Hostname: page-component-848d4c4894-8bljj Total loading time: 0 Render date: 2024-07-07T00:34:12.708Z Has data issue: false hasContentIssue false
  • English
  • Français

A role for thyroid hormones in the regulation of diet-induced thermogenesis in birds

Published online by Cambridge University Press:  09 March 2007

Jean-François Gabarrou ,
Claude Duchamp ,
John Williams  and
Pierre-André Géraert
Jean-François Gabarrou
Affiliation:
INRA, Station de Recherches Avicoles, 37380 Nouzilly, France
Claude Duchamp
Affiliation:
UMR 5578 CNRS-Université, Cl. Bernard Lyon 1/LA INRA, 69622 Villeurbane cedex, France
John Williams
Affiliation:
INRA, Station de Recherches Avicoles, 37380 Nouzilly, France
Pierre-André Géraert
Affiliation:
INRA, Station de Recherches Avicoles, 37380 Nouzilly, France
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The possible involvement of thyroid hormones in avian diet-induced thermogenesis (DIT) was investigated in two lines of cockerels divergently selected for high (R-) or low (R+) food efficiency. For a given body weight, R+ cockerels exhibited a higher food intake than R- cockerels (+49 to +76%) and increased DIT (+25%). Plasma thyroxine (T4) levels did not differ between lines whatever the feeding status of the birds. Plasma 3,5,3'-triiodothyronine (T3) level was lower in fasted R+ than in fasted R- cockerels while the opposite was observed after a meal. Iopanic acid injections reduced both plasma T3 concentrations and heat production to the same levels in both lines. Hepatic 5'-deiodinase activity measured with an exogenous sulfhydryl group (dithiothreitol) did not differ between lines, but when the sulfhydryl group was omitted, the activity was higher in R+ than in R- birds (90 ν. 42 pmol T3/min per liver). T3-binding capacity of isolated hepatic nuclei was higher (+76%) in R+ than in R- birds. Long-term or acute pair-feeding of R+ cockerels to the level of R- controls did not alter these results. The present results suggest that T3, mainly originating from peripheral conversion of T4 to T3, is involved in DIT in the R+ line. Availability of endogenous sulfhydryl groups appears to play an important part in the modulation of hepatic deiodinase activity. The higher concentration of nuclear T3 receptors may further increase the effects of the hormone, suggesting a major role of thyroid hormones associated with catecholamines in the stimulation of avian DIT. The underlying thermogenic mechanisms remain to be elucidated.

Keywords

Diet-induced thermogenesisThyroid hormonesBirds
Type
Animal Nutrition
Information
British Journal of Nutrition , Volume 78 , Issue 6 , December 1997 , pp. 963 - 973
Copyright
Copyright © The Nutrition Society 1997

