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Involvement of the hypothalamic-pituitary-thyroid axis and its interaction with the hypothalamic-pituitary-adrenal axis in the ontogeny of avian thermoregulation: a review

Published online by Cambridge University Press:  05 September 2008

M. DEBONNE ,
P.J.J. BAARENDSE ,
H. VAN DEN BRAND ,
B. KEMP ,
V. BRUGGEMAN  and
E. DECUYPERE
M. DEBONNE*
Affiliation:
Laboratory of Physiology, Immunology and Genetics of Domestic Animals, Department of Biosystems, Division of Livestock-Nutrition-Quality, Catholic University Leuven, Kasteelpark Arenberg 30, B-3001 Leuven, Belgium
P.J.J. BAARENDSE
Affiliation:
Adaptation Physiology Group, Wageningen Institute of Animal Sciences, Wageningen University, P.O. Box 338, 6700 PG, Wageningen, The Netherlands
H. VAN DEN BRAND
Affiliation:
Adaptation Physiology Group, Wageningen Institute of Animal Sciences, Wageningen University, P.O. Box 338, 6700 PG, Wageningen, The Netherlands
B. KEMP
Affiliation:
Adaptation Physiology Group, Wageningen Institute of Animal Sciences, Wageningen University, P.O. Box 338, 6700 PG, Wageningen, The Netherlands
V. BRUGGEMAN
Affiliation:
Laboratory of Physiology, Immunology and Genetics of Domestic Animals, Department of Biosystems, Division of Livestock-Nutrition-Quality, Catholic University Leuven, Kasteelpark Arenberg 30, B-3001 Leuven, Belgium
E. DECUYPERE
Affiliation:
Laboratory of Physiology, Immunology and Genetics of Domestic Animals, Department of Biosystems, Division of Livestock-Nutrition-Quality, Catholic University Leuven, Kasteelpark Arenberg 30, B-3001 Leuven, Belgium
*
Corresponding author: marian.debonne@biw.kuleuven.be
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Abstract

The emergence of thermoregulation in avian species is a complex matter in which neural as well as hormonal processes are involved. In a previous paper, the neural aspects of primary avian thermoregulation were discussed. In this paper the role of the hypothalamus-pituitary-thyroid axis (HPT-axis) and the hypothalamus-pituitary-adrenal axis (HPA-axis) in the ontogeny of avian thermoregulation is evaluated. The regulatory mechanisms and different important hormones of both axes, which have stimulatory or inhibitory effects, are discussed. Because the onset of functionality of the thermoregulatory system is of great interest, the ontogeny and functionality of the hormonal axes are clarified. There is a great difference between precocial and altricial birds in hormonal events as well as in neural processes which are involved in the emergence of thermoregulation. In precocial avian species the HPT-axis becomes functional during the mid- to late embryonic period while the same axis only becomes fully functional during the first week post-hatch in altricial avian species.

As early as the sixties, the emergence of homeothermy in chickens was investigated. It was concluded that the thyroid gland plays an important role in the thermoregulatory mechanisms of newly hatched chicks. More recent studies however were not able to show any direct effect of the thyroid hormones on the thermoregulation of day-old chicks, although blocking the conversion of T4 to T3 caused a decrease in body temperature in young chicks. Thyrotropin releasing hormone (TRH) is known to act in thermoregulation in mammals and several authors have found an effect of TRH on the metabolism of young and older chicks. However, the exact mechanism still remains unclear.

Because the HPT- and the HPA-axis show close relationships, the role of the HPA-axis in the ontogeny of thermoregulation is also taken into consideration in this review. In mammals as well as in birds, corticotropin releasing hormone (CRH) is involved in the primary thermoregulation.

We conclude that the HPT-axis has an important role in the ontogeny of avian thermoregulation. The exact role of the HPA-axis remains largely unclear although at least CRH is definitely of some importance.

