Loss of integration is associated with reduced resistance to oxidative stress

Journal of Experimental Biology

Volumn 216, Issue 12, 2013, Pages 2213-2220

  Costantini, David ^a   Monaghan, Pat ^a   Metcalfe, Neil B ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Antioxidants; Birds; Flight effort; Oxidative damage; Vertebrates

Indexed keywords

ANTIOXIDANT; REACTIVE OXYGEN METABOLITE;

ANIMAL; ANIMAL EXPERIMENT; ARTICLE; BIRD; BLOOD; FEMALE; FLIGHT EFFORT; FLYING; HORMESIS; MALE; METABOLISM; OXIDATION REDUCTION REACTION; OXIDATIVE DAMAGE; OXIDATIVE STRESS; PHYSIOLOGY; RANDOMIZATION; SONGBIRD; VERTEBRATE;

ANTIOXIDANTS; BIRDS; FLIGHT EFFORT; OXIDATIVE DAMAGE; VERTEBRATES;

ANIMALS; ANTIOXIDANTS; FEMALE; FLIGHT, ANIMAL; HORMESIS; MALE; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHYSICAL CONDITIONING, ANIMAL; RANDOM ALLOCATION; REACTIVE OXYGEN SPECIES; SONGBIRDS;

AVES; TAENIOPYGIA GUTTATA; VERTEBRATA;

EID: 84878535571     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.083154     Document Type: Article

References (68)