References

REFERENCES

Arieli, A. & Berman, A. (1979) The effect of thyroxine thermoregulation in the mature domestic fowl (Gallus domesticus). Journal of Thermal Biology 4, 247–249.CrossRefGoogle Scholar
Balsam, A. & Ingbar, S. H. (1979) Observations on the factors that control the generation of triiodothyronine from thryroxine in rat liver and the nature of the defect induced by fasting. Journal of Clinical Investigation 63, 1145–1156.CrossRefGoogle Scholar
Bilezikian, J. P. & Loeb, J. N. (1983) The influence of hyperthyroidism and hypothyroidism on α and β-adrenergic receptor systems and adrenergic responsiveness. Endocrine Review 4, 378–388.CrossRefGoogle ScholarPubMed
Bordas, A. & Mérat, P. (1984) Correlated responses in a selection experiment on residual feed intake of adult Rhode Island Red cocks and hens. Annales Agriculturae Fenniae 23, 233–237.Google Scholar
Bordas, A., Tixier-Boichard, M. & Mérat, P. (1992) Direct and correlated responses to divergent selection for residual food intake in Rhode Island Red laying hens. British Poultry Science 33, 741–754.CrossRefGoogle ScholarPubMed
Byerly, T. C., Kessler, J. W., Gous, R. M. & Thomas, P. (1980) Feed requirement for egg production. Poultry Science 59, 2500–2507.CrossRefGoogle Scholar
Danforth, E. Jr, Horton, E. S., O'Connell, M., Sims, E. A. H., Burger, A. G., Ingbar, S. H., Braverman, L. & Vagenakis, A. G. (1979) Dietary-induced alterations in thyroid hormone metabolism during overnutrition. Journal of Clinical Investigation 64, 1336–1347.CrossRefGoogle ScholarPubMed
Dauncey, M. J., Brown, D., Hayashi, M. & Ingram, D. L. (1992) Thyroid hormone nuclear receptors in skeletal muscle as influenced by environmental temperature and energy intake. Quarterly Journal of Experimental Physiology 73, 183–191.CrossRefGoogle Scholar
Decuypere, E., Buyse, J., Scanes, C. G., Huybrechts, L. & Kühn, E. R. (1987) Effects of hyper- or hypothyroid status on growth, adiposity and levels of growth hormone, somatomedin C and thyroid metabolism in broiler chickens. Reproduction Nutrition and Development 27, 555–565.CrossRefGoogle ScholarPubMed
Decuypere, E., Hermans, C., Michels, H., Kühn, E. R. & Verheyen, J. (1980) Thermoregulatory response and thyroid hormone concentration after cold exposure of young chicks treated with iopanoic acid or saline. In Advances in Physiology Science, Vol. 33, Recent Advances of Avian Endocrinology pp. 291–299 ]Pethes, G., Péczely, P. and Rudas, P., editors[. Oxford: Pergamon Press Ltd.Google Scholar
El-Kazzi, M., Bordas, A., Gandemer, G. & Minvielle, F. (1995) Divergent selection for residual food intake in Rhode Island Red egg-laying lines: gross carcase composition, carcase adiposity and lipid contents of tissues. British Poultry Science 36, 719–728.CrossRefGoogle ScholarPubMed
Fairfull, R. W. & Chambers, J. R. (1984) Breeding for feed efficiency: poultry. Canadian Journal of Animal Science 64, 513–527.CrossRefGoogle Scholar
Gabarrou, J.-F. (1996). La thermogénèse alimentaire chez les oiseaux: composantes, régulations et mécanismes (Diet-induced thermogenesis in birds: components, regulations and mechanisms), pp. 165–167. PhD Thesis, University Francois Rabelais, Tours, France.Google Scholar
Gabarrou, J. F. & Géraert, P. A. (1994 a). Regulation of diet-induced thermogenesis. In Proceedings of the 13th Symposium of Energy Metabolism of Farm Animals. European Association for Animal Production Publication no. 76, pp. 113–116. Mojacar, Spain: EAAP.Google Scholar
Gabarrou, J. F. & Géraert, P. A. (1994 b) β-Adrenergic and serotoninergic control of diet-induced thermogenesis in birds. Reproduction Nutrition and Development 34, 634.CrossRefGoogle Scholar
Gabarrou, J. F., Géraert, P. A., François, N., Guillaumin, S., Picard, M. & Bordas, A. (1998). Energy balance of laying hens selected on residual food consumption. British Poultry Science (In the Press).CrossRefGoogle ScholarPubMed
Gavin, L. A., McMahon, F. A. & Moeller, M. (1980) Dietary modification of thyroxine deiodination in rat liver is not mediated by hepatic sulfhydryls. Journal of Clinical Investigation 65, 943–946.CrossRefGoogle Scholar
Géraert, P. A. (1990) Dépense énergétique et échanges respiratoires: description d'une installation automatisée appliquée aux oiseaux (Thermogenesis and respiratory gas exchanges: description of an automated device for birds). Cahiers de Nutrition et de Diététique 25, 205.Google Scholar
