Thrifty development: Early-life diet restriction reduces oxidative damage during later growth

Functional Ecology

Volumn 25, Issue 5, 2011, Pages 1144-1153

  Noguera, José C ^a   Lores, Marta ^b   Alonso Álvarez, Carlos ^c   Velando, Alberto ^a  

^a UNIVERSITY OF VIGO   (Spain)

^b UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^c INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

Author keywords

Caloric restriction; Compensatory response; Larus michahellis; Oxidative stress; Phenotypic programming; Vitamin E; Yellow legged gull

Indexed keywords

ANTIOXIDANT; COMPENSATION; DIET; EVOLUTIONARY BIOLOGY; FOOD INTAKE; FOOD SUPPLEMENTATION; LIFE HISTORY TRAIT; LONG-TERM CHANGE; OXYGEN; SEABIRD; TRADE-OFF; VITAMIN; WILD POPULATION;

ANIMALIA; LARUS MICHAHELLIS;

EID: 80053133339     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2011.01856.x     Document Type: Article

References (75)

1. Alonso-Alvarez, C., Bertrand, S., Devevey, G., Prost, J., Faivre, B., Chastel, O. & Sorci, G. (2006) An experimental manipulation of life-history trajectories and resistance to oxidative stress. Evolution, 60, 1913-1924.
2. Alonso-Alvarez, C., Bertrand, S., Faivre, B. & Sorci, G. (2007) Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches. Functional Ecology, 21, 873-879.
3. de Ayala, R.M., Martinelli, R. & Saino, N. (2006) Vitamin E supplementation enhances growth and condition of nestling barn swallows (Hirundo rustica). Behavioral Ecology and Sociobiology, 60, 619-630.
4. Berg, B.N. & Simms, H.S. (1960) Nutrition and longevity in the rat: II. Longevity and the onset of disease with different levels of intake. Journal of Nutrition, 71, 255-263.
5. Boncoraglio, G., Rubolini, D., Romano, M., Martinelli, R. & Saino, N. (2006) Effects of elevated yolk androgens on perinatal begging behaviour in yellow-legged gull (Larus michahellis) chicks. Hormones and Behavior, 50, 442-447.
6. Brambilla, G., Fiori, M. & Archetti, L.I. (2001) Evaluation of the oxidative stress in growing pigs by microplate assays. Journal of Veterinary Medicine Series A, 48, 33-38.
7. Burdge, G.C., Hanson, M.A., Slater-Jefferies, J.L. & Lillycrop, K.A. (2007) Epigenetic regulation of transcription: a mechanism for inducing variations in phenotype (fetal programming) by differences in nutrition during early life? British Journal of Nutrition, 97, 1036-1046.
8. Cabelof, D.C., Yanamadala, S., Raffoul, J.J., Guo, Z., Soofi, A. & Heydari, A.R. (2003) Caloric restriction promotes genomic stability by induction of base excision repair and reversal of its age-related decline. DNA Repair, 2, 295-307.
9. Calabrese, E.J. & Baldwin, L.A. (2003) Hormesis: the dose-response revolution. Annual Review of Pharmacology and Toxicology, 43, 175-197.
10. Cichon, M. (1997) Evolution of longevity through optimal resource allocation. Proceedings of the Royal Society of London B, Biological Sciences, 264, 1383-1388.
11. Costantini, D., Metcalfe, N.B. & Monaghan, P. (2010) Ecological processes in a hormetic framework. Ecology Letters, 13, 1435-1447.
12. Dimova, E.G., Bryant, P.E. & Chankova, S.G. (2008) 'Adaptive response': some underlying mechanisms and open questions. Genetics and Molecular Biology, 31, 396-408.
13. Dizdaroglu, M., Laval, J. & Boiteux, S. (1993) Substrate specificity of the Escherichia coli endonuclease III: excision of thymine- and cytosine-derived lesions in DNA produced by radiation-generated free radicals. Biochemistry, 32, 12105-12111.
