Cold Adaptation and Thyroid Hormone Metabolism

Abstract

Resting oxygen consumption and energy expenditure is sensitive to slight alterations in thyroid function. This means that timing and magnitude of cold adaptation would to some extent depend on thyroid function. Local thyroid hormone metabolism is important for energy expenditure and dissipation of heat in special tissues. Recruitment of brown adipocytes and upregulation of uncoupling protein 1 in mitochondria depends on high tissue T₃ concentrations. Most of this T₃ is derived from local 5' deiodination of T₄. Brown fat is vital for cold exposed mice and rats, and may be important for temperature adaptation in human neonates. The role of thyroid hormone metabolism in adult human cold adaptation has not been finally clarified. Hypothetically, cold exposure may enhance T₃ production by deiodination of T₄ in skeletal muscle, which may enhance heat production in muscle via a change in muscle fiber type. Another hypothetical possibility is recruitment of brown adipocytes embedded in white adipose tissue in human adults. Understanding cold adaptation in human adults may lead to development of new drugs against obesity.

Key words

Arctic residence - Brown adipose tissue - Cold adaptation - Obesity - Thyroid hormone metabolism - Uncoupling protein

References

• 1 Nicholls D G, Locke R M. Thermogenic mechanisms in brown fat.  Physiol Rev. 1984;  64 1-64
• 2 Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance.  Physiol Rev. 2004;  84 277-359
• 3 Smith R E, Hoijer D J. Metabolism and cellular function in cold acclimation.  Physiol Rev. 1962;  42 60-142
• 4 Al-Adsani H, Hoffer L J, Silva J E. Resting energy expenditure is sensitive to small dose changes in patients on chronic thyroid hormone replacement.  J Clin Endocrinol Metab. 1997;  82 1118-1125
• 5 Silva J E. The thermogenic effect of thyroid hormone and its clinical implications.  Ann Intern Med. 2003;  139 205-213
• 6 Nedergaard J, Lindberg O. Norepinephrine-stimulated fatty-acid release and oxygen consumption in isolated hamster brown-fat cells. Influence of buffers, albumin, insulin and mitochondrial inhibitors.  Eur J Biochem. 1979;  95 139-145
• 7 Garlid K D, Jaburek M, Jezek P. The mechanism of proton transport mediated by mitochondrial uncoupling proteins.  FEBS Lett. 1998;  438 10-14
• 8 Sellers E A, You S S. Role of the thyroid in metabolic responses to a cold environment.  Am J Physiol. 1950;  163 81-91
• 9 Silva J E, Larsen P R. Adrenergic activation of triiodothyronine production in brown adipose tissue.  Nature. 1983;  305 712-713
• 10 Silva J E, Larsen P R. Potential of brown adipose tissue type II thyroxine 5'-deiodinase as a local and systemic source of triiodothyronine in rats.  J Clin Invest. 1985;  76 2296-2305
• 11 Bianco A C, Salvatore D, Gereben B, Berry M J, Larsen P R. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases.  Endocr Rev. 2002;  23 38-89
• 12 De Jesus L A, Carvalho S D, Ribeiro M O, Schneider M, Kim S W, Harney J W, Larsen P R, Bianco A C. The type 2 iodothyronine deiodinase is essential for adaptive thermogenesis in brown adipose tissue.  J Clin Invest. 2001;  108 1379-1385
• 13 Ribeiro M O, Carvalho S D, Schultz J J, Chiellini G, Scanlan T S, Bianco A C, Brent G A. Thyroid hormone sympathetic interaction and adaptive thermogenesis are thyroid hormone receptor isoform specific.  J Clin Invest. 2001;  108 97-105
• 14 Golozoubova V, Gullberg H, Matthias A, Cannon B, Vennstrom B, Nedergaard J. Depressed thermogenesis but competent brown adipose tissue recruitment in mice devoid of all hormone-binding thyroid hormone receptors.  Mol Endocrinol. 2004;  18 384-401
• 15 Pazos-Moura C C, Moura E G, Dorris M L, Rehnmark S, Melendez L, Silva J E, Taurog A. Effect of iodine deficiency and cold exposure on thyroxine 5’-deiodinase activity in various rat tissues.  Am J Physiol. 1991;  260 175-182
• 16 Zaninovich A A, Rebagliati I, Raices M, Ricci C, Hagmuller K. Mitochondrial respiration in muscle and liver from cold-acclimated hypothyroid rats.  J Appl Physiol. 2003;  95 1584-1590
• 17 Golozoubova V, Hohtola E, Matthias A, Jacobsson A, Cannon B, Nedergaard J. Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold.  FASEB J. 2001;  15 2048-2050
• 18 Jung R T, Leslie P, Nicholls D G, Cunningham S, Isles T E. Energy expenditure in normal and diabetic man: the role of brown adipose tissue.  Health Bull (Edinb). 1988;  46 55-62
• 19 Depocas F. Chemical thermogenesis in the functionally eviscerated cold-acclimated rat.  Can J Med Sci. 1958;  36 691-699
• 20 Boss O, Samec S, Paoloni-Giacobino A, Rossier C, Dulloo A, Seydoux J, Muzzin P, Giacobino J P. Uncoupling protein-3: a new member of the mitochondrial carrier family with tissue-specific expression.  FEBS Lett. 1997;  408 39-42
