Membrane lipid unsaturation as physiological adaptation to animal longevity

Frontiers in Physiology

Volumn 4 DEC, Issue , 2013, Pages

  Naudí, Alba ^a   Jové, Mariona ^a   Ayala, Victòria ^a   Portero Otín, Manuel ^a   Barja, Gustavo ^b   Pamplona, Reinald ^a  

^a UNIVERSITY OF LLEIDA   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Fatty acid biosynthesis; Membrane unsaturation; Oxidative damage; Peroxidizability index; Phylogenomic analysis; Rate of aging; Reactive carbonyl species

Indexed keywords

MEMBRANE LIPID; OXYGEN;

AGING; CELL MEMBRANE; CHEMICAL MODIFICATION; CYTOTOXICITY; ENERGY YIELD; EVOLUTION; GENETIC MANIPULATION; LIPID METABOLISM; LIPID PEROXIDATION; LIPID UNSATURATION; LONGEVITY; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; REVIEW; SIGNAL TRANSDUCTION; SPECIES COMPARISON;

EID: 84891687810     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00372     Document Type: Review

References (123)

1. Abele, D., Brey, T., and Philipp, E. (2009). Bivalve models of aging and the determination of molluscan lifespans. Exp. Gerontol. 44, 307-315. doi: 10.1016/j.exger.2009.02.012.
2. Arranz, L., Naudí, A., De la Fuente, M., and Pamplona, R. (2013). Exceptionally old mice are highly resistant to lipoxidation-derived molecular damage. Age (Dordr) 35, 621-635. doi: 10.1007/s11357-012-9391-0.
3. Austad, S. N. (2009). Is there a role for new invertebrate models for aging research? J. Gerontol. A Biol. Sci. Med. Sci. 64, 192-194. doi: 10.1093/gerona/gln059.
4. Ayala, V., Ilieva, E. V., Fernandez, E., Modol, M. T., Bellmunt, M. J., Prat, J., et al. (2006). Lesión oxidativa de proteínas de hígado y corazón de rata durante el proceso de envejecimiento. Rev. Esp. Geriatr. Gerontol. 41, 43-49. doi: 10.1016/S0211-139X(06)72922-5.
5. Ayala, V., Naudí, A., Sanz, A., Caro, P., Portero-Otin, M., Barja, G., et al. (2007). Dietary protein restriction decreases oxidative protein damage, peroxidizability index, and mitochondrial complex I content in rat liver. J. Gerontol. A Biol. Sci. Med. Sci. 62, 352-360. doi: 10.1093/gerona/62.4.352.
6. Ayyadevara, S., Dandapat, A., Singh, S. P., Siegel, E. R., Shmookler Reis, R. J., Zimniak, L., et al. (2007). Life span and stress resistance of Caenorhabditis elegans are differentially affected by glutathione transferases metabolizing 4-hydroxynon-2-enal. Mech. Ageing Dev. 128, 196-205. doi: 10.1016/j.mad.2006.11.025.
7. Ayyadevara, S., Engle, M. R., Singh, S. P., Dandapat, A., Lichti, C. F., Benes, H., et al. (2005). Lifespan and stress resistance of Caenorhabditis elegans are increased by expression of glutathione transferases capable of metabolizing the lipid peroxidation product 4-hydroxynonenal. Aging Cell 4, 257-271. doi: 10.1111/j.1474-9726.2005.00168.x.
8. Bielski, B. H., Arudi, R. L., and Sutherland, M. W. (1983). A study of the reactivity of HO2/O2-with unsaturated fatty acids. J. Biol. Chem. 258, 4759-4761.
9. Brand, M. D., Affourtit, C., Esteves, T. C., Green, K., Lambert, A. J., Miwa, S., et al. (2004). Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic. Biol. Med. 37, 755-767. doi: 10.1016/j.freeradbiomed.2004.05.034.
10. Brenner, R. R. (1984). Effect of unsaturated fatty acids on membrane structure and enzyme kinetics. Progr. Lipid Res. 23, 69-96. doi: 10.1016/0163-7827(84)90008-0.
11. Brigelius-Flohé, R. (2006). Glutathione peroxidases and redox-regulated transcription factors. Biol. Chem. 387, 1329-1335. doi: 10.1515/BC.2006.166.
