Exceptionally old mice are highly resistant to lipoxidation-derived molecular damage

Age

Volumn 35, Issue 3, 2013, Pages 621-635

  Arranz, Lorena ^a   Naudí, Alba ^b   De La Fuente, Mónica ^a   Pamplona, Reinald ^b  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSITY OF LLEIDA   (Spain)

Author keywords

Aging; Brain; Longevity; Peroxidizability index; Protein oxidation; Spleen

Indexed keywords

ALDEHYDE; AMINOADIPIC SEMIALDEHYDE; CAROBOXYETHYL LYSINE; CAROBOXYMETHY LYSINE; GLUMATIC SEMIALDEHYDE; MALONDIALDEHYDE LYSINE; POLYUNSATURATED FATTY ACID; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID;

ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DOUBLE BOND INDEX; ENZYME ACTIVITY; FATTY ACID ANALYSIS; FEMALE; GLYCOXIDATION; LIFESPAN; LIPID COMPOSITION; LIPID OXIDATION; LIPID PEROXIDATION; MASS FRAGMENTOGRAPHY; MEDICAL PARAMETERS; MEMBRANE RESISTANCE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PEROXIDIZABILITY INDEX; SENSITIVITY ANALYSIS; STEADY STATE; WESTERN BLOTTING;

AGING; ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; FATTY ACIDS; FEMALE; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; LIPID METABOLISM; LIPID PEROXIDATION; LONGEVITY; MALONDIALDEHYDE; MICE; MICE, INBRED BALB C; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEINS;

EID: 84880573458     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-012-9391-0     Document Type: Article

References (46)