1. Alberti, A., Bolognini, L., Macciantelli, D. and Caratelli, M. (2000). The radical cation of N,N-diethyl-para-phenylendiamine: a possible indicator of oxidative stress in biological samples. Res. Chem. Intermediat. 26, 253-267.
2. Alonso-Alvarez, C., Bertrand, S., Devevey, G., Gaillard, M., Prost, J., Faivre, B. and Sorci, G. (2004). An experimental test of the dose dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am. Nat. 164, 651-659.
3. Bauchinger, U., Keil, J., McKinney, R. A., Starck, J. M. and McWilliams, S. R. (2010). Exposure to cold but not exercise increases carbon turnover rates in specific tissues of a passerine. J. Exp. Biol. 213, 526-534.
4. Bordel, R. and Haase, E. (1993). Effects of flight on blood parameters in homing pigeons. J. Comp. Physiol. B 163, 219-224.
5. Bordel, R. and Haase, E. (2000). Influence of flight on protein catabolism, especially myofilament breakdown, in homing pigeons. J. Comp. Physiol. B 170, 51-58.
6. Buonocore, G., Perrone, S., Longini, M., Terzuoli, L. and Bracci, R. (2000). Total hydroperoxide and advanced oxidation protein products in preterm hypoxic babies. Pediatr. Res. 47, 221-224.
7. Cao, G. and Cutler, R. G. (1995). Protein oxidation and aging. I. Difficulties in measuring reactive protein carbonyls in tissues using 2,4-dinitrophenylhydrazine. Arch. Biochem. Biophys. 320, 106-114.
8. Cheverud, J. M. (1996). Developmental integration and the evolution of pleiotropy. Am. Zool. 36, 44-50.
9. Cohen, A. A. and McGraw, K. J. (2009). No simple measures for antioxidant status in birds: complexity in inter- and intraspecific correlations among circulating antioxidant types. Funct. Ecol. 23, 310-320.
10. Cohen, A. A., Martin, L. B., Wingfield, J. C., McWilliams, S. R. and Dunne, J. A. (2012). Physiological regulatory networks: ecological roles and evolutionary constraints. Trends Ecol. Evol. 27, 428-435.
11. Costantini, D. (2008). Oxidative stress in ecology and evolution: lessons from avian studies. Ecol. Lett. 11, 1238-1251.
12. Costantini, D. and Verhulst, S. (2009). Does high antioxidant capacity indicate low oxidative stress? Funct. Ecol. 23, 506-509.
13. Costantini, D., Metcalfe, N. B. and Monaghan, P. (2010). Ecological processes in a hormetic framework. Ecol. Lett. 13, 1435-1447.
14. Costantini, D., Monaghan, P. and Metcalfe, N. B. (2011). Biochemical integration of blood redox state in captive zebra finches (Taeniopygia guttata). J. Exp. Biol. 214, 1148-1152.
15. Costantini, D., Mirzai, N. and Metcalfe, N. (2012). An automated system to control and manipulate the flight activity of captive birds. Behav. Ecol. Sociobiol. 66, 1195-1199.
16. Csermely, P. and Soti, C. (2006). Cellular networks and the aging process. Arch. Physiol. Biochem. 112, 60-64.
17. Dotan, Y., Lichtenberg, D. and Pinchuk, I. (2004). Lipid peroxidation cannot be used as a universal criterion of oxidative stress. Prog. Lipid Res. 43, 200-227.
18. Dröge, W. (2002). Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95.
19. Ellman, G. L. (1959). Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82, 70-77.
20. Giuliani, A., Zbilut, J. P., Conti, F., Manetti, C. and Miccheli, A. (2004). Invariant features of metabolic networks: a data analysis application on scaling properties of biochemical pathways. Physica A 337, 157-170.
21. Haber, A. (2011). A comparative analysis of integration indices. Evol. Biol. 38, 476-488.
22. Halliwell, B. H. and Gutteridge, J. M. C. (2007). Free Radicals in Biology and Medicine, 4th edn. Oxford: Oxford University Press.
23. Hammer, Ø., Harper, D. A. T. and Ryan, P. D. (2001). PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol. Electron. 4, http://palaeo-electronica.org/2001-1/past/issue1-01. htm.
24. Hartwell, L. H., Hopfield, J. J., Leibler, S. and Murray, A. W. (1999). From molecular to modular cell biology. Nature 402 Suppl., C47-C52.
25. Iqbal, M., Probert, L. L., Alhumadi, N. H. and Klandorf, H. (1999). Protein glycosylation and advanced glycosylated endproducts (AGEs) accumulation: an avian solution? J. Gerontol. A Biol. Sci. Med. Sci. 54, B171-B176, discussion B177-B178.
26. Jenni, L., Jenni-Eiermann, S. J., Spina, F. and Schwabl, H. (2000). Regulation of protein breakdown and adrenocortical response to stress in birds during migratory flight. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278, R1182-R1189.
27. Jones, D. P. (2006). Redefining oxidative stress. Antioxid. Redox Signal. 8, 1865-1879.
28. Kirkwood, T. B. (2005). Understanding the odd science of aging. Cell 120, 437-447.
29. Klandorf, H., Probert, L. L. and Iqbal, M. (1999). In the defense against hyperglycaemia: an avian strategy. World's Poult. Sci. J. 55, 251-268.
30. Klingenberg, C. P. (2007). Analyzing modularity in complex morphological structures. J. Morphol. 268, 1094.
31. Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annu. Rev. Ecol. Evol. Syst. 39, 115-132.
32. Lajtha, A., Tettamanti, G. and Goracci, G. (2009). Handbook of Neurochemistry and Molecular Neurobiology. Neural Lipids, 3rd edn. New York: Springer Science.
33. Larcombe, S. D., Coffey, J. S., Bann, D., Alexander, L. and Arnold, K. E. (2010). Impacts of dietary antioxidants and flight training on post-exercise oxidative damage in adult parrots. Comp. Biochem. Physiol. 155B, 49-53.
