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Modulation of nutrient metabolism and homeostasis by the immune system

Published online by Cambridge University Press:  18 September 2007

B.D. Humphrey  and
K.C. Klasing
B.D. Humphrey
Affiliation:
Department of Animal Science, University of California, 1 Shields Ave., Davis, CA, USA
K.C. Klasing*
Affiliation:
Department of Animal Science, University of California, 1 Shields Ave., Davis, CA, USA
*
*Corresponding author: e-mail: kcklasing@ucdavis.edu
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Abstract

Interactions between nutrition and immunity are diverse and have profound implications on animal growth and productivity. The innate immune system provides protection during the initial stages of infection and is responsible for mediating many of the alterations in nutrient metabolism. The macrophage is the key sensory and regulatory cell of the innate immune system. Their pro-inflammatory cytokines coordinate local immunity to pathogens, yet also act systemically to alter metabolic homeostasis and decrease food intake and growth rate. Altered energy, amino acid, lipid, and mineral metabolism have nutritionally important implications. For example, an innate immune response results in decreased uptake of amino acids by skeletal muscles and a corresponding increase in uptake by the liver and to a lesser extent by leukocytes. The net result is a decrease in amino acid requirements with no change in the efficiency of their use for growth. The shift in the priority of individual tissues for nutrients appears to be accomplished by changes in the types and amounts of their nutrient transporters and storage proteins. Adaptive immune responses result in considerably more subtle changes in nutrient metabolism than innate responses.

Keywords

chickencytokineinfectioninterleukin-1leukocytemacrophagemetabolism
Type
Reviews
Information
World's Poultry Science Journal , Volume 60 , Issue 1 , March 2004 , pp. 90 - 100
Copyright
Copyright © Cambridge University Press 2004

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Footnotes

This paper was first presented at the 14th European Symposium on Poultry Nutrition, Lillehammer, Norway, August 10–14, 2003