1. Ahmed MU, Brinkmann Frye E, Degenhardt TP, Thorpe SR, Baynes JW (1997) N-Epsilon-(carboxyethyl)lysine, a product of the chemical modification of proteins by methylglyoxal, increases with age in human lens proteins. Biochem J 324:565-570
2. Arranz L, Caamaño JH, Lord JM, De la Fuente M (2010) Preserved immune functions and controlled leukocyte oxidative stress in naturally long-lived mice: possible role of nuclear factor kappa B. J Gerontol A Biol Sci Med Sci 65:941-950
3. Bielski BHJ, Arudi RI, Sutherland MW (1983) A study of the reactivity of HO2/O2- with unsaturated fatty acids. J Biol Chem 258:4759-4761
4. Buttemer WA, Battam H, Hulbert AJ (2008) Fowl play and the price of petrel: long-living Procellariformes have peroxidation-resistant membrane composition compared with short-living Galliformes. Biol Lett 4:351-354
5. Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11:81-128
6. Fu MX, Requena JR, Jenkins AJ, Lyons TJ, Baynes JW, Thorpe SR (1996) The advanced glycation end product, Nepsilon-(carboxymethyl)lysine, is a product of both lipid peroxidation and glycoxidation reactions. J Biol Chem 271:9982-9986
7. Gruber J, Schaffer S, Halliwell B (2008) The mitochondrial free radical theory of ageing - where do we stand? Front Biosci 13:6554-6579
8. Guillou H, Zadravec D, Martin PG, Jacobsson A (2010) The key roles of elongases and desaturases in mammalian fatty acid metabolism: insights from transgenic mice. Prog Lipid Res 49:186-199
9. Haddad LS, Kelbert L, Hulbert AJ (2007) Extended longevity of queen honey bees compared to workers is associated with peroxidation-resistant membranes. Exp Gerontol 42:601-609
10. Holman RT (1954) Autoxidation of fats and related substances. In: Holman RT, Lundberg WO, Malkin T (eds) Progress in chemistry of fats and other lipids. Pergamon, London, pp 51-98
11. Hulbert AJ, Faulks SC, Harper JM, Miller RA, Buffenstein R (2006) Extended longevity of wild-derived mice is associated with peroxidation- resistant membranes. Mech Ageing Dev 127:653-657
12. Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA (2007) Life and death: metabolic rate, membrane composition and life span of animals. Physiol Rev 87:1175-1213
13. Hulbert AJ, Beard LA, Grigg GC (2008) The exceptional longevity of an egg-laying mammal, the short-beaked echidna (Tachyglossus aculeatus) is associated with peroxidation-resistant membrane composition. Exp Gerontol 43:729-733
14. Jobson RW, Nabholz B, Galtier N (2010) An evolutionary genome scan for longevity-related natural selection in mammals. Mol Biol Evol 27:840-847
15. Knecht KJ, Dunn JA, McFarland KF, McCance DR, Lyons TJ, Thorpe SR, Baynes JW (1991) Effect of diabetes and aging on carboxymethyllysine levels in human urine. Diabetes 40:190-196
16. la Fuente D, Miquel J (2009) An update of the oxidation-inflammation theory of aging: the involvement of the immune system in oxi-inflamm-aging. Curr Pharm Des 15:3003-3026
17. Leeuwenburgh C, Wagner P, Holloszy JO, Sohal RS, Heinecke JW (1997) Caloric restriction attenuates dityrosine cross-linking of cardiac and skeletal muscle proteins in aging mice. Arch Biochem Biophys 346:74-80
18. Linton S, Davies MJ, Dean RT (2001) Protein oxidation and ageing. Exp Gerontol 36:1503-1518
19. Martínez A, Portero-Otin M, Pamplona R, Ferrer I (2010) Protein targets of oxidative damage in human neurodegenerative diseases with abnormal protein aggregates. Brain Pathol 20:281-297
20. Matsugo S, Kitagawa T, Minami S, Esashi Y, Oomura Y, Tokumaru S, Kojo S, Matsushima K, Sasaki K (2000) Age-dependent changes in lipid peroxide levels in peripheral organs, but not in brain, in senescence-accelerated mice. Neurosci Lett 278:105-108
21. Mitchell TW, Buffenstein R, Hulbert AJ (2007) Membrane phospholipid composition may contribute to exceptional longevity of the naked mole-rat (Heterocephalus glaber): a comparative study using shotgun lipidomics. Exp Gerontol 42:1053-1062
22. Naudi A, Jove M, Ayala V, Portero-Otin M, Barja G, Pamplona R (2011) Regulation of membrane unsaturation as antioxidant adaptive mechanism in long-lived animal species. Free Radic Antiox 1:3-12
23. Pamplona R (2008) Membrane phospholipids, lipoxidative damage and molecular integrity: a causal role in aging and longevity. Biochim Biophys Acta 1777:1249-1262
24. Pamplona R (2011) Advanced lipoxidation end-products. Chem Biol Interact 192:14-20
25. Pamplona R, Barja G (2007) Highly resistant macromolecular components and low rate of generation of endogenous damage: two key traits of longevity. Ageing Res Rev 6:189-210
26. Pamplona R, Barja G (2011) An evolutionary comparative scan for longevity-related oxidative stress resistance mechanisms in homeotherms. Biogerontology. doi: 10.1007/s10522-011-9348-1
27. Pamplona R, Costantini D (2011) Molecular and structural antioxidant defenses against oxidative stress in animals. Am J Physiol Regul Integr Comp Physiol 301:R843-R863
28. Pamplona R, Prat J, Cadenas S, Rojas C, Perez-Campo R, Lopez-Torres M, Barja G (1996) Low fatty acid unsaturation protects against lipid peroxidation in liver mitochondria from longevous species: the pigeon and human case. Mech Ageing Dev 86:53-66
29. Pamplona R, Barja G, Portero-Otín M (2002) Membrane fatty acid unsaturation, protection against oxidative stress, and maximum life span: a homeoviscous-longevity adaptation. Ann N Y Acad Sci 959:475-490
30. Pamplona R, Dalfo E, Ayala V, Bellmunt MJ, Prat J, Ferrer I, Portero-Otín M (2005a) Proteins in human brain cortex are modified by oxidation, glycoxidation, and lipoxidation. Effects of Alzheimer disease and identification of lipoxidation targets. J Biol Chem 280:21522-21530
31. Pamplona R, Portero-Otín M, Sanz A, Ayala V, Vasileva E, Barja G (2005b) Protein and lipid oxidative damage and complex I content are lower in the brain of parakeets and canaries than in mice. Relation to aging rate. AGE 27:267-280
32. Park JW, Choi CH, Kim MS, Chung MH (1996) Oxidative status in senescence accelerated mice. J Gerontol A Biol Sci Med Sci 51:B337-B345
33. Portero-Otin M, Pamplona R (2006) Is endogenous oxidative protein damage involved in the aging process? In: Pietzsch J (ed) Protein oxidation and disease. Research Signpost, Kerala, pp 91-142
34. Puca AA, Andrew P, Novelli V, Anselmi CV, Somalvico F, Cirillo NA, Chatgilialoglu C, Ferreri C (2008) Fatty acid profile of erythrocyte membranes as possible biomarker of longevity. Rejuvenation Res 11:63-72
35. Requena JR, Fu MX, Ahmed MU, Jenkins AJ, Lyons TJ, Baynes JW, Thorpe SR (1997) Quantification of malondialdehyde and 4-hydroxynonenal adducts to lysine residues in native and oxidized human low-density lipoprotein. Biochem J 322:317-325
36. Requena JR, Chao CC, Levine RL, Stadtman ER (2001) Glutamic and aminoadipic semialdehydes are the main carbonyl products of metal-catalyzed oxidation of proteins. Proc Natl Acad Sci USA 98:69-74
37. Ruiz MC, Ayala V, Portero-Otín M, Requena JR, Barja G, Pamplona R (2005) Protein methionine content and MDA-lysine adducts are inversely related to maximum life span in the heart of mammals. Mech Ageing Dev 126:1106-1114
38. Salmon AB, Richardson A, Pérez VI (2010) Update on the oxidative stress theory of aging: does oxidative stress play a role in aging or healthy aging? Free Radic Biol Med 48:642-655
39. Sanz A, Pamplona R, Barja G (2006) Is the mitochondrial free radical theory of aging intact? Antioxid Redox Signal 8(3-4):582-99
40. Shmookler Reis RJ, Xu L, Lee H, Chae M, Thaden JJ, Bharill P, Tazearslan C, Siegel E, Alla R, Zimniak P, Ayyadevara S (2011) Modulation of lipid biosynthesis contributes to stress resistance and longevity of C. elegans mutants. Aging (Albany NY) 3:125-147
41. Sohal RS (2002) Role of oxidative stress and protein oxidation in the aging process. Free Radic Biol Med 33:37-44
42. Spiteller G (2010) Is lipid peroxidation of polyunsaturated acids the only source of free radicals that induce aging and age-related diseases? Rejuvenation Res 13:91-103
43. Thornalley PJ (2008) Protein and nucleotide damage by glyoxal and methylglyoxal in physiological systems - role in ageing and disease. Drug Metabol Drug Interact 23:125-150
44. Thorpe SR, Baynes JW (2003) Maillard reaction products in tissue proteins: new products and new perspectives. Amino Acids 25:275-281
45. Tsuduki T, Honma T, Nakagawa K, Ikeda I, Miyazawa T (2011) Long-term intake of fish oil increases oxidative stress and decreases lifespan in senescence-accelerated mice. Nutrition 27:334-337
46. Xu L, Davis TA, Porter NA (2009) Rate constants for peroxidation of polyunsaturated fatty acids and sterols in solution and in lyoosomes. J Am Chem Soc 131:13037-13044