The long life of birds: The rat-pigeon comparison revisited

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Montgomery, Magdalene K ^a   Hulbert, A J ^b   Buttemer, William A ^c  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF WOLLONGONG   (Australia)

^c DEAKIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; CATALASE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; LIPID HYDROPEROXIDE; MEMBRANE LIPID; REACTIVE OXYGEN METABOLITE; SUCCINIC ACID; SUPEROXIDE; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; FATTY ACID;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; HEART MITOCHONDRION; LIFESPAN; LIPID COMPOSITION; LIPID PEROXIDATION; LIVER MITOCHONDRION; LONGEVITY; MAXIMUM LIFESPAN POTENTIAL; MEMBRANE DAMAGE; MITOCHONDRIAL RESPIRATION; MUSCLE MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PIGEON; PROTEIN CARBONYLATION; RAT; SKELETAL MUSCLE; AGING; ANIMAL; BIRD; METABOLISM; MITOCHONDRION; PHYSIOLOGY; PIGEONS AND DOVES;

AVES; COLUMBA; MAMMALIA; RATTUS;

AGING; ANIMALS; BIRDS; CATALASE; COLUMBIDAE; FATTY ACIDS, NONESTERIFIED; GLUTATHIONE PEROXIDASE; LIPID PEROXIDATION; LONGEVITY; MITOCHONDRIA; MITOCHONDRIA, HEART; MITOCHONDRIA, LIVER; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; SUPEROXIDES;

EID: 80052337273     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024138     Document Type: Article

References (80)