References

Barber, E.F. and Cousins, R.J. (1988) Interleukin-1—stimulated induction of cerulop;asmin synthesis in normal and copper-deficient rats. Journal of Nutrition 118: 375–381.CrossRefGoogle Scholar
Barnes, D.M., Song, Z., Klasing, K.C. and Bottje, W. (2002) Protein metabolism during an acute phase response in chickens. Amino Acids (Vienna) 22: 15–26.CrossRefGoogle ScholarPubMed
Beisel, W.R. (1977) Magnitude of the host nutritional responses to infection. American Journal of Clinical Nutrition 30: 1236–1247.Google ScholarPubMed
Benson, B.N., Calvert, C.C., Roura, E. and Klasing, K.C. (1993) Dietary energy source and density modulate the expression of immunologic stress in chicks. Journal of Nutrition 123: 1714–1723.CrossRefGoogle ScholarPubMed
Boyd, Y., Goodchild, M., Morroll, S. and Bumstead, N. (2001) Mapping of the chicken and mouse genes for toll-like receptor 2 (TLR2) to an evolutionarily conserved chromosomal segment. lmmunogenetics 52: 294–298.CrossRefGoogle Scholar
Butterwith, S.C. and Griffin, H.D. (1989) The effects of macrophage-derived cytokines on lipid metabolism in chicken (Gallus domesticus) hepatocytes and adipocytes. Comp Biochem Physiol A 94: 721–724.CrossRefGoogle ScholarPubMed
Cohn, M. and Langman, R. (1996) The Immune System: A Look From a Distance. Frontiers in Bioscience 1: d318–323.CrossRefGoogle ScholarPubMed
Cook, M.E. (1991) Nutrition and the immune response of the domestic fowl. Crit. Rev. Poultry Biol. 3: 167–189.Google Scholar
Dil, N. and Qureshi, M.A. (2002a) Differential expression of inducible nitric oxide synthase is associated with differential Toll-like receptor-4 expression in chicken macrophages from different genetic backgrounds. Veterinary Immunology and Immonopathology 84: 191–207.CrossRefGoogle ScholarPubMed
Dil, N. and Qureshi, M.A. (2002b) Involvement of lipopolysaccharide related receptors and nuclear factor kappa B in differential expression of inducible nitric oxide synthase in chicken macrophages from different genetic backgrounds. Veterinary Immunology and Immonopathology 88: 149–161.CrossRefGoogle ScholarPubMed
Elsasser, T.H., Klasing, K.C., Filipov, N. and Thompson, F. (2000) The metabolic consequences of stress: Targets for stress and priorities for nutrient use. Pages 77–110 in: The Biology of Animal Stress. Moberg, G. P. and Mench, J. A., eds. CAB International Press, New York.Google Scholar
Farnell, M.B., Crippen, T.L., He, H., Swaggerty, C.L. and Kogut, M.H. (2003) Oxidative burst mediated by toll like receptors (TLR) and CD14 on avian heterophils stimulated with bacterial toll agonists. Developmental & Comparative Immunology 27: 423–429.CrossRefGoogle ScholarPubMed
Fukui, A., Inoue, N., Matsumoto, M., Nomura, M., Yamada, K., Matsuda, Y., Toyoshima, K. and Seya, T. (2001) Molecular cloning and functional characterization of chicken toll-like receptors. A single chicken toll covers multiple molecular patterns. Journal of Biological Chemistry 276: 47143–47149.CrossRefGoogle ScholarPubMed
Gehad, A.E., Lillehoj, H.S., Hendricks 3Rd, G.L. and Mashaly, M.M. (2002) Initiation of humoral immunity. I. The role of cytokines and hormones in the initiation of humoral immunity using T-independent and T-dependent antigens. Developmental & Comparative Immunology 26: 751–759.CrossRefGoogle ScholarPubMed
Griffin, H.D. and Butterwith, S.C. (1988) Effect of Escherichia coli endotoxin on tissue lipoprotein lipase activities in chickens. British Poultry Science 29: 371–378.CrossRefGoogle ScholarPubMed
Guida, S., Heguy, A. and Melli, M. (1992) The chicken IL-l receptor: differential evolution of the cytoplasmic and extracellular domains. Gene 111: 239–243.CrossRefGoogle Scholar
Hammond, J. (1944) Physiological factors affecting birth weight. Proceedings of the Nutrition Society 2: 8–12.Google Scholar
Hentges, E.J., Marple, D.N., Roland, D.A. Sr. and Pritchett, J.F. (1984) Muscle protein synthesis and growth of two strains of chicks vaccinated for Newcastle disease and infectious bronchitis. Poultry Science 63: 1738–1741.CrossRefGoogle ScholarPubMed
Humphrey, B.D., Koutsos, E.A. and Klasing, K.C. (2002) Requirements and priorities of the immune system for nutrients. Pages 69–77 in: Nutrition biotechnology in the feed and food industries: Proceedings of Alltech's 18th annual symposium.Lyons, .T.P. and Jasques, K.A., eds. Nottingham University PressNottingham, UK.Google Scholar
Humphrey, B.D., Stephensen, C., Calvert, C.C. and Klasing, K.C. (2003) Effect of the acute phase response on cationic amino acid transporter (CAT) expression in lysine deficient chicks. The FASEB Journal A1122.Google Scholar