12. Buffenstein, R. (2005). The naked mole-rat: a new long-living model for human aging research. J. Gerontol. A Biol. Sci. Med. Sci. 60, 1369-1377. doi: 10.1093/gerona/60.11.1369.
13. Buttemer, W. A., Battam, H., and Hulbert, A. J. (2008). Fowl play and the price of petrel: long-living Procellariiformes have peroxidation-resistant membrane composition compared with short-living Galliformes. Biol. Lett. 4, 351-354. doi: 10.1098/rsbl.2008.0145.
14. Caro, P., Gómez, J., López-Torres, M., Sánchez, I., Naudí, A., Jove, M., et al. (2008). Forty percent and eighty percent methionine restriction decrease mitochondrial ROS generation and oxidative stress in rat liver. Biogerontology 9, 183-196. doi: 10.1007/s10522-008-9130-1.
15. Caro, P., Gomez, J., Sanchez, I., Naudi, A., Ayala, V., López-Torres, M., et al. (2009). Forty percent methionine restriction decreases mitochondrial oxygen radical production and leak at complex I during forward electron flow and lowers oxidative damage to proteins and mitochondrial DNA in rat kidney and brain mitochondria. Rejuvenation Res. 12, 421-434. doi: 10.1089/rej.2009.0902.
16. Catalá, A. (2009). Lipid peroxidation of membrane phospholipids generates hydroxyl-alkenals and oxidized phospholipids active in physiological and/or pathological conditions. Chem. Phys. Lipids 157, 1-11. doi: 10.1016/j.chemphyslip.2008.09.004.
17. Conrad, M., Schneider, M., Seiler, A., and Bornkamm, G. W. (2007). Physiological role of phospholipid hydroperoxide glutathione peroxidase in mammals. Biol. Chem. 388, 1019-1025. doi: 10.1515/BC.2007.130.
18. Copple, I. M., Goldring, C. E., Kitteringham, N. R., and Park, B. K. (2008). The Nrf2-Keap1 defence pathway: role in protection against drug-induced toxicity. Toxicology 246, 24-33. doi: 10.1016/j.tox.2007.10.029.
19. Cutler, R. G. (1985). Peroxide-producing potential of tissues: inverse correlation with longevity of mammalian species. Proc. Natl. Acad. Sci. U.S.A. 82, 4798-4802. doi: 10.1073/pnas.82.14.4798.
20. De, A. K., Chipalkatti, S., and Aiyar, A. S. (1983). Some biochemical parameters of ageing in relation to dietary protein. Mech. Ageing Dev. 21, 37-48. doi: 10.1016/0047-6374(83)90014-3.
21. Dobrosotskaya, I. Y., Seegmiller, A. C., Brown, M. S., Goldstein, J. L., and Rawson, R. B. (2002). Regulation of SREBP processing and membrane lipid production by phospholipids in Drosophila. Science 296, 879-883. doi: 10.1126/science.1071124.
22. Dowhan, W. (1997). Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu. Rev. Biochem. 66, 199-232. doi: 10.1146/annurev.biochem.66.1.199.
23. Dowling, D. K., and Simmons, L. W. (2009). Reactive oxygen species as universal constraints in life-history evolution. Proc. Royal Soc. B Biol. Sci. 276, 1737-1745. doi: 10.1098/rspb.2008.1791.
24. Echtay, K. S., Esteves, T. C., Pakay, J. L., Jekabsons, M. B., Lambert, A. J., Portero-Otín, M., et al. (2003). A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J. 22, 4103-4110. doi: 10.1093/emboj/cdg412.
25. Embley, T. M., and Martin, W. (2006). Eukaryotic evolution, changes and challenges. Nature 440, 623-630. doi: 10.1038/nature04546.
26. Enesco, H. E., and Kruk, P. (1981). Dietary restriction reduces fluorescent age pigment accumulation in mice. Exp. Gerontol. 16, 357-361. doi: 10.1016/0531-5565(81)90056-5.
27. Esterbauer, H., Schaur, R. J., and Zollner, H. (1991). Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11, 81-128. doi: 10.1016/0891-5849(91)90192-6.
