. Mitochondria and calcium: from cell signalling to cell death. J. Physiol. 2000, 529:57-68.
7. Kroemer G., Galluzzi L., Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 2007, 87:99-163.
8. Hagen T.M., Yowe D.L., Bartholomew J.C., Wehr C.M., Do K.L., Park J.Y., Ames B.N. Mitochondrial decay in hepatocytes from old rats: membrane potential declines, heterogeneity and oxidants increase. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:3064-3069.
9. Shigenaga M.K., Hagen T.M., Ames B.N. Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:10771-10778.
10. Sastre J., Pallardo F.V., Pla R., Pellin A., Juan G., O'Connor J.E., Estrela J.M., Miquel J., Vina J. Aging of the liver: age-associated mitochondrial damage in intact hepatocytes. Hepatology 1996, 24:1199-11205.
11. Yan L.J., Levine R.L., Sohal R.S. Oxidative damage during aging targets mitochondrial aconitase. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:11168-11172.
12. St-Pierre J., Buckingham J.A., Roebuck S.J., Brand M.D. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 2002, 277:44784-44790.
13. Smith R.A., Kelso G.F., Blaikie F.H., Porteous C.M., Ledgerwood E.C., Hughes G., James A.M., Ross M.F., Asin-Cayuela J., Cocheme H.M., et al. Using mitochondria-targeted molecules to study mitochondrial radical production and its consequences. Biochem. Soc. Trans. 2003, 31:1295-1299.
14. Martinez M., Hernandez A.I., Martinez N., Ferrandiz M.L. Age-related increase in oxidized proteins in mouse synaptic mitochondria. Brain Res. 1996, 731:246-248.
15. Kwong L.K., Sohal R.S. Age-related changes in activities of mitochondrial electron transport complexes in various tissues of the mouse. Arch. Biochem. Biophys. 2000, 373:16-22.
16. Lenaz G., Bovina C., D'Aurelio M., Fato R., Formiggini G., Genova M.L., Giuliano G., Merlo Pich M., Paolucci U., Parenti Castelli G., Ventura B. Role of mitochondria in oxidative stress and aging. Ann. N. Y. Acad. Sci. 2002, 959:199-213.
17. Ames B.N., Shigenaga M.K. Oxidants are a major contributor to aging. Ann. N. Y. Acad. Sci. 1992, 663:85-96.
18. Stadtman E.R. Protein oxidation and aging. Science 1992, 257:1220-1224.
19. Bakala H., Delaval E., Hamelin M., Bismuth J., Borot-Laloi C., Corman B., Friguet B. Changes in rat liver mitochondria with aging. Lon protease-like activity and N(epsilon)-carboxymethyllysine accumulation in the matrix. Eur. J. Biochem. 2003, 270:2295-2302.
20. Hamelin M., Mary J., Vostry M., Friguet B., Bakala H. Glycation damage targets glutamate dehydrogenase in the rat liver mitochondrial matrix during aging. FEBS J. 2007, 274:5949-5961.
21. Kil I.S., Lee J.H., Shin A.H., Park J.W. Glycation-induced inactivation of NADP(+)-dependent isocitrate dehydrogenase: implications for diabetes and aging. Free Radic. Biol. Med. 2004, 37(2004):1765-1778.
22. Nishikawa T., Edelstein D., Du X.L., Yamagishi S., Matsumura T., Kaneda Y., Yorek M.A., Beebe D., Oates P.J., Hammes H.P., Giardino I., Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000, 404(6779):787-790.
23. Shinohara M., Thornalley P.J., Giardino I., Beisswenger P., Thorpe S.R., Onorato J., Brownlee M. Overexpression of glyoxalase-I in bovine endothelial cells inhibits intracellular advanced glycation endproduct formation and prevents hyperglycemia-induced increases in macromolecular endocytosis. J. Clin. Invest. 1998, 101(5):1142-1147.
24. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414(6865):813-820.
25. Ahmed E.K., Rogowska-Wrzesinska A., Roepstorff P., Bulteau A.L., Friguet B. Protein modification and replicative senescence of WI-38 human embryonic fibroblasts. Aging Cell 2010, 9(2):252-272.