1. 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.
2. Lindstedt SL, Calder WA, (1976) Body Size and Longevity in Birds. Condor 78: 91-94.
3. Pearl R, (1928) The rate of living. New York Knopf.
4. Rubner M, (1908) Das Problem der Lebensdauer. Munich, Oldenburg.
5. Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ, (1991) Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem J 275 (Pt 1): 81-86.
6. Lasiewski RC, Dawson WR, (1967) A Re-Examination of Relation between Standard Metabolic Rate and Body Weight in Birds. Condor 69: 13-23.
7. Gerschman R, Gilbert DL, Nye SW, Dwyer P, Fenn WO, (1954) Oxygen poisoning and x-irradiation: a mechanism in common. Science 119: 623-626.
8. Harman D, (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11: 298-300.
9. Brown JCL, McClelland GB, Faure PA, Klaiman JM, Staples JF, (2009) Examining the mechanisms responsible for lower ROS release rates in liver mitochondria from the long-lived house sparrow (Passer domesticus) and big brown bat (Eptesicus fuscus) compared to the short-lived mouse (Mus musculus). Mech Ageing Dev 130: 467-476.
10. Buffenstein R, Edrey YH, Yang T, Mele J, (2008) The oxidative stress theory of aging: embattled or invincible? Insights from non-traditional model organisms. Age 30: 99-109.
11. Staniek K, Nohl H, (2000) Are mitochondria a permanent source of reactive oxygen species? Biochim Biophys Acta 1460: 268-275.
12. Hulbert AJ, (2005) On the importance of fatty acid composition of membranes for aging. J Theor Biol 234: 277-288.
13. Matkovics B, Novak R, Hanh HD, Szabo L, Varga I, et al. (1977) A comparative study of some more important experimental animal peroxide metabolism enzymes. Comp Biochem Physiol B 56: 31-34.
14. Barja G, Cadenas S, Rojas C, Lopez-Torres M, Perez-Campo R, (1994) A decrease of free radical production near critical targets as a cause of maximum longevity in animals. Comp Biochem Physiol Biochem Mol Biol 108: 501-512.
15. Ku H, Sohal R, (1993) Comparison of mitochondrial proxidant generation and antioxidant defenses between rat and pigeon- possible basis of variation in longevity and metabolic potential. Mech Ageing Dev 72: 67-76.
16. Lambert AJ, Buckingham JA, Boysen HM, Brand MD, (2010) Low complex I content explains the low hydrogen peroxide production rate of heart mitochondria from the long-lived pigeon, Columba livia. Aging Cell 9: 78-91.
17. Sasaki T, Unno K, Tahara S, Shimada A, Chiba Y, et al. (2008) Age-related increase of superoxide generation in the brains of mammals and birds. Aging Cell 7: 459-469.
18. Cutler RG, (1985) Peroxide-producing potential of tissues: inverse correlation with longevity of mammalian species. Proc Natl Acad Sci U S A 82: 4798-4802.
19. Perez-Campo R, Lopez-Torres M, Rojas C, Cadenas S, Barja G, (1994) Longevity and antioxidant enzymes, non-enzymatic antioxidants and oxidative stress in the vertebrate lung: a comparative study. J Comp Physiol B 163: 682-689.
20. Barja G, Cadenas S, Rojas C, Perez-Campo R, Lopez-Torres M, (1994) Low mitochondrial free radical production per unit O2 consumption can explain the simultaneous presence of high longevity and high aerobic metabolic rate in birds. Free Radic Res 21: 317-327.
21. Lambert AJ, Boysen HM, Buckingham JA, Yang T, Podlutsky A, et al. (2007) Low rates of hydrogen peroxide production by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeotherms. Aging Cell 6: 607-618.
22. Herrero A, Barja G, (1997) Sites and mechanisms responsible for the low rate of free radical production of heart mitochondria in the long-lived pigeon. Mech Ageing Dev 98: 95-111.
23. Hulbert AJ, Turner N, Hinde J, Else P, Guderley H, (2006) How might you compare mitochondria from different tissues and different species? J Comp Physiol B 176: 93-105.
24. Agarwal S, Sohal RS, (1996) Relationship between susceptibility to protein oxidation, aging, and maximum life span potential of different species. Exp Gerontol 31: 365-372.
25. Pamplona R, Portero-Otin M, Requena JR, Thorpe SR, Herrero A, et al. (1999) 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.
26. Pamplona R, Prat J, Cadenas S, Rojas C, Perez-Campo R, 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.