28. Fabelo, N., Martín, V., Marín, R., Santpere, G., Aso, E., Ferrer, I., et al. (2012). Evidence for premature lipid raft aging in APP/PS1 double-transgenic mice, a model of familial Alzheimer disease. J. Neuropathol. Exp. Neurol. 71, 868-881. doi: 10.1097/NEN.0b013e31826be03c.
29. Fritz, K. S., and Petersen, D. R. (2013). An overview of the chemistry and biology of reactive aldehydes. Free Radic. Biol. Med. 59, 85-91. doi: 10.1016/j.freeradbiomed.2012.06.025.
30. Gamliel, A., Afri, M., and Frimer, A. A. (2008). Determining radical penetration of lipid bilayers with new lipophilic spin traps. Free Radic. Biol. Med. 44, 1394-1405. doi: 10.1016/j.freeradbiomed.2007.12.028.
31. Gerstbrein, B., Stamatas, G., Kollias, N., and Driscoll, M. (2005). In vivo spectrofluorimetry reveals endogenous biomarkers that report healthspan and dietary restriction in Caenorhabditis elegans. Aging Cell 4, 127-137. doi: 10.1111/j.1474-9726.2005.00153.x.
32. Giles, G. I. (2009). "Redox-controlled transcription factors and gene expression," in Redox Signaling and Regulation in Biology and Medicine, eds C. Jacob, P. G. Winyard (Weinheim: Wiley-VCH Verlag GmbH&Co. KGaA), 245-270.
33. Gómez, J., Caro, P., Naudí, A., Portero-Otin, M., Pamplona, R., and Barja, G. (2007). Effect of 8.5% and 25% caloric restriction on mitochondrial free radical production and oxidative stress in rat liver. Biogerontology 8, 555-566. doi: 10.1007/s10522-007-9099-1.
34. Gonzalez-Covarrubias, V., Beekman, M., Uh, H. W., Dane, A., Troost, J., Paliukhovich, I., et al. (2013). Lipidomics of familial longevity. Aging Cell 12, 426-434. doi: 10.1111/acel.12064.
35. Guillou, H., Zadravec, D., Martin, P. G., and 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. doi: 10.1016/j.plipres.2009.12.002.
36. Gutiérrez, A. M., Reboredo, G. R., Arcemis, C. J., and Catalá, A. (2000). Non-enzymatic lipid peroxidation of microsomes and mitochondria isolated from liver and heart of pigeon and rat. Int. J. Biochem. Cell Biol. 32, 73-79. doi: 10.1016/S1357-2725(99)00105-3.
37. Haddad, L. S., Kelbert, L., and Hulbert, A. J. (2007). Extended longevity of queen honey bees compared to workers is associated with peroxidation-resistant membranes. Exp. Gerontol. 42, 601-609. doi: 10.1016/j.exger.2007.02.008.
38. Halliwell, B. (1999). Antioxidant defence mechanisms: from the beginning to the end (of the beginning). Free Radic. Res. 31, 261-272. doi: 10.1080/10715769900300841.
39. Halliwell, B., and Gutteridge, J. M. C. (2007). Free Radicals in Biology and Medicine. New York, NY: Oxford University Press.
40. Herrero, A., Portero-Otín, M., Bellmunt, M. J., Pamplona, R., and Barja, G. (2001). Effect of the degree of fatty acid unsaturation of rat heart mitochondria on their rates of H2O2 production and lipid and protein oxidative damage. Mech. Ageing Dev. 122, 427-443. doi: 10.1016/S0047-6374(01)00214-7.
41. Higdon, A., Diers, A. R., Oh, J. Y., Landar, A., and Darley-Usmar, V. M. (2012). Cell signaling by reactive lipid species: new concepts and molecular mechanisms. Biochem. J. 442, 453-464. doi: 10.1042/BJ20111752.
42. Hillyard, S. L., and German, J. B. (2009). Quantitative lipid analysis and life span of the fat-3 mutent of Caenorhabditis elegans. J. Agric. Food Chem. 57, 3389-3396. doi: 10.1021/jf8031414.
43. Holman, R. T. (1954). "Autoxidation of fats and related substances," in Progress in Chemistry of Fats and Other Lipids, eds R. T. Holman, W. O. Lundberg, and T. Malkin (London: Pergamon Press), 51-98.
44. Hulbert, A. J. (2011). Longevity, lipids and C. Elegans. Aging 3, 81-82.
45. Hulbert, A. J., Beard, L. A., and Grigg, G. C. (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. doi: 10.1016/j.exger.2008.05.015.