Keywords

thermoregulationHPA-axisHPT-axisontogenychicken
Type
Review Article
Information
World's Poultry Science Journal , Volume 64 , Issue 3 , September 2008 , pp. 309 - 321
Copyright
Copyright © World's Poultry Science Association 2008

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References

ARANCIBIA, S., RAGE, F., ASTIER, H. and TAPIA-ARANCIBIA, L. (1996) Neuroendocrine and autonomous mechanisms underlying thermoregulation in cold environment. Neuroendocrinology 64: 257-267.CrossRefGoogle ScholarPubMed
BAARENDSE, P.J.J., DEBONNE, M., DECUYPERE, E., KEMP, B. and VAN DEN BRAND, H. (2007) Ontogeny of avian thermoregulation from a neural point of view. World's Poultry Science Journal 63: 267-276.CrossRefGoogle Scholar
BARTHA, T. (1993) Thyroid hormone metabolism in broiler chickens as influenced by exogenous and endogenous factors. Ph. D. Thesis, Katholieke Universiteit Leuven.Google Scholar
BORGES, M.J., LABOVRENE, J. and INGBAR, S.H. (1980) Changes in hepatic iodothyronine metabolism during ontogeny of the chick embryo. Endocrinology 107: 1751-1761.CrossRefGoogle ScholarPubMed
CARLIN, K.M., VALE, W.W. and BALE, T.L. (2006) Vital functions of corticotrophin-releasing factor in maintenance and regulation of energy metabolism. Proceedings of the National Academy of Sciences of the United States of America, 103 (9), pp. 3462-3467.Google Scholar
CARSIA, R.V. and HARVEY, S. (2000) Adrenals. In: WHITTOW, G.C. (Ed) Sturkie's Avian Physiology, pp. 489-537 (California, Academic Press).Google Scholar
DAUGÈRAS, N., BRISSON, A., LAPOINTE-BOULU, F. and LACHIVER, F. (1976) Thyroidal iodine metabolism during the development of the chick embryo. Endocrinology 98: 1321-1331.CrossRefGoogle ScholarPubMed
DAVISON, T.F. (1976) Circulating thyroid hormones in the chicken before and after hatching. General and Comparative Endocrinology 29: 21-27.CrossRefGoogle ScholarPubMed
DECUYPERE, E., HERMANS, C., MICHELS, H., KÜHN, E.R. and VERHEYEN, J. (1981) Thermoregulatory response and thyroid hormone concentration after cold exposure of young chicks treated with iopanoic acid or saline. In: Pethes, G., Péczely, P. & Rudas, P. (Eds) Advances in Physiological Sciences Vol. 33, Recent Advances of Avian Endocrinology, pp. 291-299 (New York, Pergamon Press).Google Scholar
DECUYPERE, E., KÜHN, E.R., CLIJMANS B., , NOUWEN, E.J. and MICHELS, H. (1982) Prenatal peripheral monodeiodination in chick embryo. General and Comparative Endocrinology 47: 15-17.Google Scholar
DECUYPERE, E., IQBAL, A., MICHELS, H., KÜHN, E.R., SCHNEIDER, R. and ABDEL AZEEM, A. (1988) Thyroid hormone response to thyrotropin releasing hormone after cold treatment during pre- and postnatal development in the domestic fowl. Hormone and metabolic research 20: 484-489.CrossRefGoogle ScholarPubMed
DE FANTI, B.A. and MARTINEZ, J.A. (2002) Central urocortin activation of sympathetic-regulated energy metabolism in Wistar rats. Brain Research 930: 37-41.CrossRefGoogle ScholarPubMed
DE GROEF, B., GORIS, N., ARCKENS, L., KÜHN, E.R. and DARRAS, V.M. (2003) Corticotropin-releasing hormone (CRH)-induced thyrotropin release is directly mediated through CRH receptor 2 on thyrotrophs. Endocrinology 144: 5537-5544.CrossRefGoogle Scholar