14. Dubey, A., Forster, M.J., Lal, H. & Sohal, R.S. (1996) Effect of age and caloric intake on protein oxidation in different brain regions and on behavioral functions of the mouse. Archives of Biochemistry and Biophysics, 333, 189-197.
15. Erel, O. (2004) A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clinical Biochemistry, 37, 277-285.
16. Finkel, T. & Holbrook, N.J. (2000) Oxidants, oxidative stress and the biology of ageing. Nature, 408, 239-247.
17. Forster, M.J., Sohal, B.H. & Sohal, R.S. (2000) Reversible effects of long-term caloric restriction on protein oxidative damage. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 55, 522-529.
18. Gedik, C.M. & Collins, A. (2005) Establishing the background level of base oxidation in human lymphocyte DNA: results of an interlaboratory validation study. FASEB Journal, 19, 82-84.
19. Girard, P.M., Guibourt, N. & Boiteux, S. (1997) The Ogg1 protein of S cerevisiae: a 7, 8-dihydro-8-oxoguanine DNA glycosylase/AP lyase whose lysine 241 is a critical residue for catalytic activity. Nucleic Acids Research, 25, 3404-3411.
20. Gluckman, P.D., Hanson, M.A. & Beedle, A.S. (2007) Early life events and their consequences for later disease: a life history and evolutionary perspective. American Journal of Human Biology, 19, 1-19.
21. Gredilla, R. & Barja, G. (2005) The role of oxidative stress in relation to caloric restriction and longevity. Endocrinology, 146, 3713-3717.
22. 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 Journal, 15, 1589-1591.
23. Hall, M.E., Blount, J.D., Forbes, S. & Royle, N.J. (2009) Does oxidative stress mediate the trade-off between growth and self-maintenance in structured families? Functional Ecology, 32, 365-373.
24. Halliwell, B. & Gutteridge, J.M.C. (2007) Free Radicals in Biology and Medicine. Oxford University Press Inc, New York.
25. Han, E.S., Levin, N., Bengani, N., Roberts, J.L., Suh, Y., Karelus, K. & Nelson, J.R. (1995) Hyperadrenocorticism and food restriction-induced life extension in the rat: evidence for divergent regulation of pituitary proopiomelanocortin RNA and adrenocorticotropic hormone biosynthesis. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 50, 288-294.
26. Honarmand, M., Goymann, W. & Naguib, M. (2010) Stressful dieting: nutritional conditions but not compensatory growth elevate corticosterone levels in Zebra finch nestlings and fledglings. PLoS ONE, 5, e12930.
27. Jackson, S.P. & Bartek, J. (2009) The DNA-damage response in human biology and disease. Nature, 461, 1071-1078.
28. Kaneko, G., Yoshinaga, T., Yanagawa, Y., Ozaki, Y., Tsukamoto, K. & Watabe, S. (2011) Calorie restriction-induced maternal longevity is transmitted to their daughters in a rotifer. Functional Ecology, 25, 209-216.
29. Karatas, F., Karatepe, M. & Baysar, A. (2002) Determination of free malondialdehyde in human serum by high performance liquid chromatography. Analytical Biochemistry, 311, 76-79.
30. Kim, S.Y., Noguera, J.C., Morales, J. & Velando, A. (2011) Quantitative genetic evidence for trade-off between growth and resistance to oxidative stress in a wild bird. Evolutionary Ecology, 25, 461-472.
31. Kitaysky, A.S., Piatt, J.F., Wingfield, J.C. & Romano, M. (1999) The adrenocortical stress response of black-legged kittiwake chicks in relation to dietary restrictions. Journal of Comparative Physiology B, Biochemical Systemic and Environmental Physiology, 169, 303-310.
32. Kow, Y.W. & Dare, A. (2000) Detection of Abasic sites and oxidative DNA base damage using an ELISA-Like assay. Methods, 22, 164-169.
