Effects of immune supplementation and immune challenge on oxidative status and physiology in a model bird: Implications for ecologists

Journal of Experimental Biology

Volumn 213, Issue 20, 2010, Pages 3527-3535

  Van De Crommenacker, Janske ^a   Horrocks, Nicholas P C ^a   Versteegh, Maaike A ^a   Komdeur, Jan ^a   Tieleman, B Irene ^a   Matson, Kevin D ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Antioxidants; Columbiformes; Endotoxin; Haptoglobin; Innate immunity; Lipopolysaccharide; Lysozyme; Metabolic rate; Pigeons; Reactive oxygen species

Indexed keywords

ANTIOXIDANT; LIPOPOLYSACCHARIDE; LYSOZYME; OXIDIZING AGENT; REACTIVE OXYGEN METABOLITE;

ANIMAL; ANIMAL MODEL; ARTICLE; DIET SUPPLEMENTATION; DRUG EFFECT; ENVIRONMENTAL ASPECTS AND RELATED PHENOMENA; FEMALE; IMMUNOLOGY; INFLAMMATION; MALE; METABOLISM; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PATHOLOGY; PHYSIOLOGY; PIGEONS AND DOVES;

ANIMALS; ANTIOXIDANTS; COLUMBIDAE; DIETARY SUPPLEMENTS; ECOLOGICAL AND ENVIRONMENTAL PHENOMENA; FEMALE; INFLAMMATION; LIPOPOLYSACCHARIDES; MALE; MODELS, ANIMAL; MURAMIDASE; OXIDANTS; OXIDATIVE STRESS; OXYGEN CONSUMPTION; REACTIVE OXYGEN SPECIES;

ANIMALIA; AVES; BACTERIA (MICROORGANISMS); COLUMBA; COLUMBA LIVIA; COLUMBIFORMES;

EID: 77957850640     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.045591     Document Type: Article

References (80)