EDELMAN, I.S. and ISMAIL-BEIGI, F. (1974) Thyroid thermogenesis and active sodium transport. Recent Progress in Hormone Research 30: 235-257.Google ScholarPubMed
FREEMAN, B.M. (1964) The emergence of the homeothermic-metabolic response in the fowl (Gallus domesticus). Comparative Biochemistry and Physiology 13: 413-422.CrossRefGoogle ScholarPubMed
FREEMAN, B.M. (1970) Thermoregulatory mechanisms of the neonate fowl. Comparative Biochemistry and Physiology 33: 219-230.CrossRefGoogle Scholar
GERIS, K.L., KOTANEN, S.P., BERGHMAN, L.R., KÜHN, E.R. and DARRAS, V.M. (1996) Evidence of a thyrotropin-releasing activity of ovine corticotropin-releasing factor in the domestic fowl (Gallus domesticus). General and Comparative Endocrinology 104: 139-146.CrossRefGoogle ScholarPubMed
GERIS, K.L., BERGHMAN, L.R., KÜHN, E.R. and DARRAS, V.M. (1998) Pre- and posthatch developmental changes in hypothalamic thyrotropin-releasing hormone and somatostatin concentrations and in circulating growth hormone and thyrotropin levels in the chicken. Journal of endocrinology 159: 219-225.CrossRefGoogle ScholarPubMed
GERIS, K.L., DE GROEF, B., KÜHN, E.R. and DARRAS, V.M. (2003) In vitro study of corticotropin-releasing hormone-induced thryotropin release: ontogeny and inhibition by somatostatin. General and Comparative Endocrinology 132: 272-277.CrossRefGoogle Scholar
GREENSPAN, F.S. and RAPOPORT, B. (1991) Thyroid gland. In: Basic and clinical endocrinology, 3rd edition. London.Google Scholar
HADLEY, M.E. (2000) Thyroid hormones. In: Endocrinology 5th edition, Prentice-Hall international. London.Google Scholar
HWANG-BO, J., MURAMATSU, J. and OKUMURA, J. (1990a) Relative biopotency of triiodothyronine and of thyroxine for inducing oxygen consumption in young chicks. Poultry Science 69:1027-1029.Google Scholar
HWANG-BO, J., MURAMATSU, J. and OKUMURA, J. (1990b) . Age dependency of triiodothyronine-induced thermogenesis in young chicks: inhibition by propylthiouracil. Poultry Science 69:1599-1601.CrossRefGoogle ScholarPubMed
JÓZSA, R., VIGH, S., MESS, B. and SCHALLY, A.V. (1986) Ontogenetic development of corticotropin-releasing factor (CRF)-containing neural elements in the brain of the chicken during incubation and after hatching. Cell and Tissue Research 244: 81-685.CrossRefGoogle ScholarPubMed
KÜHN, E.R., DECUYPERE, E., COLEN, L.M. and MICHELS, H. (1982) Posthatch growth and development of a circadian rhythm for thyroid hormones in chicks incubated at different temperatures. Poultry Science 61: 540-549.CrossRefGoogle ScholarPubMed
LIN, M.T., CHANDRA, A., CHERN, Y.F. and TSAY, B.L. (1980) Effects of thyrotropic-releasing hormone (TRH) on thermoregulation in the rat. Experientia 36: 1077-1078.Google Scholar
LIU, L. and PORTER, T.E. (2004) Endogenous thyroid hormones modulate pituitary somatotroph differentiation during chicken embryonic development. Journal of Endocrinology 180: 45-53.Google Scholar
MARAUD, R., AUDINE, M. and STOLL, R. (1983) Influence of an early grafted adenohypophysis on the thyroid of the chicken embryo. General and Comparative Endocrinology 51: 329-337.CrossRefGoogle Scholar