• 21 Larkin S, Mull E, Miao W, Pittner R, Albrandt K, Moore C, Young A, Denaro M, Beaumont K. Regulation of the third member of the uncoupling protein family, UCP3, by cold and thyroid hormone.  Biochem Biophys Res Commun. 1997;  240 222-227
• 22 Lean M EJ. Brown adipose tissue in humans.  Proc Nutr Soc. 1989;  48 243-256
• 23 Burrow G N, Fisher D A, Larsen P R. Maternal and fetal thyroid function.  N Engl J Med. 1994;  331 1072-1078
• 24 Oden J, Freemark M. Thyroxine supplementation in preterm infants: critical analysis.  Curr Opin Pediatr. 2002;  14 447-452
• 25 Garruti G, Ricquier D. Analysis of uncoupling protein and its mRNA in adipose tissue deposits of adult humans.  Int J Obes Relat Metab Disord. 1992;  16 383-390
• 26 Ricquier D, Nechad M, Mory G. Ultrastructural and biochemical characterization of human brown adipose tissue in pheochromocytoma.  J Clin Endocrinol Metab. 1982;  54 803-807
• 27 Paakkonen T, Leppaluoto J. Cold exposure and hormonal secretion: a review.  Int J Circumpolar Health. 2002;  61 265-276
• 28 Nagata H, Izumiyama T, Kamata K, Kono S, Yukimura Y. An increase of plasma triiodothyronine concentration in man in a cold environment.  J Clin Endocrinol Metab. 1976;  43 1153-1156
• 29 Reed H L, Brice D, Shakir K M, Burman K D, D’Alesandro M M, O’Brian J T. Decreased free fraction of thyroid hormones after prolonged Antarctic residence.  J Appl Physiol. 1990;  69 1467-1472
• 30 Leppaluoto J, Sikkila K, Hassi J. Seasonal variation of serum TSH and thyroid hormones in males living in subarctic environmental conditions.  Int J Circumpolar Health. 1998;  57 383-385
• 31 Sawhney R C, Malhotra A S, Nair C S, Bajaj A C, Rajan K C, Pal K, Prasad R, Basu M. Thyroid function during a prolonged stay in Antarctica.  Eur J Appl Physiol Occup Physiol. 1995;  72 127-133
• 32 Do N V, Mino L, Merriam G R, LeMar H, Case H S, Palinkas L A, Reedy K, Reed H L. Elevation in serum thyroglobulin during prolonged Antarctic residence: effect of thyroxine supplement in the polar 3,5,3’-triiodothyronine syndrome.  J Clin Endocrinol Metab. 2004;  89 1529-1533
• 33 Reed H L, Silverman E D, Shakir K M, Dons R, Burman K D, O’Brian J T. Changes in serum triiodothyronine (T3) kinetics after prolonged Antarctic residence: the polar T3 syndrome.  J Clin Endocrinol Metab. 1990;  70 965-974
• 34 Laurberg P. Thyroxine and 3,5,3'-triiodothyronine content of thyroglobulin in thyroid needle aspirates in hyperthyroidism and hypothyroidism.  J Clin Endocrinol Metab. 1987;  64 969-974
• 35 Laurberg P, Jakobsen P E, Hoeck H C, Vestergaard P. Growth hormone and thyroid function: is secondary thyroid failure underdiagnosed in growth hormone deficient patients?.  Thyroidology. 1994;  6 73-79
• 36 Reed H L, Quesada M, Hesslink R L Jr, D’Alesandro M M, Hays M T, Christopherson R J, Turner B V, Young B A. Changes in serum triiodothyronine kinetics and hepatic type I 5'-deiodinase activity of cold-exposed swine.  Am J Physiol. 1994;  266 786-795
• 37 Wassen F W, Klootwijk W, Kaptein E, Duncker D J, Visser T J, Kuiper G G. Characteristics and thyroid state-dependent regulation of iodothyronine deiodinases in pigs.  Endocrinology. 2004;  145 4251-4263
• 38 De Meis L. Role of the sarcoplasmic reticulum Ca2+-ATPase on heat production and thermogenesis.  Biosci Rep. 2001;  21 113-137
• 39 Everts M E. Effects of thyroid hormones on contractility and cation transport in skeletal muscle.  Acta Physiol Scand. 1996;  156 325-333
• 40 Clausen T, Van Hardeveld C, Everts M E. Significance of cation transport in control of energy metabolism and thermogenesis.  Physiol Rev. 1991;  71 733-774
• 41 Simonides W S, Thelen M H, van der Linden C G, Muller A, van Hardeveld C. Mechanism of thyroid-hormone regulated expression of the SERCA genes in skeletal muscle: implications for thermogenesis.  Biosci Rep. 2001;  21 139-154
• 42 Reis M, Farage M, de Meis L. Thermogenesis and energy expenditure: control of heat production by the Ca(2+)-ATPase of fast and slow muscle.  Mol Membr Biol. 2002;  19 301-310
• 43 Hosoi Y, Murakami M, Mizuma H, Ogiwara T, Imamura M, Mori M. Expression and regulation of type II iodothyronine deiodinase in cultured human skeletal muscle cells.  J Clin Endocrinol Metab. 1999;  84 3293-3300
• 44 Himms-Hagen J. Exercise in a pill: feasibility of energy expenditure targets.  Curr Drug Targets CNS Neurol Disord. 2004;  3 389-409
• 45 Magnus-Levy A. Ueber den respiratorischen Gaswechsel unter dem Einfluss der Thyreoidea sowie unter verschiedenen pathologischen Zustaenden.  Berliner Klinische Wochenschrift. 1895;  30 650-652