27. Lopez-Torres M, Perez-Campo R, Cadenas S, Rojas C, Barja G, (1993) A comparative study of free radicals in vertebrates--II. Non-enzymatic antioxidants and oxidative stress. Comp Biochem Physiol B 105: 757-763.
28. Portero-Otin M, Requena JR, Bellmunt MJ, Ayala V, 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.
29. Hulbert AJ, (2008) The links between membrane composition, metabolic rate and lifespan. Comp Biochem Physiol A Mol Integr Physiol 150: 196-203.
30. Trzcionka M, Withers KW, Klingenspor M, Jastroch M, (2008) The effects of fasting and cold exposure on metabolic rate and mitochondrial proton leak in liver and skeletal muscle of an amphibian, the cane toad Bufo marinus. J Exp Biol 211: 1911-1918.
31. Gornall AG, Bardawill CJ, David MM, (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177: 751-766.
32. Reynafarje B, Costa LE, Lehninger AL, (1985) O2 solubility in aqueous media determined by a kinetic method. Anal Biochem 145: 406-418.
33. St-Pierre J, Buckingham J, Roebuck S, Brand M, (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277: 44784-44790.
34. Gredilla R, Sanz A, Lopez-Torres M, Barja G, (2001) Caloric restriction decreases mitochondrial free radical generation at complex I and lowers oxidative damage to mitochondrial DNA in the rat heart. FASEB J 15: 1589-1591.
35. Erel O, (2004) A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 37: 277-285.
36. Benzie IF, Strain JJ, (1996) The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. Anal Biochem 239: 70-76.
37. Mccord JM, Fridovich I, (1969) Superoxide Dismutase an Enzymic Function for Erythrocuprein (Hemocuprein). J Biol Chem 244: 6049-6055.
38. Maral J, Puget K, Michelson AM, (1977) Comparative study of superoxide dismutase, catalase and glutathione peroxidase levels in erythrocytes of different animals. Biochem Biophys Res Commun 77: 1525-1535.
39. Cao G, Cutler RG, (1995) Protein oxidation and aging. I. Difficulties in measuring reactive protein carbonyls in tissues using 2,4-dinitrophenylhydrazine. Arch Biochem Biophys 320: 106-114.
40. Baeza E, Chartrin P, Meteau K, Bordeau T, Juin H, et al. (2010) Effect of sex and genotype on carcase composition and nutritional characteristics of chicken meat. Br Poult Sci 51: 344-353.
41. Bize P, Devevey G, Monaghan P, Doligez B, Christe P, (2008) Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology 89: 2584-2593.
42. Price ER, Guglielmo CG, (2009) The effect of muscle phospholipid fatty acid composition on exercise performance: a direct test in the migratory white-throated sparrow (Zonotrichia albicollis). Am. J. Physiol. Regul. Integr. Comp. Physiol 297: R775-R782.
43. Wiersma P, Selman C, Speakman JR, Verhulst S, (2004) Birds sacrifice oxidative protection for reproduction. Proc R Soc Lond [Biol] 271: S360-S363.
44. Chang CK, Huang HY, Tseng HF, Hsuuw YD, Tso TK, (2007) Interaction of vitamin E and exercise training on oxidative stress and antioxidant enzyme activities in rat skeletal muscles. J Nutr Biochem 18: 39-45.
45. Ji LL, Dillon D, Wu E, (1990) Alteration of antioxidant enzymes with aging in rat skeletal muscle and liver. Am J Physiol 258: R918-923.
46. Lambert AJ, Brand MD, (2004) Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Biol Chem 279: 39414-39420.
47. Larrain RE, Richards MP, Schaefer DM, Ji LL, Reed JD, (2007) Growth performance and muscle oxidation in rats fed increasing amounts of high-tannin sorghum. J Anim Sci 85: 3276-3284.
48. Pinho RA, Andrades ME, Oliveira MR, Pirola AC, Zago MS, et al. (2006) Imbalance in SOD/CAT activities in rat skeletal muscles submitted to treadmill training exercise. Cell Biol Int 30: 848-853.
49. Tahara EB, Navarete FD, Kowaltowski AJ, (2009) Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation. Free Radic Biol Med 46: 1283-1297.
50. Brand MD, (2010) The sites and topology of mitochondrial superoxide production. Exp Gerontol 45: 466-472.
51. Dargel R, (1974) Effect of Ca2+ on coupling of rat liver mitochondria. FEBS Lett 42: 57-60.
52. Hinkle PC, Yu ML, (1979) The phosphorus/oxygen ratio of mitochondrial oxidative phosphorylation. J Biol Chem 254: 2450-2455.
53. Halliwell B, Gutteridge JMC, (2007) Free Radicals in Biology and Medicine. In: Halliwell B, Gutteridge JMC, editors. New York Oxford University Press.