MCNABB, F.M. and MCNABB, R.A. (1977) Thyroid development in precocial and altricial avian embryos. The Auk 94: 736-742.Google Scholar
MCNABB, F.M., WEIRICH, R.T. and MCNABB, R.A. (1981) Thyroid function in embryonic and perinatal Japanese Quail. General and Comparative Endocrinology 43, 218-226.CrossRefGoogle ScholarPubMed
MCNABB, F.M.A. and HUGHES, T.E. (1983) The role of serum binding proteins in determining free thyroid hormone concentrations during development in quail. Endocrinology 113: 957-963.CrossRefGoogle ScholarPubMed
MCNABB, F.M.A., STANTON, F.W. and DICKEN, S.G. (1984) Post-hatching thyroid development and body growth in precocial vs altricial birds. Comparative Biochemistry and Physiology 78A: 629-635.CrossRefGoogle ScholarPubMed
MCNABB, F.M.A. and CHENG, M.F. (1985) Thyroid development in altricial Ring Doves, Streptopelia risoria. General and Comparative Endocrinology 58: 243-251.CrossRefGoogle ScholarPubMed
MCNICHOLS, M.J. and MCNABB, F.M. (1988) Development of thyroid function and its pituitary control in embryonic and hatchling precocial Japanese quail and altricial Ring doves. General and Comparative Endocrinology 70(1): 109-118.CrossRefGoogle ScholarPubMed
MEEUWIS, R., MICHIELSEN, R., DECUYPERE, E. and KÜHN, E.R. (1989) Thyrotropic activity of the ovine corticotropin-releasing factor in the chick embryo. General and Comparative Endocrinology 76: 357-363.Google Scholar
METCALF, G. (1974) TRH: a possible mediator of thermoregulation. Nature 252: 310-311.Google Scholar
MORAES, V.M.B., MALHEIROS, R.D., BRUGGEMAN, V., COLLIN, A., TONA, K., VAN AS, P., ONAGBESAN, O.M., BUYSE, J., DECUYPERE, E. and MACARI, M. (2004) The effect of timing of thermal conditioning during incubation on embryo physiological parameters and its relationship to thermotolerance in adult broiler chickens. Journal of Thermal Biology 29: 55-61.Google Scholar
NISTICÒ, G., ROTIROTI, A., DE SARRO, J.D. and STEPHENSON, J.D. (1978) Behavioural, electrocortical and body temperature effects after intracerebral infusion of TRH in fowls. European Journal of Pharmacology 50: 253-260.CrossRefGoogle ScholarPubMed
PRATI, M., CALVO, R. and ESCOBAR, DE G.M. (1992) L-Thyroxine and 3,5,3’-triiodothyronine concentrations in the chicken egg and in the embryo before and after the onset of thyroid function. Endocrinology 130: 2651-2659.CrossRefGoogle ScholarPubMed
RIVEST, S., DESHAIES, Y. and RICHARD, D. (1989) Effects of corticotropin-releasing factor on energy balance in rats are sex dependent. American Journal of Physiology 257: R1417-R1422.Google ScholarPubMed
SASAKI, F., DOSHITA, A., MATSUMOTO, Y., KUWAHARA, S., TSUKAMOTO, Y. and OGAWA, K. (2003) Embryonic development of the pituitary gland in the chick. Cells Tissues Organs 173: 65-74.CrossRefGoogle ScholarPubMed
SHAIN, W.G., HILFER, S.R. and FONTE, V.G. (1972) Early organogenesis of the embryonic chick thyroid. I. Morphology and biochemistry. Developmental Biology 28(1): 202-218.CrossRefGoogle ScholarPubMed
SPIERS, D.E., MCNABB, R.A. and MCNABB, F.M.A. (1974) The development of thermoregulatory ability, heat seeking activities, and thyroid function in hatchling Japanese quail (Coturnix coturnix japonica). Journal of Comparative Physiology 89: 159-174.CrossRefGoogle Scholar
