Changes in rat liver mitochondria with aging: Lon protease-like activity and Nε-carboxymethyllysine accumulation in the-matrix

European Journal of Biochemistry

Volumn 270, Issue 10, 2003, Pages 2295-2302

  Bakala, Hilaire ^a   Delaval, Evelyne ^a   Hamelin, Maud ^a   Bismuth, Jeanne ^a   Borot Laloi, Caroline ^a   Corman, Bruno ^b   Friguet, Bertrand ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b Service de Biologie Cellulaire   (France)

Author keywords

Aging; Carboxymethyllysine; Lon protease; Matrix; Mitochondria

Indexed keywords

ADENOSINE TRIPHOSPHATE; ENDOPEPTIDASE LA; LYSINE DERIVATIVE; N EPSILON CARBOXYMETHYLYSINE; PROTEINASE; UNCLASSIFIED DRUG;

AGING; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; IMMUNOCHEMISTRY; LIVER MITOCHONDRION; MALE; NONHUMAN; OXIDATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; RESPIRATORY CHAIN; STRESS;

ADENOSINE TRIPHOSPHATE; AGING; ANIMALS; BLOTTING, WESTERN; CELL SURVIVAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOPEPTIDASES; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOCHEMISTRY; LYSINE; MALE; METHYLATION; MICROSCOPY, ELECTRON; MITOCHONDRIA; MITOCHONDRIA, LIVER; OXYGEN; OXYGEN CONSUMPTION; PEPTIDES; RATS; RATS, WISTAR; STRESS; TIME FACTORS;

ANIMALIA;

EID: 0037517056     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03598.x     Document Type: Article

References (45)

