Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-27T00:21:48.929Z Has data issue: false hasContentIssue false
  • English
  • Français

Coping with metabolic stress in wild and domesticated animals

Published online by Cambridge University Press:  27 February 2018

C. M. Pond  and
E. A. Newsholme
C. M. Pond
Affiliation:
Department of Biology, Open University, Milton Keynes MK7 6AA
E. A. Newsholme
Affiliation:
Merton College, Oxford OX1 4JD
Get access

Abstract

Ethological and ecological studies of wild animals are producing evidence for metabolic stress during courtship, breeding and parental care comparable with that of domestic livestock. Resistance to disease may be compromised by the demand for fatty acids and proteins during reproduction and even more during lactation. The adipose tissue around major lymph nodes is indistinguishable histologically from that in larger depots. In vitro and in vivo studies reveal that it is specialized to respond to lipolytic agonists secreted by lymphoid cells but is insensitive to the endocrine conditions of short-term fasting. These properties enable it to provision adjacent immune cells. Such adipose tissue may act as a forum for competing demands of mammary glands, muscles etc. and local defences against pathogens. Glutamine is essential to the nutrition of the immune system and is used by the mammary gland. Muscle is the best known source but adipose tissue also participates in glutamine metabolism and may become more important in animals in which the musculature is wasted through prolonged lactation.

Type
Research Article
Information
BSAP Occasional Publication , Volume 24: Metabolic stress in dairy cows , 1999 , pp. 9 - 20
Copyright
Copyright © British Society of Animal Science 1999