46. Hulbert, A. J., Faulks, S. C., and Buffenstein, R. (2006a). Oxidation-resistant membrane phospholipids can explain longevity differences among the longest-living rodents and similarly-sized mice. J. Gerontol. A Biol. Sci. Med. Sci. 61, 1009-1018. doi: 10.1093/gerona/61.10.1009.
47. Hulbert, A. J., Faulks, S. C., Harper, J. M., Miller, R. A., and Buffenstein, R. (2006b). Extended longevity of wild-derived mice is associated with peroxidation-resistant membranes. Mech. Ageing Dev. 127, 653-657. doi: 10.1016/j.mad.2006.03.002.
48. Hulbert, A. J., Pamplona, R., Buffenstein, R., and Buttemer, W. A. (2007). Life and death: metabolic rate, membrane composition, and life span of animals. Physiol. Rev. 87, 1175-1213. doi: 10.1152/physrev.00047.2006.
49. Imai, H., and Nakagawa, Y. (2003). Biological significance of phospholipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radic. Biol. Med. 34, 145-169. doi: 10.1016/S0891-5849(02)01197-8.
50. Itoh, Y. H., Sugai, A., Uda, I., and Itoh, T. (2001). The evolution of lipids. Adv. Space Res. 28, 719-724. doi: 10.1016/S0273-1177(01)00321-0.
51. Jacobson, J., Lambert, A. J., Portero-Otín, M., Pamplona, R., Magwere, T., Miwa, S., et al. (2010). Biomarkers of aging in Drosophila. Aging Cell 9, 466-477. doi: 10.1111/j.1474-9726.2010.00573.x.
52. Jobson, R. W., Nabholz, B., and Galtier, N. (2010). An evolutionary genome scan for longevity-related natural selection in mammals. Mol. Biol. Evol. 27, 840-847. doi: 10.1093/molbev/msp293.
53. Jové, M., Ayala, V., Ramírez-Núñez, O., Naudí, A., Cabré, R., Spickett, C. M., et al. (2013a). Specific lipidome signatures in central nervous system from methionine-restricted mice. J. Proteome Res. 12, 2679-2689. doi: 10.1021/pr400064a.
54. Jové, M., Naudi, A., Aledo, J. C., Cabre, R., Ayala, V., Portero-Otin, M., et al. (2013b). Plasma long-chain free fatty acids predict mammalian longevity. Sci. Rep. 3, 3346. doi: 10.1038/srep03346.
55. Laganiere, S., and Yu, B. P. (1987). Anti-lipoperoxidation action of food restriction. Biochem. Biophys. Res. Commun. 145, 1185-1191. doi: 10.1016/0006-291X(87)91562-2.
56. Laganiere, S., and Yu, B. P. (1993). Modulation of membrane phospholipid fatty acid composition by age and food restriction. Gerontology 39, 7-18. doi: 10.1159/000213509.
57. Lambert, A. J., Portero-Otin, M., Pamplona, R., and Merry, B. J. (2004). Effect of aging and caloric restriction on specific markers of protein oxidative damage and membrane peroxidizability in rat liver mitochondria. Mech. Ageing Dev. 125, 529-538. doi: 10.1016/j.mad.2004.06.002.
58. Lane, N. (2002). Oxygen. The Molecule That Made the World. New York, NY: Oxford University Press.
59. Lombard, J., López-García, P., and Moreira, D. (2012). The early evolution of lipid membranes and the three domains of life. Nat. Rev. Microbiol. 10, 507-515. doi: 10.1038/nrmicro2815.
60. Magwere, T., Pamplona, R., Miwa, S., Martinez-Diaz, P., Portero-Otin, M., Brand, M. D., et al. (2006). Flight activity, mortality rates, and lipoxidative damage in Drosophila. J. Gerontol. A Biol. Sci. Med. Sci. 61, 136-145. doi: 10.1093/gerona/61.2.136.
61. Maher, J., and Yamamoto, M. (2010). The rise of antioxidant signaling-The evolution and hermetic actions of Nrf2. Toxicol Appl. Pharmacol. 244, 4-15. doi: 10.1016/j.taap.2010.01.011.