54. Kojima T, Kikugawa K, Kosugi H, (1990) Is the thiobarbituric acid-reactivity of blood plasma specific to lipid peroxidation? Chem Pharm Bull (Tokyo) 38: 3414-3418.
55. Lapenna D, Ciofani G, Pierdomenico SD, Giamberardino MA, Cuccurullo F, (2001) Reaction conditions affecting the relationship between thiobarbituric acid reactivity and lipid peroxides in human plasma. Free Radic Biol Med 31: 331-335.
56. Hulbert AJ, Trzcionka M, Buttemer WA, (2010) Membrane fatty acid composition and longevity of mammals and birds. In: Pamplona r, Barja G, editors. Longevity, mitochondria and oxygen free radicals.
57. Ku HH, Brunk UT, Sohal RS, (1993) Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species. Free Radic Biol Med 15: 621-627.
58. Muller FL, Liu Y, Abdul-Ghani MA, Lustgarten MS, Bhattacharya A, et al. (2008) High rates of superoxide production in skeletal-muscle mitochondria respiring on both complex I- and complex II-linked substrates. Biochem J 409: 491-499.
59. Jacobson J, Lambert AJ, Portero-Otin M, Pamplona R, Magwere T, et al. (2010) Biomarkers of aging in Drosophila. Aging Cell 9: 466-477.
60. Pérez V, Buffenstein R, Masamsetti V, Leonard S, Salmon A, et al. (2009) Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole-rat. Proc Natl Acad Sci U S A 106: 3059-3064.
61. Giron-Calle J, Schmid PC, Schmid HH, (1997) Effects of oxidative stress on glycerolipid acyl turnover in rat hepatocytes. Lipids 32: 917-923.
62. Toppo S, Flohe L, Ursini F, Vanin S, Maiorino M, (2009) Catalytic mechanisms and specificities of glutathione peroxidases: variations of a basic scheme. Biochim Biophys Acta 1790: 1486-1500.
63. Ursini F, Maiorino M, Gregolin C, (1985) The selenoenzyme phospholipid hydroperoxide glutathione peroxidase. Biochim Biophys Acta 839: 62-70.
64. Cordis GA, Maulik G, Bagchi D, Riedel W, Das DK, (1998) Detection of oxidative DNA damage to ischemic reperfused rat hearts by 8-hydroxydeoxyguanosine formation. J Mol Cell Cardiol 30: 1939-1944.
65. Valavanidis A, Vlachogianni T, Fiotakis C, (2009) 8-hydroxy-2′-deoxyguanosine (8-OHdG): A critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 27: 120-139.
66. Berlett BS, Stadtman ER, (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272: 20313-20316.
67. Onyango AN, Baba N, (2010) New hypotheses on the pathways of formation of malondialdehyde and isofurans. Free Radic Biol Med 49: 1594-1600.
68. Andziak B, Buffenstein R, (2006) Disparate patterns of age-related changes in lipid peroxidation in long-lived naked mole-rats and shorter-lived mice. Aging Cell 5: 525-532.
69. Andziak B, O'Connor TP, Qi W, DeWaal EM, Pierce A, et al. (2006) High oxidative damage levels in the longest-living rodent, the naked mole-rat. Aging Cell 5: 463-471.
70. Wilhelm Filho D, Althoff SL, Dafre AL, Boveris A, (2007) Antioxidant defenses, longevity and ecophysiology of South American bats. Comp Biochem Physiol C Toxicol Pharmacol 146: 214-220.
71. Gutierrez AM, Reboredo GR, Arcemis CJ, Catala 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.
72. Abbott SK, Else PL, Hulbert AJ, (2010) Membrane fatty acid composition of rat skeletal muscle is most responsive to the balance of dietary n-3 and n-6 PUFA. Br J Nutr 103: 522-529.
73. Hulbert AJ, Turner N, Storlien LH, Else P, (2005) Dietary fats and membrane function: implications for metabolism and disease. Biol Rev 80: 155-169.
74. 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.
75. Greenberg ME, Li XM, Gugiu BG, Gu XD, Qin J, et al. (2008) The lipid whisker model of the structure of oxidized cell membranes. J Biol Chem 283: 2385-2396.
76. 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.
77. Hulbert AJ, Faulks SC, Buffenstein R, (2006) 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.
78. Shmookler Reis RJ, Xu L, Lee H, Chae M, Thaden JJ, et al. (2010) Modulation of lipid biosynthesis contributes to stress resistance and longevity of C. elegans mutants. Aging (Albany NY) 3: 125-147.
79. Hulbert AJ, Longevity, lipids and C. elegans. Aging (Albany NY) 3: 81-82.
80. Jobson RW, Nabholz B, Galtier N, (2010) An evolutionary genome scan for longevity-related natural selection in mammals. Mol Biol Evol 27: 840-847.