1. Youngman, L.D., Park, J.Y. & Ames, B.N. (1992) Protein oxidation associated with aging is reduced by dietary restriction of protein or calories. Proc. Natl Acad. Sci. USA 89, 9112-9116.
2. Giardino, I., Edelstein, D. & Brownlee, M. (1994) Nonenzymatic glycosylation in vitro and in bovine endothelial cells alters basic fibroblast growth factor activity. A model for intracellular glycosylation in diabetes. J. Clin. Invest. 94, 110-117.
3. Vlassara, H., Bucala, R. & Striker, L. (1994) Pathogenic effects of advanced glycosylation: biochemical, biologic, and clinical implications for diabetes and aging. Laboratory Invest. 70, 138-151.
4. King, G.L., Shiba, T., Oliver, J., Inoguchi, T. & Bursell, S.E. (1994) Cellular and molecular abnormalities in the vascular endothelium of diabetes mellitus. Annu. Rev. Med. 45, 179-188.
5. Verbeke, P., Perichon, M., Borot-Laloi, C., Schaeverbeke, J. & Bakala, H. (1997) Accumulation of advanced glycation endproducts in the rat nephron: link with circulating AGEs during aging. J. Histochem. Cytochem. 45, 1059-1068.
6. Requena, J.R., Fu, M.X., Ahmed, M.U., Jenkins, A.J., Lyons, T.J., Baynes, J.W. & Thorpe, S.R. (1997) Quantification of malondialdehyde and 4-hydroxynonenal adducts to lysine residues in native and oxidized human low-density lipoprotein. Biochem. J. 322, 317-325.
7. Miyata, T., Inagi, R., Asahi, K., Yamada, Y., Horie, K., Sakai, H., Uchida, K. & Kurokawa, K. (1998) Generation of protein carbonyls by glycoxidation and lipoxidation reactions with autoxidation products of ascorbic acid and polyunsaturated fatty acids. FEBS Lett. 437, 24-28.
8. Motomiya, Y., Oyama, N., Iwamoto, H., Uchimura, T. & Maruyama, I. (1998) N-epsilon-(carboxymethyl) lysine in blood from maintenance hemodialysis patients may contribute to dialysis-related amyloidosis. Kidney Int. 54, 1357-1366.
9. Traverso, N., Menini, S., Cottalasso, D., Odetti, P., Marinari, U.M. & Pronzato, M.A. (1997) Mutual interaction between glycation and oxidation during non-enzymatic protein modification. Biochim. Biophys. Acta 1336, 409-418.
10. Kristal, B.S. & B.P. (1992) An emerging hypothesis: synergistic induction of aging by free radicals and Maillard reactions. J. Gerontol. 47, B107-B114.
11. Pamplona, R., Requena, J.R., Portero-Otin, M., Prat, J., Thorpe, S.R. & Bellmunt, M.J. (1998) Carboxymethylated phosphatidylethanolamine in mitochondrial membranes of mammalsEvidence for intracellular lipid glycoxidation. Eur. J. Biochem. 255, 685-689.
12. Chance, B., Sies, H. & Boveris, A. (1979) Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59, 527-605.
13. Kalous, M. & Drahota, Z. (1996) The role of mitochondria in aging. Physiol. Res. 45, 351-359.
14. Turrens, Z. (1997) Superoxide production by the mitochondrial respiratory chain. Bioscience Report 17, 3-7.
15. Shigenaga, M.K., Hagen, T.M. & Ames, B.N. (1994) Oxidative damage and mitochondrial decay in aging. Proc. Natl Acad. Sci. USA 91, 10771-10778.
16. Sastre, J., Pallardo, F.V., Garcia de la Ascunsion, J. & Vina, J. (1999) Mitochondria, oxidative stress and aging. Free Rad. Res. 32, 189-198.
17. Yan, L.J., Levine, R.L. & Sohal, R.S. (1997) Oxidative damage during aging targets mitochondrial aconitase. Proc. Natl Acad. Sci. USA 94, 11168-11172.
18. Yan, L.J. & Sohal, R.S. (1998) Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proc. Natl Acad. Sci. USA 95, 12896-12901.
19. Martinez, M., Hernandez, A.I., Martinez, N. & Ferrandiz, M.L. (1996) Age-related increase in oxidized proteins in mouse synaptic mitochondria. Brain Res. 731, 246-248.
20. 1 complex in skeletal muscle mitochondria. Biochim. Biophys. Acta 1315, 66-72.
21. Wong, L.K. & Sohal, R.S. (2000) Age-related changes in activities of mitochondrial electron transport complexes in various tissues of the mouse. Arch. Biochem. Biophys. 373, 16-22.
22. Lee, C.K., Klopp, R.G., Weindruch, R. & Prolla, T.A. (1999) Gene expression profile of aging and its retardation by caloric restriction. Science 285, 1390-1393.
23. Wang, N., Gottesman, S., Willingaham, M.C., Gottesman, M. & Maurizi, M.R. (1993) A human mitochondrial ATP-dependent protease that is highly homologous to bacterial Lon protease. Proc. Natl Acad. Sci. USA 90, 11247-11251.