1. Adler, K. L., Peng, P. H., Peng, R. K. and Klasing, K. C. (2001). The kinetics of hemopexin and α1-acid glycoprotein levels induced by injection of inflammatory agents in chickens. Avian Dis. 45 289-296.
2. 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. Intermed. 26, 253-267.
3. 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.
4. Ames, B. N., Shigenaga, M. K. and Hagen, T. M. (1993). Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. USA 90, 7915-7922.
5. Barja, G. (2007). Mitochondrial oxygen consumption and reactive oxygen species production are independently modulated: implications for aging studies. Rejuvination Res. 10 215-224.
6. Beckman, K. B. and Ames, B. N. (1998). The free radical theory of aging matures. Physiol. Rev. 78, 547-581.
7. Bertrand, S., Criscuolo, F., Faivre, B. and Sorci, G. (2006). Immune activation increases susceptibility to oxidative tissue damage in Zebra Finches. Funct. Ecol. 20, 1022-1027.
8. Bond, C. F. and Gilbert, P. W. (1958). Comparative study of blood volume in representative aquatic and nonaquatic birds. Am. J. Physiol. 194, 519-521.
9. Brand, M. D. (2000). Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp. Gerontol. 35, 811-820.
10. Brundige, D. R., Maga, E. A., Klasing, K. C. and Murray, J. D. (2008). Lysozyme transgenic goats' milk influences gastrointestinal morphology in young pigs. J. Nutr. 138 921-926.
11. Calder, W. A. and Schmidt-Nielsen, K. (1967). Temperature regulation and evaporation in the pigeon and the roadrunner. Am. J. Physiol. 213, 883-889.
12. Cerven, D., DeGeorge, G. and Bethell, D. (2008). 28-Day repeated dose oral toxicity of recombinant human apo-lactoferrin or recombinant human lysozyme in rats. Regul. Toxicol. Pharmacol. 51 162-167.
13. 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.
14. Cohen, A. A., Klasing, K. C. and Ricklefs, R. E. (2007). Measuring circulating antioxidants in wild birds. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 147, 110-121.
15. Cohen, A. A., Hau, M. and Wikelski, M. (2008). Stress, metabolism, and antioxidants in two wild passerine bird species. Physiol. Biochem. Zool. 81, 463-472.
16. Cohen, A. A., Mauck, R. A., Wheelwright, N. T., Huntington, C. E. and McGraw, K. J. (2009a). Complexity in relationships between antioxidants and individual life-history parameters in a seabird and a songbird. Oikos 118, 1854-1861.
17. Cohen, A. A., McGraw, K. J. and Robinson, W. D. (2009b). Serum antioxidant levels in wild birds vary in relation to diet, season, life history strategy, and species. Oecologia 161, 673-683.
18. Costantini, D. (2008). Oxidative stress in ecology and evolution: lessons from avian studies. Ecol. Lett. 11, 1238-1251.
19. Costantini, D. and Dell'Omo, G. (2006). Effects of T-cell-mediated immune response on avian oxidative stress. Comp. Biochem. Physiol. A Physiol. 145, 137-142.
20. Costantini, D. and Møller, A. P. (2009). Does immune response cause oxidative stress in birds? A meta-analysis. Comp. Biochem. Physiol. A Physiol. 153, 339-344.
21. Costantini, D. and Verhulst, S. (2009). Does high antioxidant capacity indicate low oxidative stress? Funct. Ecol. 23, 506-509.
22. Costantini, D., Coluzza, C., Fanfani, A. and Dell'Omo, G. (2007). Effects of carotenoid supplementation on colour expression, oxidative stress and body mass in rehabilitated captive adult kestrels (Falco tinnunculus). J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 177, 723-731.
23. Costantini, D., Dell'Ariccia, G. and Lipp, H. P. (2008). Long flights and age affect oxidative status of homing pigeons (Columba livia). J. Exp. Biol. 211, 377-381.
24. Delers, F., Strecker, G. and Engler, R. (1988). Glycosylation of chicken haptoglobin: isolation and characterization of three molecular variants and studies of their distribution in hen plasma before and after turpentine-induced inflammation. Biochem. Cell Biol. 66, 208-217.
25. Demas, G. E., Chefer, V., Talan, M. I. and Nelson, R. J. (1997). Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice. Am. J. Physiol. 273 R1631-R1637. (Pubitemid 27518112)
26. Dobryszycka, W. (1997). Biological functions of haptoglobin-new pieces to an old puzzle. Eur. J. Clin. Chem. Clin. Biochem. 35, 647-654.
27. Dowling, D. K. and Simmons, L. W. (2009). Reactive oxygen species as universal constraints in life-history evolution. Proc. R. Soc. Lond. B. Biol. Sci. 276 1737-1745.
28. Exton, M. S. (1997). Infection-induced anorexia: active host defence strategy. Appetite 29, 369-383.