Johnson, A.L., Bridgham, J.T., Munks, M. and Witty, J.P. (1998) Characterization of the chicken interleukin-lbeta converting enzyme (caspase-I) cDNA and expression of caspase-l mRNA in the hen. Gene 219: 55–62.CrossRefGoogle Scholar
Johnson, R.W., Curtis, S.E., Dantzer, R. and Kelley, K.W. (1993) Central and peripheral prostaglandins are involved in sickness behavior in birds. Physiology & Behavior 53: 127–131.CrossRefGoogle ScholarPubMed
Kadis, S., Udeze, F.A., Polanco, J. and Dreesen, D.W. (1984) Relationship of iron administration to susceptibility of newborn pigs to enterotoxic colibacillosis. American Journal of Veterinary Research 45: 255–259.Google ScholarPubMed
Klasing, K.C. (1984) Effect of inflammatory agents and interleukin I on iron and zinc metabolism. American Journal of Physiology 247: R901–904.Google ScholarPubMed
Klasing, K.C. (1988) Nutritional Aspects of Leukocytic Cytokines. Journal of Nutrition 118: 1436–1446.CrossRefGoogle ScholarPubMed
Klasing, K.C. (1998) Avian macrophages: regulators of local and systemic immune responses. Poultry Science 77: 983–989.CrossRefGoogle ScholarPubMed
Klasing, K.C. (1999) Interleukin-1 contributes to the acute phase response in growing quail challenged with Salmonella typhimurium lipopolysaccharide. Poultry Science 78: 104.Google Scholar
Klasing, K.C. and Austic, R.E. (1984a) Changes in protein degradation in chickens due to an inflammatory challenge. Proceedings of the Socity for Experimental Biology and Medicine 176: 292–296.CrossRefGoogle Scholar
Klasing, K.C. and Austic, R.E. (1984b) Changes in protein synthesis due to an inflammatory challenge. Proceedings of the Society for Experimenial Biology & Medicine 176: 285–291.CrossRefGoogle Scholar
Klasing, K.C. and Barnes, D.M. (1988) Decreased Amino Acid Requirements of Growing Chicks Due to lmmunologic Stress. Journal of Nutrition 118: 1158–1164.CrossRefGoogle ScholarPubMed
Klasing, K.C. and Calvert, C.C. (1999) The care and feeding of an immune system: an analysis of lysine needs. Pages 253–264 in: Prorein Merabolism and Nurrition. Lobley, G.E., White, A., and Macrae, , eds. Wageningen Pres.Google Scholar
Klasing, K.C., Laurin, D.E., Peng, R.K. and Fry, M. (1987) Immunologically Mediated Growth Depression in Chicks: Influence of Feed Intake, Corticosterone and Interleukin-1. Journal of Nutrition 117: 1629–1637.CrossRefGoogle ScholarPubMed
Klasing, K.C. and Peng, R.K. (2001) Soluble type-I interleukin-1 receptor blocks chicken IL-l activity. Developmental & Comparative lmmunology 25: 345–352.CrossRefGoogle Scholar
Knight, C.D., Klasing, K.C. and Forsyth, D.M. (1983) E. coli growth in serum of iron dextran-supplement pigs. Journal of Animal Science 57: 387–395.CrossRefGoogle ScholarPubMed
Koh, T.S., Peng, R.K. and Klasing, K.C. (1996) Dietary copper level affects copper metabolism during lipopolysaccharide-induced immunological stress in chicks. Poultry Science 75: 867–872.CrossRefGoogle ScholarPubMed
Koutsos, E.A. and Klasing, K.C. (2001) Interactions between the immune system, nutrition, and productivity of animals. Pages 173–190 in: Recent Advances in Animal Nutrition, 2001. Garnsworthy, P. C. and Wiseman, J., eds. Nottingham University Press, Nottingham.Google Scholar
Laurin, D.E. and Klasing, K.C. (1987) Effects of repetitive immunogen injections and fasting versus feeding on iron, zinc, and copper metabolism in chicks. Biology of Trace Element Research 14: 153–165.CrossRefGoogle ScholarPubMed
Leshchinsky, T.V. and Klasing, K.C. (2001) Divergence of the inflammatory response in two types of chickens. Developmental & Comparative Immunology 25: 629–638.CrossRefGoogle ScholarPubMed
Leutz, A., Damm, K.,Sterneck, E., Kowenz, E., Ness, S.,Frank, R., Gausepohl, H., Pan, Y.C., Smart, J. and Hayman, M. (1989) Molecular cloning of the chicken myelomonocytic growth factor (cMGF) reveals relationship to interleukin 6 and granulocyte colony stimulating factor. European Molecular Biology Organization Journal 8: 175–181.CrossRefGoogle ScholarPubMed
Leveque, G., Forgetta, V., Morroll, S., Smith, A.L., Bumstead, N., Barrow., P., Loredo-Osti, J.C., Morgan, K. and Malo, D. (2003) Allelic variation in TLR4 is linked to susceptibility to Salmonella enterica serovar Sphimurium infection in chickens. Infecr lmmun 71: 1116–1124.CrossRefGoogle ScholarPubMed
Martin, A., Dunnington, E.A., Gross, W.B., Briles, W.E., Briles, R.W. and Siegel, P.B. (1990) Production traits and alloantigen systems in lines of chickens selected for high or low antibody responses to sheep erythrocytes. Poultry Science 69: 871–878.CrossRefGoogle ScholarPubMed
