Decreased Serum T3 after an Exercise Session is Independent of Glucocorticoid Peak

R. A. L. Neto; M. C. de Souza dos Santos; I. F. Rangel; M. B. Ribeiro; J. P. A. Cavalcanti-de-Albuquerque; A. C. F. Ferreira; L. C. Cameron; D. P. Carvalho; J. P. S. Werneck de Castro

doi:10.1055/s-0033-1351279

Hormone and Metabolic Research, Table of Contents

Horm Metab Res 2013; 45(12): 893-899
DOI: 10.1055/s-0033-1351279

Humans, Clinical

Decreased Serum T3 after an Exercise Session is Independent of Glucocorticoid Peak

R. A. L. Neto

¹Laboratório de Biologia do Exercício, Escola de Educação Física e Desportos, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

²Laboratório de Fisiologia Endócrina Doris Rosenthal, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

M. C. de Souza dos Santos

²Laboratório de Fisiologia Endócrina Doris Rosenthal, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

I. F. Rangel

¹Laboratório de Biologia do Exercício, Escola de Educação Física e Desportos, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

M. B. Ribeiro

¹Laboratório de Biologia do Exercício, Escola de Educação Física e Desportos, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

J. P. A. Cavalcanti-de-Albuquerque

¹Laboratório de Biologia do Exercício, Escola de Educação Física e Desportos, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

²Laboratório de Fisiologia Endócrina Doris Rosenthal, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

A. C. F. Ferreira

²Laboratório de Fisiologia Endócrina Doris Rosenthal, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

L. C. Cameron

³Laboratório de Bioquímica de Proteínas, UNIRIO, Rio de Janeiro, Brazil

,

D. P. Carvalho

²Laboratório de Fisiologia Endócrina Doris Rosenthal, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

J. P. S. Werneck de Castro

¹Laboratório de Biologia do Exercício, Escola de Educação Física e Desportos, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

³Laboratório de Bioquímica de Proteínas, UNIRIO, Rio de Janeiro, Brazil

› Author Affiliations

Abstract

Physical exercise increases serum glucocorticoids, which is believed to be involved in the fall of T3 after high intensity exercise. The objective was to evaluate whether a physical exercise session alters the thyroid economy and adrenal axis in humans, and the possible role of corticosteroids in thyroid function disturbance. Active but not athlete subjects were enrolled in an open field competition and cortisol, TSH, T3, and T4 were measured before and after the race. To give new insights into the mechanisms underlying the changes in thyroid economy after exercise, we used a rat model to evaluate the impact of blocking corticosterone synthesis during treadmill exercise by metyrapone administration. Cortisol levels increased 1.5-fold (from 28.2±3.8 to 42.2±2.2 μg/dl; p<0.05), while serum T3 decreased by 13% (from 115±5 to 99±5 μg/dl; p<0.05) 6 h after the race in humans. Also, in rats, glucocorticoid increased by 2-fold while T3 decreased 15% after exercise session (p<0.05). However, the complete blockage of corticosterone peak did not impair serum T3 decrease observed in rats submitted to exercise. Interestingly, the lack of corticosterone peak led not only to lower serum T3, but also to decreased serum T4, indicating that corticosterone might be fundamental for the maintenance of serum thyroid hormone levels after high intensity exercise. Although cortisol increases and T3 decreases after high intensity exercise in both humans and rats, it does not seem to be a cause-effect response since pharmacological blockage of corticosterone peak does not modulate T3 response.