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ardawi, M. S. M. and Newsholme, E. A. 1990. Glutamine, the immune system and the intestine. Journal of Laboratory and Clinical Medicine 115: 654–655.Google ScholarPubMed
Bathija, A., Davis, S. and Trubowitz, S. 1979. Bone marrow adipose tissue: response to acute starvation. American Journal of Haematology 6:191–198.Google Scholar
Beisel, W. R. 1977. Magnitude of host nutritional response to infection. American Journal of Clinical Nutrition 30: 1236–1247.Google Scholar
Berkowitz, D. E., Brown, D., Lee, K. M., Emala, C, Palmer, D., An, Y. and Breslow, M. 1998. Endotoxin-induced alteration in the expression of leptin and beta(3)-adrenergic receptor in adipose tissue. American Journal of Physiology 37: E992–E997.Google Scholar
Boyd, I. L., Croxall, J. P., Lunn, N. J. and Reid, K. 1995. Population demography of antarctic fur seals — the costs of reproduction and implications for life histories. Journal of Animal Ecology 64: 505–518.CrossRefGoogle Scholar
Caro, J. F., Scutia, M. K., Kalaczynski, J. W., Zhang, P. L. and Coursidine, R. V. 1996. Leptin, the tale of an obesity gene. Diabetes 45:1455–1462.CrossRefGoogle ScholarPubMed
Castell, L. M., Poortmans, J. and Newsholme, E. A. 1996. Does glutamine have a rôle in reducing infections in athletes? European Journal of Applied Physiology 73:488–491.Google Scholar
Chandra, R. K. 1992. Nutrition and immunology. ARTS Biomedicai, St. John’s, Newfoundland.Google Scholar
Clutton-Brock, T. H. and Parker, G. A. 1992. Potential reproductive rates and the operation of sexual selection. Quarterly Review of Biology 67:437–456.Google Scholar
Deerenberg, C., Arpanius, V., Daan, S. and Bos, N. 1997. Reproductive effort decreases antibody responsiveness. Proceedings of the Royal Society of London, B 264: 1021–1029.Google Scholar
Derocher, A. E. and Stirling, I. 1996. Aspects of survival in juvenile polar bears. Canadian Journal of Zoology 74:1246–52.Google Scholar
Derocher, A. E. and Stirling, I. 1998. Maternal investment and factors affecting offspring size in polar bears (Ursus maritimus). Journal of Zoology, London 245: 253–260.CrossRefGoogle Scholar
Digby, J. E. 1998. The role of different adipose depots in glutamine metabolism following feeding, fasting and exercise in the guinea-pig. Ph.D. thesis, Open University, UK.Google Scholar
Etherton, T. D. and Bauman, D. E. 1998. Biology of somatotropin in growth and lactation of domestic animals. Physiological Reviews 78: 745–761.CrossRefGoogle ScholarPubMed
Flier, J. S. 1995. The adipocyte: storage depot or node in the energy information superhighway? Cell 80:15–18.Google Scholar
Folstad, I. and Karter, A. J. 1992. Parasites, bright males and the immunocompetence handicap. American Naturalist 139: 603–622.CrossRefGoogle Scholar
Gretz, J. E. Anderson, A. O. and Shaw, S. 1997. Cords, channels, corridors and conduits: critical architectural elements facilitating cell interactions in the lymph node cortex. Immunology Reviews 156:11–24.Google Scholar
Griffiths, R. D., Jones, C and Palmer, T. E. A. 1997. Six-month outcome of critically ill patients given glutamine-supplemented parental nutrition. Nutrition 13: 295–302.Google Scholar
Grimble, J. M., Dorheim, M.-A., Cheng, Q., Medina, K., Wang, C.-S., Jones, R., Koren, E., Pietrangeli, C. and Kincade, P. W. 1990. Adipogenesis in a murine bone marrow stromal cell line capable of supporting B lymphocyte growth and proliferation: biochemical and molecular characterization. European journal of Immunology 20:379–387.Google Scholar
John, J. L. 1994. The avian spleen: a neglected organ. Quarterly Review of Biology 69: 327–351.Google Scholar
Klasing, K. C. and Austic, R. E. 1984a. Changes in protein synthesis due to inflammatory challenge. Proceedings of the Society for Experimental Biology and Medicine 176: 285–291.Google Scholar
Klasing, K. C. and Austic, R. E. 1984b. Changes in protein degradation due to inflammatory challenge. Proceedings of the Society for Experimental Biology and Medicine 176: 292–296.Google Scholar
Lord, G. M., Matarese, G., Howard, J. K., Baker, R. J., Bloom, S. R. and Lechler, R. I. 1998. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature, London 394:987–989.Google Scholar
MacQueen, H. A. and Pond, C. M. 1998. Immunofluorescent localization of tumour necrosis factor-a receptors on the popliteal lymph node and the surrounding adipose tissue following simulated immune challenge. journal of Anatomy 192: 223–231.Google Scholar
Mattacks, C. A. and Pond, C. M. 1997. The effects of feeding suet-enriched chow on site-specific differences in the composition of triacylglycerol fatty acids in adipose tissue and its interactions in vitro with lymphoid cells. British journal of Nutrition 77: 621–643.CrossRefGoogle ScholarPubMed