26. Short K.R., Bigelow M.L., Kahl J., Singh R., Coenen-Schimke J., Raghavakaimal S., Nair K.S. Decline in skeletal muscle mitochondrial function with aging in humans. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:5618-5623.
27. Mao P., Gallagher P., Nedungadi S., Manczak M., Shirendeb U.P., Kohama S.G., Ferguson B., Park B.S., Reddy P.H. Mitochondrial DNA deletions and differential mitochondrial DNA content in Rhesus monkeys: implications for aging. Biochim. Biophys. Acta 2012, 1822:111-119.
28. Lopez M.E., Van Zeeland N.L., Dahl D.B., Weindruch R., Aiken J.M. Cellular phenotypes of age-associated skeletal muscle mitochondrial abnormalities in rhesus monkeys. Mutat. Res. 2000, 452:123-138.
29. Peng T.I., Yu P.R., Chen J.Y., Wang H.L., Wu H.Y., Wei Y.H., Jou M.J. Visualizing common deletion of mitochondrial DNA-augmented mitochondrial reactive oxygen species generation and apoptosis upon oxidative stress. Biochim. Biophys. Acta 2006, 1762:241-255.
30. Rooyackers O.E., Adey D.B., Ades P.A., Nair K.S. Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:15364-15369.
31. Hudson E.K., Tsuchiya N., Hansford R.G. Age-associated changes in mitochondrial mRNA expression and translation in the Wistar rat heart. Mech. Ageing Dev. 1998, 103:179-193.
32. Barazzoni R., Short K.R., Nair K.S. Effects of aging on mitochondrial DNA copy number and cytochrome c oxidase gene expression in rat skeletal muscle, liver, and heart. J. Biol. Chem. 2000, 275:3343-3347.
33. Delaval E., Perichon M., Friguet B. Age-related impairment of mitochondrial matrix aconitase and ATP-stimulated protease in rat liver and heart. Eur. J. Biochem. 2004, 271:4559-4564.
34. Bakala H., Hamelin M., Mary J., Borot-Laloi C., Friguet B. Catalase, a target of glycation damage in rat liver mitochondria with aging. Biochim. Biophys. Acta 2012, 1822:1527-1534.
35. Shevchenko A., Loboda A., Ens W., Schraven B., Standing K.G., Shevchenko A. Archived polyacrylamide gels as a resource for proteome characterization by mass spectrometry. Electrophoresis 2001, 22:1194-1203.
36. Tank A.W., Weiner H., Thurman J.A. Enzymology and subcellular localization of aldehyde oxidation in rat liver. Oxidation of 3,4-dihydroxyphenylacetaldehyde derived from dopamine to 3,4-dihydroxyphenylacetic acid. Biochem. Pharmacol. 1981, 30:3265-3275.
37. Zeng J., Li D. Expression and purification of His-tagged rat mitochondrial medium-chain acyl-CoA dehydrogenase wild-type and Arg256 mutant proteins. Protein Expr. Purif. 2004, 37:472-478.
38. Liu X., Wu L., Deng G., Li N., Chu X., Guo F., Li D. Characterization of mitochondrial trifunctional protein and its inactivation study for medicine development. Biochim. Biophys. Acta 2008, 1784:1742-1749.
39. Baraibar M.A., Hyzewicz J., Rogowska-Wrzesinska A., Ladouce R., Roepstorff P., Mouly V., Friguet B. Oxidative stress-induced proteome alterations target different cellular pathways in human myoblasts. Free Radic. Biol. Med. 2011, 51(8):1522-1532.
40. Ventura B., Genova M.L., Bovina C., Formiggini G., Lenaz G. Control of oxidative phosphorylation by Complex I in rat liver mitochondria: implications for aging. Biochim. Biophys. Acta 2002, 1553:249-260.
41. Petersen K.F., Befroy D., Dufour S., Dziura J., Ariyan C., Rothman D.L., Di Pietro L., Cline G.W., Shulman G.I. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 2003, 300:1140-1142.
42. Korshunov S.S., Skulachev V.P., Starkov A.A. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 1997, 416:15-18.
43. Nicholls D.G. Mitochondrial function and dysfunction in the cell: its relevance to aging and aging-related disease. Int. J. Biochem. Cell Biol. 2002, 34:1372-1381.