62. McCord, J. M. (2000). The evolution of free radicals and oxidative stress. Am. J. Med. 108, 652-659. doi: 10.1016/S0002-9343(00)00412-5.
63. Miller, R. A., Harper, J. M., Dysko, R. C., Durkee, S. J., and Austad, S. N. (2002). Longer life spans and delayed maturation in wild-derived mice. Exp. Biol. Med. 227, 500-508.
64. Mitchell, T. W., Buffenstein, R., and Hulbert, A. J. (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. doi: 10.1016/j.exger.2007.09.004.
65. Moller, M., Botti, H., Batthyany, C., Rubbo, H., Radi, R., and Denicola, A. (2005). Direct measurement of nitric oxide and oxygen partitioning into liposomes and low density lipoprotein. J. Biol. Chem. 280, 8850-8854. doi: 10.1074/jbc.M413699200.
66. Montgomery, M. K., Hulbert, A. J., and Buttemer, W. A. (2011). The long life of birds: the rat-pigeon comparison revisited. PLoS ONE 6:e24138. doi: 10.1371/journal.pone.0024138.
67. Munro, D., and Blier, P. U. (2012). The extreme longevity of Arctica islandica is associated with increased peroxidation resistance in mitochondrial membranes. Aging Cell 11, 845-855. doi: 10.1111/j.1474-9726.2012.00847.x.
68. Nakamura, M. T., and Nara, T. Y. (2004). Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases. Annu. Rev. Nutr. 24, 345-376. doi: 10.1146/annurev.nutr.24.121803.063211.
69. Naudi, A., Ayala, V., Jove, M., Portero-Otin, M., Sriram, A., Sanz, A., et al. (2013). Membrane unsaturation contributes to stress resistance and longevity of wild-type and long-lived mutant strains of Drosophila melanogaster. FEBS. J. 280, 588-589.
70. Naudí, A., Caro, P., Jové, M., Gómez, J., Boada, J., Ayala, V., et al. (2007). Methionine restriction decreases endogenous oxidative molecular damage and increases mitochondrial biogenesis and uncoupling protein 4 in rat brain. Rejuvenation Res. 10, 473-484. doi: 10.1089/rej.2007.0538.
71. Naudí, A., Jové, M., Ayala, V., Cabré, R., Portero-Otín, M., and Pamplona, R. (2013). Non-enzymatic modification of aminophospholipids by carbonyl-amine reactions. Int. J. Mol. Sci. 14, 3285-3313. doi: 10.3390/ijms14023285.
72. Ohno-Iwashita, Y., Shimada, Y., Hayashi, M., and Inomata, M. (2010). Plasma membrane microdomains in aging and disease. Geriatr. Gerontol. Int. 10, S41-S52. doi: 10.1111/j.1447-0594.2010.00600.x.
73. Pamplona, R. (2008). Membrane phospholipids, lipoxidative damage and molecular integrity: a causal role in aging and longevity. Biochim. Biophys. Acta 1777, 1249-1262. doi: 10.1016/j.bbabio.2008.07.003.
74. Pamplona, R. (2011). Advanced lipoxidation end-products. Chem. Biol. Interact. 192, 14-20. doi: 10.1016/j.cbi.2011.01.007.
75. Pamplona, R., and Barja, G. (2003). "Aging rate, free radical production, ans constitutive sensitivity to lipid peroxidation: insights from comparative studies," in Biology of Aging and its Modulation Series, Vol. 1. Aging at the Molecular Level, ed T. Van Zglinicki (New York: Kluwer Academic Publisher), 47-64.
76. Pamplona, R., and Barja, G. (2006). Mitochondrial oxidative stress, aging and caloric restriction: the protein and methionine connection. Biochim. Biophys. Acta 1757, 496-508. doi: 10.1016/j.bbabio.2006.01.009.
77. Pamplona, R., and Barja, G. (2011). An evolutionary comparative scan for longevity-related oxidative stress resistance mechanisms in homeotherms. Biogerontology 12, 409-435. doi: 10.1007/s10522-011-9348-1.
78. Pamplona, R., Barja, G., and Portero-Otín, M. (2002a). Membrane fatty acid unsaturation, protection against oxidative stress, and maximum life span: a homeoviscous-longevity adaptation?. Ann. N.Y. Acad. Sci. 959, 475-490. doi: 10.1111/j.1749-6632.2002.tb02118.x.