24. Desautels, M. & Goldberg, A.L. (1982) Demonstration of an ATP-dependent, vanadate-sensitive endoprotease in the matrix of rat liver mitochondria. J. Biol. Chem. 257, 11673-11679.
25. Watabe, S. & Kimura, T. (1985) Adrenal cortex mitochondrial enzyme with ATP-dependent protease and protein-dependent ATPase activities. J. Biol. Chem. 260, 14498-14504.
26. Ishii, S., Watabe, S. & Hamada, H. (1992) ATP-dependent protease in human placenta. Placenta 13, 343-347.
27. Marcillat, O., Zhang, O., Lin, S.W. & Davies, K.J.A. (1988) Mitochondria contain a proteolytic system which can recognize and degrade oxidatively-denaturated proteins. Biochem. J. 254, 677-683.
28. Bota, D.A. & Davies, K.J. (2002) Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nature Cell Biol. 4, 674-680.
29. Gray, J.E., Van Zwieten, M.J. & Hollander, C.F. (1982) Early light microscopic changes of chronic progressive nephrosis in several strains of aging laboratory rats. J. Gerontol. 37, 142-150.
30. Murata, T., Nagai, R., Ishibashi, T., Inomuta, H., Ikeda, K. & Horiuchi, S. (1997) The relationship between accumulation of advanced glycation end products and expression of vascular endothelial growth factor in human diabetic retinas. Diabetologia 40, 764-769.
31. Aprille, J.R. & Asimakis, G.K. (1980) Postnatal development of rat liver mitochondria; state 3 respiration, adenine nucleotide translocase activity and the net accumulation of adenine nucleotide. Arch. Biochem. Biophys. 201, 564-575.
32. Ventura, B., Genova, M.L., Bovina, C., Formiggini, G. & Lenaz, G. (2002) Contol of oxidative phosphorylation by Complex I in rat liver mitochondria: implications for aging. Biochim. Biophys. Acta 1553, 249-260.
33. Sohal, R.S. & Dubay, A. (1994) Mitochondrial oxidative damage, hydrogen peroxide release, and aging. Free Radic. Biol. Med. 16, 621-626.
34. Nagai, M., Takahashi, R. & Goto, S. (2000) Dietary restriction initiated late in life can reduce mitochondrial protein carbonyls in rat livers: Western blot studies. Biogerontology 1, 321-328.
35. Fu, M.X., Requena, J.R., Jenkins, A.J., Lyons, T.J., Baynes, J.W. & Thorpe, S.R. (1996) The advanced glycation end product, N-(carboxymethyl) lysine, is a product of both lipid peroxidation and glycoxidation reactions. J. Biol. Chem. 271, 9982-9986.
36. Miyata, T., Fu, M.X., Kurokawa, K., Van Ypersele de Strihou, C., Thorpe, S.R. & Baynes, J.W. (1998) Autoxidation products of both carbohydrates and lipids are increased in uremic plasma: is there oxidative stress in uremia? Kidney Int. 54, 1290-1295.
37. Thornalley, P.J. (1990) The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem. J. 269, 1-11.
38. Shinohara, M., Thornalley, P.J., Giardino, I., Beisswenger, P., Thorpe, S.R., Onorato, J. & Brownlee, M. (1998) 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. 101, 1142-1147.
39. Nishikawa, T., Du Edelstein, D.X.L., Yamagishi, S., Matsumura, T., Kaneda, Y., Yorek, M.A., Beebe, D., Oates, P.J., Hammes, H.P., Giardino, I. & Brownlee, M. (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404, 787-789.
40. Colbeau, A., Nachbaur, J. & Vignais, P.M. (1971) Enzymic characterization and lipid composition of rat liver subcellular membranes. Biochim. Biophys. Acta 249, 462-492.
41. Daum, G. (1985) Lipids of mitochondria. Biochim. Biophys. Acta 822, 1-42.
42. Paradies, G., Petrosillo, G., Pistolese, M. & Ruggiero, F.M. (2000) The effect of reactive oxygen species generated from the mitochondrial electron transport chain on the cytochrome c oxidase activity and on the cardiolipin content in bovine heart sub-mitochondrial particles. FEBS Lett. 466, 323-326.
43. Ikeda, K., Higashi, T., Sano, H., Jinnouchi, Y., Yoshida, M., Araki, T., Ueda, S. & Hurochi, S. (1996) N (epsilon) -(carboxymethyl) lysine protein adduct is a major immunological epitope in proteins modified with advanced glycation end products of the Maillard reaction. Biochemistry 35, 8075-8083.
44. Das, N., Levine, R.L., Orr, W.C. & Sohal, R.S. (2001) Selectivity of protein oxidative damage during aging in Drosophila melanogaster. Biochem. J. 15, 209-216.
45. Fannin, S.W., Lesnefsky, E.J., Slabe, T.J., Hassan, M.O. & Hoppel, C.L. (1999) Aging selectively decreases oxidative capacity in rat heart interfibrillar mitochondria. Arch. Biochem. Biophys. 372, 399-407.