34. Lessells, C. M. and 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. and Stadtman, E. R. (1990). Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 186, 464-478.
36. Mattson, M. P. and Calabrese, E. J. (2010). Hormesis: a Revolution in Biology, Toxicology and Medicine. New York/London: Springer.
37. McWilliams, S. R., Guglielmo, C., Pierce, B. and Klaassen, M. (2004). Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J. Avian Biol. 35, 377-393.
38. Mitteroecker, P. and Bookstein, F. (2007). The conceptual and statistical relationship between modularity and morphological integration. Syst. Biol. 56, 818-836.
39. Monaghan, P., Metcalfe, N. B. and Torres, R. (2009). Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 12, 75-92.
40. 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.
41. Nikolaidis, M. G., Kyparos, A., Spanou, C., Paschalis, V., Theodorou, A. A. and Vrabas, I. S. (2012). Redox biology of exercise: an integrative and comparative consideration of some overlooked issues. J. Exp. Biol. 215, 1615-1625.
42. Nudds, R. L. and Bryant, D. M. (2000). The energetic cost of short flights in birds. J. Exp. Biol. 203, 1561-1572.
43. Nudds, R. L. and Bryant, D. M. (2001). Exercise training lowers the resting metabolic rate of zebra finches, Taeniopygia guttata. Funct. Ecol. 15, 458-464.
44. Paglia, D. E. and Valentine, W. N. (1967). Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 70, 158-169.
45. Pamplona, R. and Costantini, D. (2011). Molecular and structural antioxidant defences against oxidative stress in animals. Am. J. Physiol. 301, R843-R863.
46. Papin, J. A., Reed, J. L. and Palsson, B. O. (2004). Hierarchical thinking in network biology: the unbiased modularization of biochemical networks. Trends Biochem. Sci. 29, 641-647.
47. Parter, M., Kashtan, N. and Alon, U. (2007). Environmental variability and modularity of bacterial metabolic networks. BMC Evol. Biol. 7, 169.
48. Pavlicev, M., Cheverud, J. M. and Wagner, G. P. (2009). Measuring morphological integration using eigenvalue variance. Evol. Biol. 36, 157-170.
49. R Development Core Team (2012). R: A Language and Environment for Statistical Computing. Version 2.15.0. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://www.R-project.org/.
50. Radak, Z., Chung, H. Y., Koltai, E., Taylor, A. W. and Goto, S. (2008). Exercise, oxidative stress and hormesis. Ageing Res. Rev. 7, 34-42.
51. Ravasz, E., Somera, A. L., Mongru, D. A., Oltvai, Z. N. and Barabási, A. L. (2002). Hierarchical organization of modularity in metabolic networks. Science 297, 1551-1555.
52. Ricklefs, R. E. and Wikelski, M. (2002). The physiology-life history nexus. Trends Ecol. Evol. 17, 462-468.
53. Ristow, M., Zarse, K., Oberbach, A., Klöting, N., Birringer, M., Kiehntopf, M., Stumvoll, M., Kahn, C. R. and Blüher, M. (2009). Antioxidants prevent health-promoting effects of physical exercise in humans. Proc. Natl. Acad. Sci. USA 106, 8665-8670.
54. Romero, L. M. (2004). Physiological stress in ecology: lessons from biomedical research. Trends Ecol. Evol. 19, 249-255.
55. Schlosser, G. and Wagner, G. P. (2004). Modularity in Development and Evolution. Chicago: University of Chicago Press.
56. Schwilch, R., Jenni, L. and Jenni-Eiermann, S. J. (1996). Metabolic responses of homing pigeons to flight and subsequent recovery. J. Comp. Physiol. 166B, 77-87.
57. Sepp, T., Sild, E., Blount, J. D., Männiste, M., Karu, U. and Hõrak, P. (2012). Individual consistency and covariation of measures of oxidative status in greenfinches. Physiol. Biochem. Zool. 85, 299-307.
58. Sies, H. (1991). Oxidative Stress II. Oxidants and Antioxidants. London: Academic Press.
59. Sohal, R. S. and Orr, W. C. (2012). The redox stress hypothesis of aging. Free Radic. Biol. Med. 52, 539-555.
60. Soltow, Q. A., Jones, D. P. and Promislow, D. E. L. (2010). A network perspective on metabolism and aging. Integr. Comp. Biol. 50, 844-854.
61. Southam, C. M. and Ehrlich, J. (1943). Effects of extracts of western red cedar heartwood on certain wood-decaying fungi in culture. Phytopathology 33, 517-524.
62. Southworth, L. K., Owen, A. B. and Kim, S. K. (2009). Aging mice show a decreasing correlation of gene expression within genetic modules. PLoS Genet. 5, e1000776.
63. Surai, P. (2002). Natural Antioxidants in Avian Nutrition and Reproduction. Nottingham, UK: Nottingham University Press.
64. Tsahar, E., Arad, Z., Izhaki, I. and Guglielmo, C. G. (2006). The relationship between uric acid and its oxidative product allantoin: a potential indicator for the evaluation of oxidative stress in birds. J. Comp. Physiol. B 176, 653-661.
65. Tun, K., Dhar, P. K., Palumbo, M. C. and Giuliani, A. (2006). Metabolic pathways variability and sequence/networks comparisons. BMC Bioinformatics 7, 24.
66. Weinert, B. T. and Timiras, P. S. (2003). Invited review: Theories of aging. J. Appl. Physiol. 95, 1706-1716.
67. Wiersma, P., Selman, C., Speakman, J. R. and Verhulst, S. (2004). Birds sacrifice oxidative protection for reproduction. Proc. Biol. Sci. 271 Suppl., S360-S363.
68. Woolliams, J. A., Wiener, G., Anderson, P. H. and McMurray, C. H. (1983). Variation in the activities of glutathione peroxidase and superoxide dismutase and in the concentration of copper in the blood in various breed crosses of sheep. Res. Vet. Sci. 34, 253-256.