79. Pamplona, R., Portero-Otin, M., Bellmunt, M. J., Gredilla, R., and Barja, G. (2002b). Aging increases Nepsilon-(carboxymethyl)lysine and caloric restriction decreases Nepsilon-(carboxyethyl)lysine and Nepsilon-(malondialdehyde)lysine in rat heart mitochondrial proteins. Free Radic. Res. 36, 47-54. doi: 10.1080/10715760210165.
80. Pamplona, R., Portero-Otín, M., Requena, J. R., Gredilla, R., and Barja, G. (2002c). Oxidative, glycoxidative and lipoxidative damage to rat heart mitochondrial proteins is lower after 4 months of caloric restriction than in age-matched controls. Mech. Ageing Dev. 123, 1437-1446. doi: 10.1016/S0047-6374(02)00076-3.
81. Pamplona, R., and Costantini, D. (2011). Molecular and structural antioxidant defences against oxidative stress in animals. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301, R843-R863. doi: 10.1152/ajpregu.00034.2011.
82. Pamplona, R., Portero-Otín, M., Requena, J. R., Thorpe, S. R., Herrero, A., and Barja, G. (1999a). A low degree of fatty acid unsaturation leads to lower lipid peroxidation and lipoxidation-derived protein modification in heart mitochondria of the longevous pigeon than in the short-lived rat. Mech. Ageing Dev. 106, 283-296. doi: 10.1016/S0047-6374(98)00121-3.
83. Pamplona, R., Portero-Otín, M., Riba, D., Ledo, F., Gredilla, R., Herrero, A., et al. (1999b). Heart fatty acid unsaturation and lipid peroxidation, and aging rate, are lower in the canary and the parakeet than in the mouse. Aging (Milano) 11, 44-49. doi: 10.1016/j.cbi.2011.01.007.
84. Pamplona, R., Portero-Otín, M., Riba, D., Requena, J. R., Thorpe, S. R., López-Torres, M., et al. (2000a). Low fatty acid unsaturation: a mechanism for lowered lipoperoxidative modification of tissue proteins in mammalian species with long life spans. J. Gerontol. A Biol. Sci. Med. Sci. 55, B286-B291. doi: 10.1093/gerona/55.6.B286.
85. Pamplona, R., Portero-Otín, M., Ruiz, C., Gredilla, R., Herrero, A., and Barja, G. (2000b). Double bond content of phospholipids and lipid peroxidation negatively correlate with maximum longevity in the heart of mammals. Mech. Ageing Dev. 112, 169-183. doi: 10.1016/S0047-6374(99)00045-7.
86. Pamplona, R., Portero-Otín, M., Riba, D., Ruiz, C., Prat, J., Bellmunt, M. J., et al. (1998). Mitochondrial membrane peroxidizability index is inversely related to maximum life span in mammals. J. Lipid Res. 39, 1989-1994.
87. Pamplona, R., Portero-Otín, M., Sanz, A., Ayala, V., Vasileva, E., and Barja, G. (2005). Protein and lipid oxidative damage and complex I content are lower in the brain of budgerigards and canaries than in mice. Relation to aging rate. Age 27, 267-280. doi: 10.1007/s11357-005-4562-x.
88. Pamplona, R., Portero-Otin, M., Sanz, A., Requena, J., and Barja, G. (2004). Modification of the longevity-related degree of fatty acid unsaturation modulates oxidative damage to proteins and mitochondrial DNA in liver and brain. Exp. Gerontol. 39, 725-733. doi: 10.1016/j.exger.2004.01.006.
89. Pamplona, R., Prat, J., Cadenas, S., Rojas, C., Pérez-Campo, R., López-Torres, M., et al. (1996). Low fatty acid unsaturation protects against lipid peroxidation in liver mitochondria from long-lived species: the pigeon and human case. Mech. Ageing Dev. 86, 53-66. doi: 10.1016/0047-6374(95)01673-2.
90. Park, J. W., Choi, C. H., Kim, M. S., and Chung, M. H. (1996). Oxidative status in senescence accelerated mice. J. Gerontol. A Biol. Sci. Med. Sci. 51, B337-B345. doi: 10.1093/gerona/51A.5.B337.