33. Le Bourg, E. (2003) Delaying aging: could the study of hormesis be more helpful than that of the genetic pathway used to survive starvation? Biogerontology, 4, 319-324.
34. Lessells, C.M., Boag & P.T. (1987) Unrepeatable repeatabilities: a common mistake. Auk, 104, 116-121.
35. Levine, R.L., Garland, D., Oliver, C.N., Amici, A., Climent, I., Lenz, A.G., Ahn, B.W., Shaltiel, S. & Stadtman, E.R. (1990) Determination of carbonyl content in oxidatively modified proteins. Methods in Enzymology, 186, 464-478.
36. Lindström, J. (1999) Early development and fitness in birds and mammals. Trends in Ecology and Evolution, 14, 343-348.
37. Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D. & Schabenberger, O. (2006) SAS System for Mixed Models, 2nd edn. SAS Institute Inc, Cary, NC, USA.
38. López-Torres, M., Gredilla, R., Sanz, A. & Barja, G. (2002) Influence of aging and long-term caloric restriction on oxygen radical generation and oxidative DNA damage in rat liver mitochondria. Free Radical Biology and Medicine, 32, 882-889.
39. Lummaa, V. & Clutton-Brock, T. (2002) Early development, survival and reproduction in humans. Trends in Ecology and Evolution, 17, 141-147.
40. Mangel, M. (2008) Environment, damage and senescence: modelling the life-history consequences of variable stress and caloric intake. Functional Ecology, 22, 422-430.
41. Masoro, E.J. (1998) Hormesis and the antiaging action of dietary restriction. Experimental Gerontology, 33, 61-66.
42. Masoro, E.J. (2005) Overview of caloric restriction and ageing. Mechanisms of Ageing and Development, 126, 913-922.
43. Masoro, E.J. (2006) Dietary restriction-induced life extension: a broadly based biological phenomenon. Biogerontology, 7, 153-155.
44. Matsuo, M., Gomi, F., Kuramoto, K. & Sagai, M. (1993) Food restriction suppresses an age-dependent increase in exhalation rate of pentane from rats: a longitudinal study. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 48, 133-138.
45. Mattson, M.P. (2008) Hormesis and disease resistance: activation of cellular stress response pathways. Human and Experimental Toxicology, 27, 155-162.
46. McCay, C.M., Cromwell, M.F. & Maynard, L.A. (1935) The effect of retarded growth upon the length of life span and upon the ultimate body size. Journal of Nutrition, 10, 63-79.
47. Merry, B.J. (1995) Effect of dietary restriction on aging-an update. Reviews in Clinical Gerontology, 5, 247-258.
48. Metcalfe, N.B. & Alonso-Alvarez, C. (2010) Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Functional Ecology, 24, 984-996.
49. Metcalfe, N.B. & Monaghan, P. (2001) Compensation for a bad start: grow now, pay later? Trends in Ecology and Evolution, 16, 254-260.
50. Minois, N. (2000) Longevity and aging: beneficial effects of exposure to mild stress. Biogerontology, 1, 15-29.
51. Monaghan, P. (2008) Early growth conditions, phenotypic development and environmental change. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 363, 1635-1645.
52. Noguera, J.C., Morales, J., Perez, C. & Velando, A. (2010a) On the oxidative cost of begging: antioxidants enhance vocalizations in gull chicks. Behavioral Ecology, 21, 479-484.
53. Noguera, J.C., Alonso-Alvarez, C., Kim, S.Y., Morales, J. & Velando, A. (2011) Yolk testosterone reduces levels of oxidative damages during postnatal development. Biology Letters, 7, 93-95.
54. Nussey, D.H., Pemberton, J.M., Pilkington, J.G. & Blount, J.D. (2009) Life history correlates of oxidative damage in a free-living mammal population. Functional Ecology, 23, 809-817.