SPIERS, D.E. and RINGER, R.K. (1984) Thyroid hormone changes in the Bobwhite (Colinus virginianus) after hatching. General and Comparative Endocrinology 53: 302-308.CrossRefGoogle ScholarPubMed
TACHIBANA, T., SAITO, E-S., SAITO, S., TOMONAGA, S., DENBOW, D.M. and FURUSE, M. (2004) Comparison of brain arginine-vasotocin and corticotropin-releasing factor for physiological responses in chicks. Neuroscience Letters 360: 165-169.CrossRefGoogle ScholarPubMed
TACHIBANA, T., TAKAHASHI, H., DENBOW, D.M. and FURUSE, M. (2006) Thyrotopin-releasing hormone increased heat production without the involvement of corticotropin-releasing factor in neonatal chicks. Pharmacology, Biochemistry and Behavior 83: 528-532.CrossRefGoogle Scholar
TAKAHASHI, H., IIGO, M., ANDO, K., TACHIBANA, T., DENBOW, D.M. and FURUSE, M. (2005) Regulation of body temperature by thyrotropin-releasing hormone in neonatal chicks. Developmental Brain Research 157: 58-64.Google Scholar
TAZAWA, H., MORIYA, K., TAMURA, A., KOMORO, T. and AKIYAMA, R. (2001) Ontogenic study of thermoregulation in birds. Journal of Thermal Biology 26, 281-286.CrossRefGoogle Scholar
THOMMES, R.C. (1958) Vasculogenesis in selected endocrine glands of normal and hypophysectomized chick embryos. I. The thyroid. Growth 22, 243-264.Google Scholar
THOMMES, R.C. and HYLKA, V.W. (1977) Plasma iodothyronines in the embryonic and immediate post-hatch chick. General and Comparative Endocrinology 32: 417-422.CrossRefGoogle ScholarPubMed
THOMMES, R.C. and HYLKA, V.W. (1978) Hypothalamo-adenohypophyseal-thyroid interrelationships in the chick embryo. I. TRH and TSH sensitivity. General and Comparative Endocrinology 34: 193-200.Google Scholar
THOMMES, R.C. and TONETTA, S.A. (1979) Hypothalamo-adenohypophyseal-thyroid interrelationships in the chick embryo. II. Effects of thiourea treatment on plasma total thyroxine levels and thyroidal 125I uptake. General and Comparative Endocrinology 37: 167-176.CrossRefGoogle ScholarPubMed
THOMMES, R.C., MARTENS, J.B., HOPKINS, W.E., CALIENDO, J., SORRENTINO, M.J. and WOODS, J.E. (1983) Hypothalamo-adenohypophyseal-thyroid interrelationships in the chick embryo IV. Immunocytochemical demonstration of TSH in the hypophyseal pars distalis. General and Comparative Endocrinology 51: 434-443.CrossRefGoogle ScholarPubMed
THOMMES, R.C., CALIENDO, J. and WOODS, J.E. (1985) Hypothalamo-adenohypophyseal-thyroid interrelationships in the chick embryo IIV. Immunocytochemical demonstration of thyrotrophin-releasing hormone. General and Comparative Endocrinology 57: 1-9.CrossRefGoogle Scholar
VÝBOH, P., ZEMAN, M., JÚRANI, M., BUYSE, J. and DECUYPERE, E. (1996) Plasma thyroid hormone and growth hormone patterns in precocial Japanese quail and altricial European starlings during postnatal development. Comparative Biochemistry and Physiology 114: 23-27.Google Scholar
VÝBOH, P., ZEMAN, M., BUYSE, J., JURÁNI, M. and DECUYPERE, E. (2001) Developmental changes in thyrotropic and somatotropic effect of TRH in precocial Japanese quail and altricial European starling. General and Comparative Endocrinology 124: 293-299.CrossRefGoogle Scholar