91. Philipp, E. E., and Abele, D. (2010). Masters of longevity: lessons from long-lived bivalves-a mini-review. Gerontology 56, 55-65. doi: 10.1159/000221004.
92. Portero-Otin, M., Bellmunt, M. J., Requena, J. R., and Pamplona, R. (2003). Protein modification by advanced Maillard adducts can be modulated by dietary polyunsaturated fatty acids. Biochem. Soc. Trans. 31, 1403-1405. doi: 10.1042/BST0311403.
93. Portero-Otín, M., Bellmunt, M. J., Ruiz, M. C., Barja, G., and Pamplona, R. (2001). Correlation of fatty acid unsaturation of the major liver mitochondrial phospholipid classes in mammals to their maximum life span potential. Lipids 36, 491-498. doi: 10.1007/s11745-001-0748-y.
94. Portero-Otín, M., Requena, J. R., Bellmunt, M. J., Ayala, V., and Pamplona, R. (2004). Protein nonenzymatic modifications and proteasome activity in skeletal muscle from the short-lived rat and long-lived pigeon. Exp. Gerontol. 39, 1527-1535. doi: 10.1016/j.exger.2004.08.001.
95. Puca, A. A., Andrew, P., Novelli, V., Anselmi, C. V., Somalvico, F., Cirillo, N. A., et al. (2008). Fatty acid profile of erythrocyte membranes as possible biomarker of longevity. Rejuvenation Res. 11, 63-72. doi: 10.1089/rej.2007.0566.
96. Rabini, R. A., Moretti, N., Staffolani, R., Salvolini, E., Nanetti, L., Franceschi, C., et al. (2002). Reduced susceptibility to peroxidation of erythrocyte plasma membranes from centenarians. Exp. Gerontol. 37, 657-663. doi: 10.1016/S0531-5565(02)00006-2.
97. Rao, G., Xia, E., Nadakavukaren, M. J., and Richardson, A. (1990). Effect of dietary restriction on the age-dependent changes in the expression of antioxidant enzymes in rat liver. J. Nutr. 120, 602-609.
98. Ruiz, M. C., Ayala, V., Portero-Otín, M., Requena, J. R., Barja, G., and Pamplona, R. (2005). Protein methionine content and MDA-lysine protein adducts are inversely related to maximum life span in the heart of mammals. Mech. Ageing Dev. 126, 1106-1114. doi: 10.1016/j.mad.2005.04.005.
99. Sanz, A., Caro, P., Ayala, V., Portero-Otin, M., Pamplona, R., and Barja, G. (2006). Methionine restriction decreases mitochondrial oxygen radical generation and leak as well as oxidative damage to mitochondrial DNA and proteins. FASEB J. 20, 1064-1073. doi: 10.1096/fj.05-5568com.
100. Sanz, A., Gredilla, R., Pamplona, R., Portero-Otín, M., Vara, E., Tresguerres, J. A., et al. (2005). Effect of insulin and growth hormone on rat heart and liver oxidative stress in control and caloric restricted animals. Biogerontology 6, 15-26. doi: 10.1007/s10522-004-7380-0.
101. Sanz, A., Soikkeli, M., Portero-Otín, M., Wilson, A., Kemppainen, E., McIlroy, G., et al. (2010). Expression of the yeast NADH dehydrogenase Ndi1 in Drosophila confers increased lifespan independently of dietary restriction. Proc. Natl. Acad. Sci. U.S.A. 107, 9105-9110. doi: 10.1073/pnas.0911539107.
102. Schirrmeister, B. E., de Vos, J. M., Antonelli, A., and Bagheri, H. C. (2013). Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event. Proc. Natl. Acad. Sci. U.S.A. 110, 1791-1796. doi: 10.1073/pnas.1209927110.
103. Sheehan, D., Meade, G., Foley, V. M., and Dowd, C. A. (2001). Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem. J. 360, 1-16. doi: 10.1042/0264-6021:3600001.
104. Shi, Y., Pulliam, D. A., Liu, Y., Hamilton, R. T., Jernigan, A. L., Bhattacharya, A., et al. (2013). Reduced mitochondrial ROS, enhanced antioxidant defense, and distinct age-related changes in oxidative damage in muscles of long-lived Peromyscus leucopus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 304, R343-R355. doi: 10.1152/ajpregu.00139.2012.