44. Takasawa S., Hayakawa M., Ozawa T. Changes in skeletal muscle, heart and liver mitochondrial electron transport activities in rats and dogs of various ages. Biochem. Mol. Biol. Int. 1993, 5:937-944.
45. Kumaran S., Panneerselvam K.S., Shila S., Sivarajan K., Panneerselvam C. Age-associated deficit of mitochondrial oxidative phosphorylation in skeletal muscle: role of carnitine and lipoic acid. Mol. Cell. Biochem. 2005, 280(1-2):83-89.
46. Genova M.L., Pich M.M., Bernacchia A., Bianchi C., Biondi A., Bovina C., Falasca A.I., Formiggini G., Castelli G.P., Lenaz G. The mitochondrial production of reactive oxygen species in relation to aging and pathology. Ann. N. Y. Acad. Sci. 2004, 1011:86-100.
47. García-Cazorla A., Rabier D., Touati G., Chadefaux-Vekemans B., Marsac C., de Lonlay P., Saudubray J.M. Pyruvate carboxylase deficiency: metabolic characteristics and new neurological aspects. Ann. Neurol. 2006, 59:121-127.
48. Ferré P. The biology of peroxisome proliferator-activated receptors: relationship with lipid metabolism and insulin sensitivity. Diabetes 2004, (Suppl. 1):S43-S50.
49. Heikkinen S., Auwerx J., Argmann C.A. PPARgamma in human and mouse physiology. Biochim. Biophys. Acta 2007, 1771:999-1013.
50. Wagner M., Zollner G., Trauner M. Nuclear receptors in liver disease. Hepatology 2011, 53:1023-1034.
51. Gan Q., Huang J., Zhou R., Niu J., Zhu X., Wang J., Zhang Z., Tong T. PPAR{gamma}accelerates cellular senescence by inducing p16INK4{alpha} expression in human diploid fibroblasts. J. Cell Sci. 2008, 121:2235-2245.
52. Farrés J., Wang T.T., Cunningham S.J., Weiner H. Investigation of the active site cysteine residue of rat liver mitochondrial aldehyde dehydrogenase by site-directed mutagenesis. Biochemistry 1995, 34:2592-2598.
53. Zeng J., Li D. Expression and purification of His-tagged rat mitochondrial 3-ketoacyl-CoA thiolase wild-type and His352 mutant proteins. Protein Expr. Purif. 2004, 35:320-326.
54. Yao D., Taguchi T., Matsumura T., Pestell R., Edelstein D., Giardino I., Suske G., Ahmed N., Thornalley P.J., Sarthy V.P., Hammes H.P., Brownlee M. Methylglyoxal modification of mSin3A links glycolysis to angiopoietin-2 transcription. Cell 2006, 124:275-286.
55. Ahmed N. Advanced glycation endproducts-role in pathology of diabetic complications. Diabetes Res. Clin. Pract. 2005, 67:3-21.
56. Yan H., Harding J.J. Glycation-induced inactivation and loss of antigenicity of catalase and superoxide dismutase. Biochem. J. 1997, 328:599-605.
57. Lucas D.T., Szweda L.I. Declines in mitochondrial respiration during cardiac reperfusion: age-dependent inactivation of α-ketoglutarate dehydrogenase. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:6689-6693.
58. Simoneau J.A., Kelley D.E. Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J. Appl. Physiol. 1997, 83:166-171.
59. Amati F., Dube J.J., Coen P.M., Stefanovic-Racic M., Toledo F.G., Goodpaster B.H. Physical inactivity and obesity underlie the insulin resistance of aging. Diabetes Care 2009, 32:1547-1549.
60. Rajpathak S.N., Gunter M.J., Wylie-Rosett J., Ho G.Y., Kaplan R.C., Muzumdar R., Rohan T.E., Strickler H.D. The role of insulin-like growth factor-I and its binding proteins in glucose homeostasis and type 2 diabetes. Diabetes Metab. Res. Rev. 2009, 25:3-12.
61. Kondo T., Kitano T., Iwai K., Watanabe M., Taguchi Y., Yabu T., Umehara H., Domae N., Uchiyama T., Okazaki T. Control of ceramide-induced apoptosis by IGF-1: involvement of PI-3 kinase, caspase-3 and catalase. Cell Death Differ. 2002, 9:682-692.