55. Ohlsson, T., Smith, H.G., Råberg, L. & Hasselquist, D. (2002) Pheasant sexual ornaments reflect nutritional conditions during early growth. Proceedings of the Royal Society of London B, Biological Science, 269, 21-27.
56. Pérez, C., Lores, M. & Velando, A. (2008) Availability of nonpigmentary antioxidant affects red coloration in gulls. Behavioral Ecology, 19, 967-973.
57. Piper, M.D.W., Mair, W. & Partridge, L. (2005) Counting the calories: the role of specific nutrients in extension of life span by food restriction. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 60, 549-555.
58. Quinn, G.P. & Keough, M.J. (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge.
59. Rietjens, I.M.C.M., Boersma, M.G., de Haan, L., Spenkelink, B., Awad, B., Cnubben, N.H.P., van Zanden, J.J., van der Woude, H., Alink, G.M. & Koeman, J.H. (2002) The pro-oxidant chemistry of the natural antioxidants vitamin C, vitamin E, carotenoids and flavonoids. Environmental Toxicology and Pharmacology, 11, 321-333.
60. Rollo, C.D. (2002) Growth negatively impacts the life span of mammals. Evolution & Development, 4, 55-61.
61. Royle, N.J., Surai, P.F. & Hartley, P.F. (2001) Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behavioral Ecology, 12, 381-385.
62. Rubolini, D., Romano, M., Boncoraglio, G., Ferrari, R.P., Martinelli, R., Galeotti, P., Fasola, M. & Saino, N. (2005) Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks. Hormones and Behavior, 47, 592-605.
63. Sacher, G.A. (1977) Life table modifications and life prolongation. Handbook of the Biology of Aging (eds C.E. Finch & L. Hayflick ). pp. 582-638, Van Nostrand Reinhold, New York, USA.
64. Schulz, T.J., Zarse, K., Voigt, A., Urban, N., Birringer, M. & Ristow, M. (2007) Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metabolism, 6, 280-293.
65. Sohal, R.S. & Weindruch, R. (1996) Oxidative stress, caloric restriction, and aging. Science, 273, 59-63.
66. Sohal, R.S., Agarwal, S., Candas, M., Forster, M.J. & Lal, H. (1994) Effect of age and caloric restriction on DNA oxidative damage in different tissues of C57BL/6 mice. Mechanisms of Ageing and Development, 76, 215-224.
67. Stuart, J.A., Karahalil, B., Hogue, B.A., Souza-Pinto, N.C. & Bohr, V.A. (2004) Mitochondrial and nuclear DNA base excision repair are affected differently by caloric restriction. FASEB Journal, 18, 595-597.
68. Surai, P.F. (2002) Natural Antioxidants in Avian Nutrition and Reproduction. Nottingham University Press, Nottingham.
69. Tavernarakis, N. & Driscoll, M. (2002) Caloric restriction and lifespan: a role for protein turnover? Mechanisms of Ageing and Development, 123, 215-229.
70. Van Remmen, H., Ward, W.F., Sabia, R.V. & Richardson, A. (1995) Gene expression and protein degradation. Handbook of Physiology-Aging (ed. J. Masoro ). pp. 171-234, Oxford University Press, New York.
71. Wells, J.C.K. (2007) The thrifty phenotype as an adaptive maternal effect. Biol Rev Camb Philos Soc, 82, 143-172.
72. West-Eberhard, M.J. (2003) Developmental Plasticity and Evolution. Oxford University Press, New York.
73. Yu, B.P. (1994) How diet influences the aging process of the rat. Proceedings of the Society for Experimental Biology and Medicine, 205, 97-105.
74. Zainal, T.A., Oberley, T.D., Allison, D.B., Szweda, L.I. & Weindruch, R. (2000) Caloric restriction of rhesus monkeys lowers oxidative damage in skeletal muscle. FASEB Journal, 14, 1825-1836.
75. Zera, A.J. & Harshman, l. (2001) The physiology of life history trade-offs in animals. Annual Review of Ecology and Systematics, 32, 95-126.