29. Finkel, T. and Holbrook, N. J. (2000). Oxidants, oxidative stress and the biology of ageing. Nature 408, 239-247.
30. Gavilanes, J. G. (1982). Pigeon egg white lysozyme. Int. J. Pept. Prot. Res. 20, 238-245.
31. Gessaman, J. A. (1987). Energetics. In Raptor Management Techniques Manual (ed. G. A. Giron Pendeleton, B. A. Millsap, K. W. Cline and D. M. Bird), pp. 289-320. Washington, DC: National Wildlife Federation.
32. Gutteridge, J. M. C. (1987). The antioxidant activity of haptoglobin towards haemoglobin-stimulated lipid peroxidation. Biochim. Biophys. Acta 917, 219-223.
33. Halliwell, B. and Gutteridge, J. M. C. (1985). Oxygen radicals and the nervous system. Trends Neurosci. 8, 22-26.
34. Halliwell, B. and Gutteridge, J. M. C. (1999) Free Radicals in Biology and Medicine. Oxford: Oxford University Press.
35. Hansen, N. E., Karle, H. and Andersen, V. (1971). Lysozyme turnover in the rat. J. Clin. Invest. 50, 1473-1477.
36. Hansen, N. E., Karle, H., Andersen, V. and Olgaard, K. (1972). Lysozyme turnover in man. J. Clin. Invest. 51, 1146-1155.
37. Herrero, A. and Barja, G. (1998). H2O2 production of heart mitochondria and aging rate are slower in canaries and parakeets than in mice: sites of free radical generation and mechanisms involved. Mech. Ageing Dev. 103, 133-146.
38. Hill, R. W. (1972). Determination of oxygen consumption by use of the paramagnetic oxygen analyzer. J. Appl. Physiol. 33, 261-263.
39. Hõrak, P., Zilmer, M., Saks, L., Ots, I., Karu, U. and Zilmer, K. (2006). Antioxidant protection, carotenoids and the costs of immune challenge in greenfinches. J. Exp. Biol. 209 4329-4338.
40. Hõrak, P., Saks, L., Zilmer, M., Karu, U. and Zilmer, K. (2007). Do dietary antioxidants alleviate the cost of immune activation? An experiment with greenfinches. Am. Nat. 170 625-635.
41. Humphrey, B. D., Huang, N. and Klasing, K. C. (2002). Rice expressing lactoferrin and lysozyme has antibiotic-like properties when fed to chicks. J. Nutr. 132, 1214-1218.
42. Iamele, L., Fiocchi, R. and Vernocchi, A. (2002). Evaluation of an automated spectrophotometric assay for reactive oxygen metabolites in serum. Clin. Chem. Lab. Med. 40 673-676.
43. Ji, L. L. (1999). Antioxidants and oxidative stress in exercise. Exp. Biol. Med. 222, 283-292.
44. Jolles, P. and Jollès, J. (1984). What's new in lysozyme research? Mol. Cell. Biochem. 63, 165-189.
45. Klebanoff, S. J. and Clark, R. A. (1978) The Neutrophil: Function and Clinical Disorders. Amsterdam: Holland Publishing Company.
46. Klockars, M. and Roberts, P. (1976). Stimulation of phagocytosis by human lysozyme. Acta Haematol. 55, 289-295.
47. Körmöczi, G. F., Säemann, M. D., Buchta, C., Peck-Radosavljevic, M., Mayr, W. R., Schwartz, D. W. M., Dunkler, D., Spitzauer, S. and Panzer, S. (2006). Influence of clinical factors on the haemolysis marker haptoglobin. Eur. J. Clin. Invest. 36, 202-209.
48. Lasiewski, R. C., Acosta, A. L. and Bernstein, M. H. (1966). Evaporative water loss in birds-I. Characteristics of the open flow method of determination, and their relation to estimates of thermoregulatory ability. Comp. Biochem. Physiol. 19, 445-457.
49. Lavoie, E. T. (2005). Avian immunosenescence. Age 27 281-285.
50. Lee, K. A. (2006). Linking immune defenses and life history at the levels of the individual and the species. Integr. Comp. Biol. 46, 1000-1015.
51. Leeuwenburgh, C. and Heinecke, J. W. (2001). Oxidative stress and antioxidants in exercise. Curr. Med. Chem. 8, 829-838.
52. Liu, H., Zheng, F., Cao, Q., Ren, B., Zhu, L., Striker, G. and Vlassara, H. (2006). Amelioration of oxidant stress by the defensin lysozyme. Am. J. Physiol. 290, E824-E832.
53. Matson, K. D. (2006). Are there differences in immune function between continental and insular birds? Proc. R. Soc. Lond. B. Biol. Sci. 273, 2267-2274.
54. Matson, K. D., Ricklefs, R. E. and Klasing, K. C. (2005). A hemolysis-hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev. Comp. Immunol. 29 275-286.
55. Matson, K. D., Cohen, A. A., Klasing, K. C., Ricklefs, R. E. and Scheuerlein, A. (2006). No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl. Proc. R. Soc. Lond. B. Biol. Sci. 273, 815-822.
56. McEwen, B. S. (1998). Protective and damaging effects of stress mediators. N. Engl. J. Med. 338, 171-179.
57. Millet, S., Bennett, J., Lee, K. A., Hau, M. and Klasing, K. C. (2007). Quantifying and comparing constitutive immunity across avian species. Dev. Comp. Immunol. 31 188-201.