Oprea, M., Van Nimwegen, E. and Perelson, A.S. (2000) Dynamics of one-pass germinal center models: implications for affinity maturation. Bull Math Biology 62: 121–153.CrossRefGoogle ScholarPubMed
Parmentier, H.K., Bronkhorst, S., Nieuwland, M.G., De Reilingh, G.V., Van Der Linden, J.M., Heetkamp, M.J., Kemp, B., Schrama, J.W., Verstegen, M.W. and Van Den Brand, H. (2002) Increased fat deposition after repeated immunization in growing chickens. Poulr Sci. 81: 1308–1316.CrossRefGoogle ScholarPubMed
Parmentier, H.K., Nieuwland, M.G., Ruke, E., De Vries Reilingh, G. and Schrama, J.W. (1996) Divergent antibody responses to vaccines and divergent body weights of chicken lines selected for high and low humoral responsiveness to sheep red blood cells. Avian Diseases 40: 634–644.CrossRefGoogle ScholarPubMed
Peng, R.K. and Klasing, K.C. (1997) Expression of the chicken Interleukin-1 receptor in broilers in vivo and in vitro. Poultry Science 74.Google Scholar
Qureshi, M.A. and Havenstein, G.B. (1994) A comparison of the immune performance of a 1991 commercial broiler with a 1957 randombred strain when fed “typical” 1957 and 1991 broiler diets. Poultry Science 73: 1805–1812.CrossRefGoogle ScholarPubMed
Rautenschlein, S., Subramanian, A. and Sharma, J.M. (1999) Bioactivities of a tumour necrosis-like factor released by chicken macrophages. Dev Comp Immunol. 23: 629–640.CrossRefGoogle ScholarPubMed
Roura, E., Homedes, J. and Klasing, K.C. (1992) Prevention of Immunologic Stress Contributes To the Growth-Permitting Ability of Dietary Antibiotics in Chicks. Journal of Nurririon 122: 2383–2390.Google Scholar
Schneider, K., Klaas, R., Kaspers, B. and Staeheli, P. (2001) Chicken interleukin-6. cDNA structure and biological properties. European Journal of Biochemistry 268: 4200–4206.CrossRefGoogle ScholarPubMed
Siegel, H.S., Henken, A.M., Verstegen, M.W.A. and Van Der Hel, W. (1982a) Heat production during the induction of an immune response to sheep red blood cells in growing pullets. Poultry Science 61: 2296–2300.CrossRefGoogle ScholarPubMed
Siegel, P.B., Gross, W.B. and Cherry, J.A. (1982b) Correlated responses of chickens to selection for production of antibodies to sheep erythrocytes. Animal Blood Groups, Biochemistry, & Genetics 13: 291–297.CrossRefGoogle ScholarPubMed
Staeheli, P., Puehler, F., Schneider, K., Gobel, T.W. and Kaspers, B. (2001) Cytokines of birds: conserved functions-a largely different look. Journal of Interferon and Cytokine Research 21: 993–1010.CrossRefGoogle ScholarPubMed
Takahashi, K., Ohta, N. and Akiba, Y. (1997) Influences of dietary methionine and cysteine on metabolic responses to immunological stress by Escherichia coli lipopolysaccharide injection, and mitogenic response in broiler chickens. British Journal of Nutrition 78: 815–821.CrossRefGoogle ScholarPubMed
Tian, S. and Baracos, V.E. (1989a) Effect of Escherichia coli infection on growth and protein metabolism in broiler chicks (Callus domesticus). Comparative Biochemistry & Physiology Pan A. 94: 323–331.CrossRefGoogle Scholar
Tian, S. and Baracos, V.E. (1989b) Prostaglandin-dependent muscle wasting during infection in the broiler chick (Gallus domesticus) and the laboratory rat (Rattus norvegicus). Biochem Journal 263: 485–490.CrossRefGoogle ScholarPubMed
Tufft, L.S., Nockels, C.F. and Fettman, M.J. (1988) Effects of Escherichia coli on iron, copper, and zinc metabolism in chicks. Avian Diseases 32: 779–786.CrossRefGoogle ScholarPubMed
Webel, D.M., Johnson, R.W. and Baker, D.H. (1998a) Lipopolysaccharide-induced reductions in body weight gain and feed intake do not reduce the efficiency of arginine utilization for whole-body protein accretion in the chick. Poultry Science 77: 1893–1898.CrossRefGoogle Scholar
Webel, D.M., Johnson, R.W. and Baker, D.H. (1998b) Lipopolysaccharide-induced reductions in food intake do not decrease the efficiency of lysine and threonine utilization for protein accretion in chickens. Journal of Nutrition 128: 1760–1766.CrossRefGoogle Scholar
Weinberg, E.D. (1999) Iron Loading and Disease Surveillance. Emerging Infectious Diseases 5: 346–352.CrossRefGoogle ScholarPubMed
Weining, K.C., Sick, C., Kaspers, B. and Staeheli, P. (1998) A chicken homolog of mammalian interleukin-1 beta: cDNA cloning and purification of active recombinant protein. European Journal of Biochemistry 258: 994–1000.CrossRefGoogle ScholarPubMed
Yasuda, M., Kajiwara, E., Ekino, S., Taura, Y., Hirota, Y., Horiuchi, H., Matsuda, H. and Furusawa, S. (2003) Immunobiology of chicken germinal center: 1. Changes in surface Ig class expression in the chicken splenic germinal center after antigenic stimulation. Developmental & Comparative Immunology 27: 159–166.CrossRefGoogle ScholarPubMed