Géraert, P. A., Guillaumin, S., Bordas, A. & Mérat, P. (1991). Evidence of a genetic control of diet-induced thermogenesis in poultry. In Proceedings of the 12th Symposium of Energy Metabolism of Farm Animals. European Association for Animal Production Publication no. 58, pp. 380–383. Kartause Ittinen, Switzerland: EAAP.Google Scholar
Harris, A. R. C., Fang, S-L., Hinerfeld, L., Braverman, L. E. & Vagenakis, A. G. (1979) The role of sulfhydryl groups on the impaired hepatic 3',3,5-triiodothyronine generation from thyroxine in the hypothyroid, starved, fetal, and neonatal rodent. Journal of Clinical Investigation 63, 516–524.CrossRefGoogle Scholar
Harrison, A. P., Rowlerson, A. M. & Dauncey, M. J. (1996) Selective regulation of myofiber differentiation by energy status during postnatal development. American Journal of Physiology 270, R667–R674.Google ScholarPubMed
Hwang-Bo, J., Muramatsu, T. & Okumura, J. (1990) Effect of dietary protein and fat content on tri-iodothyronine-induced thermogenesis in young chicks (Gallus domesticus). Comparative Biochemistry and Physiology 95A, 429–433.Google Scholar
Kittok, R. J., Greninger, T. J., DeShazer, J. A., Lowary, S. R. & Mather, F. B. (1982) Metabolic response of the rooster after exogenous thyroid hormones. Poultry Science 61, 1748–1752.CrossRefGoogle ScholarPubMed
Klandorf, H., Sharp, P. J. & MacLeod, M. G. (1981) The relation between heat production and concentration of plasma thyroid hormones in the domestic hen. General Comparative Endocrinology 45, 513–520.CrossRefGoogle Scholar
Kuhn, E. R., Verheyen, G., Chiasson, R. B., Huts, C., Huybrechts, L., Van den Steen, P. & Decuypere, E. (1987) Growth hormone stimulates the peripheral conversion of thyroxine into triiodothyronine by increasing the liver 5'-monodeiodinase activity in the fasted and normal fed chicken. Hormone and Metabolic Research 19, 304–308.CrossRefGoogle Scholar
Labarca, C. & Paigen, K. (1980) A simple, rapid and sensitive DNA assay procedure. Analytical Biochemistry 102, 344–352.CrossRefGoogle ScholarPubMed
Lazar, M. A. (1993) Thyroid hormone receptors: multiple forms, multiple possibilities. Endocrine Review 14, 184–193.Google ScholarPubMed
Macari, M., Dauncey, M. J., Ramsden, D. B. & Ingram, D. L. (1983) Thyroid hormone metabolism after acclimatization to a warm or cold temperature under conditions of high or low energy intake. Quarterly Journal of Experimental Physiology 68, 709–718.CrossRefGoogle ScholarPubMed
May, J. D. (1989) The role of the thyroid in avian species. Critical Review of Poultry Biology 2, 171–186.Google Scholar
Morovat, A. & Dauncey, M. J. (1992) Short-term changes in the 3,5,3'-tri-iodothyronine nuclear receptor-binding capacity of porcine skeletal muscle following food intake. Journal of Endocrinology 134, 67–72.CrossRefGoogle Scholar
Romijn, C. & Lokhorst, W. (1961). Some aspect of energy metabolism in birds. In Proceedings of the 2nd Symposium on Energy Metabolism of Farm Animals. European Association for Animal Production Publication no. 10, pp. 49–59. Wageningen: EAAP.Google Scholar
Rothwell, N. J. & Stock, M. J. (1979) A role for brown adipose tissue in diet-induced thermogenesis. Nature 281, 31–35.CrossRefGoogle ScholarPubMed
Singh, A., Reineke, E. P. & Ringer, R. K. (1968) Influence of thyroid status of the chick on growth and metabolism, with observations on several parameters of thyroid function. Poultry Science 47, 212–219.CrossRefGoogle ScholarPubMed
Surks, M. I. & Oppenheimer, J. H. (1977) Concentration of l-thyroxine and l-triiodothyronine specifically bound to nuclear receptors in rat liver and kidney. Journal of Clinical Investigation 60, 555–562.CrossRefGoogle ScholarPubMed
Tixier, M., Bordas, A. & Mérat, P. (1988). Divergent selection for residual feed intake in laying hens: effect on growth and fatness. In Leanness in Domestic Birds pp. 129–132 ]Leclercq, B. and Whitehead, C.C., editors[. London: Butterworths Ltd.CrossRefGoogle Scholar
Visser, T. J., Van Der Does-Tobe, I., Docter, R. & Hennemann, G. (1976) Kinetics of enzymic reductive deiodination of iodothyronines. Biochemical Journal 157, 479–482.CrossRefGoogle Scholar
Zein-El-Dein, A., Bordas, A. & Mérat, P. (1985) Selection divergente pour la composante résiduelle de la consommation alimentaire des poules pondeuses, effets sur la composition corporelle (Divergent selection on residual food consumption in laying hens, effects on body composition). Archiv für Geflügelkünde 49, 158–160.Google Scholar