105. Shmookler Reis, R. J., Xu, L., Lee, H., Chae, M., Thaden, J. J., Bharill, P., et al. (2011). Modulation of lipid biosynthesis contributes to stress resistance and longevity of C. elegans mutants. Aging 3, 125-147. doi: 10.1007/s00360-013-0786-8.
106. Terman, A., and Brunk, U. T. (2004). Lipofuscin. Int. J. Biochem. Cell Biol. 36, 1400-1404. doi: 10.1016/j.biocel.2003.08.009.
107. Thorpe, S. R., and Baynes, J. W. (2003). Maillard reaction products in tissue proteins: new products and new perspectives. Amino Acids 25, 275-281. doi: 10.1007/s00726-003-0017-9.
108. Tomoiu, A., Larbi, A., Fortin, C., Dupuis, G., and Fulop, T. Jr. (2007). Do membrane rafts contribute to human immunosenescence? Ann. N.Y. Acad. Sci. 1100, 98-110. doi: 10.1196/annals.1395.008.
109. Tsuchida, M., Miura, T., and Aibara, K. (1987). Lipofuscin and lipofuscin-like substances. Chem. Phys. Lipids 44, 297-325. doi: 10.1016/0009-3084(87)90055-7.
110. Tsuduki, T., Honma, T., Nakagawa, K., Ikeda, I., and Miyazawa, T. (2011). Long-term intake of fish oil increases oxidative stress and decreases lifespan in senescence-accelerated mice. Nutrition 27, 334-337. doi: 10.1016/j.nut.2010.05.017.
111. Valencak, T. G., and Ruf, T. (2007). N-3 polyunsaturated fatty acids impair lifespan but have no role for metabolism. Aging Cell 6, 15-25. doi: 10.1111/j.1474-9726.2006.00257.x.
112. Valencak, T. G., and Ruf, T. (2013). Phospholipid composition and longevity: lessons from Ames dwarf mice. Age 35, 2303-2313. doi: 10.1007/s11357-013-9533-z.
113. Vance, D. E., and Vance, J. E. (1996). Biochemistry of Lipids, Lipoproteins and Membranes. Amsterdam: Elsevier Science BV.
114. Van Meer, G., Voelker, D. R., and Feigenson, G. W. (2008). Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112-124. doi: 10.1038/nrm2330.
115. Wakabayashi, N., Dinkova-Kostova, A. T., Holtzclaw, W. D., Kang, M. I., Kobayashi, A., Yamamoto, M., et al. (2004). Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc. Natl. Acad. Sci. U.S.A. 101, 2040-2045. doi: 10.1073/pnas.0307301101.
116. Wallis, J. G., Watts, J. L., and Browse, J. (2002). Polyunsaturated fatty acid synthesis: what will they think of next?. Trends Biochem. Sci. 27, 467-473. doi: 10.1016/S0968-0004(02)02168-0.
117. Wanamaker, A. D. Jr., Heinemeier, J., Scourse, J. D., Richardson, C. A., Butler, P. G., Eiriksson, J., et al. (2008). Very long-lived mollusks confirm 17th century AD tephra-based radiocarbon reservoir ages for North Icelandic shelf waters. Radiocarbon 50, 399-412.
118. West, J. D., and Marnett, L. J. (2006). Endogenous reactive intermediates as modulators of cell signaling and cell death. Chem. Res. Toxicol. 19, 173-194. doi: 10.1021/tx050321u.
119. Winston, M. L. (1987). The Biology of the Honey Bee. Cambridge MA: Harvard University Press.
120. Yeagle, P. (1993). The Membranes of Cells. San Diego, CA: Academic Press.
121. Yu, B. P. (2005). Membrane alteration as a basis of aging and the protective effects of calorie restriction. Mech. Ageing Dev. 126, 1003-1010. doi: 10.1016/j.mad.2005.03.020.
122. Yu, B. P., Suescun, E. A., and Yang, S. Y. (1992). Effect of age-related lipid peroxidation on membrane fluidity and phospholipase A2: modulation by dietary restriction. Mech. Ageing Dev. 65, 17-33. doi: 10.1016/0047-6374(92)90123-U.
123. Zimniak, P. (2011). Relationship of electrophilic stress to aging. Free Radic. Biol. Med. 51, 1087-1105. doi: 10.1016/j.freeradbiomed.2011.05.039.