58. 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.
59. Nomoto, S. (1996). Diurnal variations in fever induced by intravenous LPS injection in pigeons. Pflügers Arch. Eur. J. Physiol. 431, 987-989.
60. Norris, K. and Evans, M. R. (2000). Ecological immunology: life history trade-offs and immune defense in birds. Behav. Ecol. 11, 19-26.
61. Ohno, N. and Morrison, D. C. (1989). Lipopolysaccharide interaction with lysozyme. Binding of lipopolysaccharide to lysozyme and inhibition of lysozyme enzymatic activity. J. Biol. Chem. 264 4434-4441.
62. Ots, I., Kerimov, A. B., Ivankina, E. V., Ilyina, T. A. and Horak, P. (2001). Immune challenge affects basal metabolic activity in wintering great tits. Proc. R. Soc. Lond. B. Biol. Sci. 268 1175-1181.
63. Pérez-Rodriguez, L., Mougeot, F., Alonso-Alvarez, C Blas, J., Vinuela, J. and Bortolotti, G. R. (2008). Cell-mediated immune activation rapidly decreases plasma carotenoids but does not affect oxidative stress in red-legged partridges (Alectorisrufa). J. Exp. Biol. 211, 2155-2161.
64. Räberg, L., Grahn, M., Hasselquist, D. and Svensson, E. (1998). On the adaptive significance of stress-induced immunosuppression. Proc. R. Soc. Lond. B. Biol. Sci. 265, 1637-1641.
65. Raetz, C. R. H. (1990). Biochemistry of endotoxins. Annu. Rev. Biochem. 59, 129-170.
66. Rasbash, J., Steele, F., Browne, W. and Prosser, B. (2004). A User's Guide to Mlwin Version 2.0. London: Institute of Education.
67. Rodnan, G. P., Ebaugh, F. G., Jr, Fox, M. R. S. and Chambers, D. M. (1957). The life span of the red blood cell and the red blood cell volume in the chicken, pigeon and duck as estimated by the use of Na2Cr51O4: with observations on red cell turnover rate in the mammal, bird and reptile. Blood 12, 355-366.
68. Roura, E., Homedes, J. and Klasing, K. C. (1992). Prevention of immunologic stress contributes to the growth-permitting ability of dietary antibiotics in chicks. J. Nutr. 122 2383-2390.
69. Saino, N., Calza, S. and Møller, A. P. (1998). Effects of a dipteran ectoparasite on immune response and growth trade-offs in barn swallow, Hirundo rustica, nestlings. Oikos 81, 217-228.
70. Saino, N., Dall'Ara, P., Martinelli, R. and Møller, A. P. (2002). Early maternal effects and antibacterial immune factors in the eggs, nestlings and adults of the barn swallow. J. Evol. Biol. 15 735-743.
71. Salvante, K. G. (2006). Techniques for studying integrated immune function in birds. Auk 123, 575-586.
72. Sava, G. (1996). Pharmacological aspects and therapeutic applications of lysozymes Lysozymes: Model Enzymes in Biochemistry and Biology (ed. P. Jollès), pp. 433-449. Basel: Birkhauser Verlag.
73. Siwicki, A. K., Klein, P., Morand, M., Kiczka, W. and Studnicka, M. (1998). Immunostimulatory effects of dimerized lysozyme (KLP-602) on the nonspecific defense mechanisms and protection against furunculosis in salmonids. Vet. Immunol. Immunopathol. 61, 369-378.
74. Speakman, J. R., Talbot, D. A., Selman, C., Snart, S., McLaren, J. S., Redman, P., Krol, E., Jackson, D. M., Johnson, M. S. and Brand, M. D. (2004). Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3 87-95.
75. Speijers, G. J. A. and Van Apeldoorn, M. M. E. (1998). Lysozyme. In Clinical Safety Information. IPCS Inchem. Bilthoven, The Netherlands: Laboratory for Toxicology.
76. Tieleman, B. I., Williams, J. B., Ricklefs, R. E. and Klasing, K. C. (2005). Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proc. R. Soc. Lond. B. Biol. Sci. 272 1715-1720.
77. Tieleman, B. I., Versteegh, M. A., Fries, A., Helm, B., Dingemanse, N. J., Gibbs, H. L. and Williams, J. B. (2009). Genetic modulation of energy metabolism in birds through mitochondrial function. Proc. R. Soc. Lond. B. Biol. Sci. 276, 1685-1693.
78. Torres, R. and Velando, A. (2007). Male reproductive senescence: the price of immune-induced oxidative damage on sexual attractiveness in the blue-footed booby. J. Anim. Ecol. 76 1161-1168.
79. Tummeleht, L., Mägi, M., Kilgas, P., Mänd, R. and Hõrak, P. (2006). Antioxidant protection and plasma carotenoids of incubating great tits (Parus major L.) in relation to health state and breeding conditions. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 144, 166-172.
80. Wagner, L., Gessl, A., Parzer, S. B., Base, W., Waldhausl, W. and Pasternack, M. S. (1996). Haptoglobin phenotyping by newly developed monoclonal antibodies. Demonstration of haptoglobin uptake into peripheral blood neutrophils and monocytes. J. Immunol. 156, 1989-1996.