Mattacks, C. A. and Pond, C. M. 1999. Interactions of noradrenalin and tumour necrosis factor-a, interleukin-4 and interleukin-6 in the control of lipolysis from adipocytes around lymph nodes. Cytokine 11: 334–346.CrossRefGoogle Scholar
Miles, E. A. and Calder, P. C. 1998. Modulation of immune function by dietary fatty acids. Proceedings of the Nutrition Society 57:277–292.Google Scholar
Mailer, A. P. 1997. Immune defences extra-paternity and sexual selection in birds. Proceedings of the Royal Society of London, B 264: 561–566.Google Scholar
Møller, A. P. and Erritzøe, J. 1996. Parasite virulence and host immune defense — host immune-response is related to nest reuse in birds. Evolution 50:2066–2072.Google Scholar
Newsholme, E. A. and Calder, P. C. 1997. The proposed role of glutamine in some cells of the immune system and speculative consequences for the whole animal. Nutrition 13: 728–730.Google Scholar
Newsholme, E. A., Crabtree, B. and Ardawi, M. S. M. 1985. Glutamine metabolism in lymphocytes: its biochemical, physiological and clinical importance. Quarterly Journal of Experimental Physiology and Cognate Medical Science 70: 473–489.Google Scholar
Newsholme, E. A. and Parry-Billings, M. 1990. Properties of glutamine release and its importance for the immune system, journal of Parenteral and Enterai Nutrition 14: S63–S67.Google Scholar
Nordling, D., Andersson, M., Zohari, S. and Gustafsson, L. 1998. Reproductive effort reduces specific immune response and parasite resistance. Proceedings of the Royal Society of London, B 265: 1291–1298.CrossRefGoogle Scholar
Oláh, I. and Glick, B. 1983. Avian lymph nodes: light and electron microscope study. Anatomical Record 205:287–299.Google Scholar
Pond, C. M. 1977. The significance of lactation in the evolution of mammals. Evolution 31: 177–199.Google Scholar
Pond, C. M. 1992. An evolutionary and functional view of mammalian adipose tissue. Proceedings of the Nutrition Society 51:367–377.Google Scholar
Pond, C. M. 1996. Interactions between adipose tissue and the immune system. Proceedings of the Nutrition Society 55: 111–126.Google Scholar
Pond, C. M. 1998. The fats of life. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Pond, C. M. and Mattacks, C. A. 1995. Interactions between adipose tissue around lymph nodes and lymphoid cells in vitro, journal of Lipid Research 36: 2219–2231.CrossRefGoogle ScholarPubMed
Pond, C. M. and Mattacks, C. A. 1998. In vivo evidence for the involvement of the adipose tissue surrounding lymph nodes in immune responses. Immunology Letters 63: 159–167.Google Scholar
Ramsay, M. A. and Dunbrack, R. L. 1986. Physiological constraints on life history phenomena: the example of small bear cubs at birth. American Naturalist 127: 735–743.Google Scholar
Ramsay, M. A. and Stirling, I. 1988. Reproductive biology and ecology of female polar bears (Ursus maritimus). Journal of Zoology, London 214: 601–634.Google Scholar
Rollo, C. D., Rintoul, J. and Kajiura, L. J. 1997. Lifetime reproduction of giant transgenic mice: the energy stress paradigm. Canadian journal of Zoology 75: 1336–1345.Google Scholar
Singh, D. and Bronstad, P. M. 1997. Sex differences in the anatomical locations of human body scarification and tattooing as a function of pathogen prevalence. Evolution and Human Behavior 18: 403–416.Google Scholar
Turner, R. J. 1994. Immunology: a comparative approach. John Wiley & Sons. Chichester.Google Scholar
Van Heek, M., Mullins, D. E., Wirth, M. A., Graziano, M. P., Fawzi, A. B., Compton, D. S., France, C. F., Hoos, L. M., Casale, R. L., Sybertz, E. J., Strader, C. D. and Davis, H. R. 1997. The relationship of tissue localization, distribution and turnover to feeding after intraperitoneal 125I leptin administration to ob/ob and dbldb mice. Hormone and Metabolism Research 28: 653–568.Google Scholar
Vernon, R. G., Doris, R., Finley, E., Houslay, M. D., Kilgour, E. and Lindsay-Watt, S. 1995. Effects of lactation on the signal-transduction systems regulating lipolysis in sheep subcutaneous and omental adipose-tissue. Biochemical Journal 308: 291–296.Google Scholar
Wu, G. Y., Meier, S. A. and Knabe, D. A. 1996. Dietary glutamine supplementation prevents jejunal atrophy in weaned pigs. Journal of Nutrition 127: 2253–2259.Google Scholar
Yaqoob, P. and Calder, P. C. 1995. Effects of dietary lipid manipulation upon inflammatory mediator production by murine macrophages. Cellular Immunology 163: 120–128.Google Scholar
Yoo, S. S., Field, C. J. and McBurney, M. I. 1997. Glutamine supplementation maintains intramuscular glutamine concentrations and normalised lymphocyte function in infected early weaned pigs. Journal of Nutrition 126: 2578–2584.Google Scholar
Zuk, M. 1996. Disease, endocrine-immune interactions and sexual selection. Ecology 77:1037–1042.Google Scholar