Key words

thyroid hormones - deiodinase - glucocorticoids - high intensity exercise

Full Text

References

References
1 Mastorakos G, Pavlatou M. Exercise as a stress model and the interplay between the hypothalamus-pituitary-adrenal and the hypothalamus-pituitary-thyroid axes. Horm Metab Res 2005; 37: 577-584
2 Gereben B, Zavacki AM, Ribich S, Kim BW, Huang SA, Simonides WS, Zeold A, Bianco AC. Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocr Rev 2008; 29: 898-938
3 Simonides WS, van Hardeveld C. Thyroid hormone as a determinant of metabolic and contractile phenotype of skeletal muscle. Thyroid 2008; 18: 205-216
4 Olivares EL, Marassi MP, Fortunato RS, da Silva AC, Costa-e-Sousa RH, Araujo IG, Mattos EC, Masuda MO, Mulcahey MA, Huang SA, Bianco AC, Carvalho DP. Thyroid function disturbance and type 3 iodothyronine deiodinase induction after myocardial infarction in rats a time course study. Endocrinology 2007; 148: 4786-4792
5 Bianco AC. Minireview: cracking the metabolic code for thyroid hormone signaling. Endocrinology 2011; 152: 3306-3311
6 Drigo RA, Fonseca TL, Werneck-de-Castro JP, Bianco AC. Role of the type 2 iodothyronine deiodinase (D2) in the control of thyroid hormone signaling. Biochim Biophys Acta 2013; 1830: 3956-3964
7 Maia AL, Kim BW, Huang SA, Harney JW, Larsen PR. Type 2 iodothyronine deiodinase is the major source of plasma T3 in euthyroid humans. J Clin Invest 2005; 115: 2524-2533
8 Grozovsky R, Ribich S, Rosene ML, Mulcahey MA, Huang SA, Patti ME, Bianco AC, Kim BW. Type 2 deiodinase expression is induced by peroxisomal proliferator-activated receptor-gamma agonists in skeletal myocytes. Endocrinology 2009; 150: 1976-1983
9 Heemstra KA, Soeters MR, Fliers E, Serlie MJ, Burggraaf J, van Doorn MB, van der Klaauw Romijn JA, Smit JW, Corssmit EP, Visser TJ. Type 2 iodothyronine deiodinase in skeletal muscle: effects of hypothyroidism and fasting. J Clin Endocrinol Metab 2009; 94: 2144-2150
10 Wilber JF, Utiger RD. The effect of glucocorticoids on thyrotropin secretion. J Clin Invest 1969; 48: 2096-2103
11 Bianco AC, Nunes MT, Hell NS, Maciel RM. The role of glucocorticoids in the stress-induced reduction of extrathyroidal 3,5,3′-triiodothyronine generation in rats. Endocrinology 1987; 120: 1033-1038
12 Ciloglu F, Peker I, Pehlivan A, Karacabey K, Ilhan N, Saygin O, Ozmerdivenli R. Exercise intensity and its effects on thyroid hormones. Neuro Endocrinol Lett 2005; 26: 830-834
13 Fortunato RS, Ignacio DL, Padron AS, Pecanha R, Marassi MP, Rosenthal D, Werneck-de-Castro JP, Carvalho DP. The effect of acute exercise session on thyroid hormone economy in rats. J Endocrinol 2008; 198: 347-353
14 Hackney AC, Kallman A, Hosick KP, Rubin DA, Battaglini CL. Thyroid hormonal responses to intensive interval versus steady-state endurance exercise sessions. Hormones (Athens) 2012; 11: 54-60
15 Rone JK, Dons RF, Reed HL. The effect of endurance training on serum triiodothyronine kinetics in man: physical conditioning marked by enhanced thyroid hormone metabolism. Clin Endocrinol (Oxf) 1992; 37: 325-330
16 Matthews CE, Heil DP, Freedson PS, Pastides H. Classification of cardiorespiratory fitness without exercise testing. Med Sci Sports Exerc 1999; 31: 486-493
17 Cunha FA, Midgley AW, Monteiro WD, Farinatti PT. Influence of cardiopulmonary exercise testing protocol and resting VO(2) assessment on %HR(max), %HRR, %VO(2max) and %VO(2)R relationships. Int J Sports Med 2010; 31: 319-326
18 Toyoda N, Yasuzawa-Amano S, Nomura E, Yamauchi A, Nishimura K, Ukita C, Morimoto S, Kosaki A, Iwasaka T, Harney JW, Larsen PR, Nishikawa M. Thyroid hormone activation in vascular smooth muscle cells is negatively regulated by glucocorticoid. Thyroid 2009; 19: 755-763
19 Berry MJ, Banu L, Larsen PR. Type I iodothyronine deiodinase is a selenocysteine-containing enzyme. Nature 1991; 349: 438-440
20 Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254
21 Deligiannis A, Karamouzis M, Kouidi E, Mougios V, Kallaras C. Plasma TSH T3, T4 and cortisol responses to swimming at varying water temperatures. Br J Sports Med 1993; 27: 247-250
22 Kilic M. Effect of fatiguing bicycle exercise on thyroid hormone and testosterone levels in sedentary males supplemented with oral zinc. Neuro Endocrinol Lett 2007; 28: 681-685
23 Huang WS, Yu MD, Lee MS, Cheng CY, Yang SP, Chin HM, Wu SY. Effect of treadmill exercise on circulating thyroid hormone measurements. Med Princ Pract 2004; 13: 15-19
24 Yamaguchi K, Hashiguchi Y. A significant adverse correlation between serum cortisol and TSH in a case of cyclic Cushing’s disease based on a continuous three-year observation. Endocrine Journal 2003; 50: 833-834
25 Walter KN, Corwin EJ, Ulbrecht J, Demers LM, Bennett JM, Whetzel CA, Klein LC. Elevated thyroid stimulating hormone is associated with elevated cortisol in healthy young men and women. Thyroid Res 2012; 5: 13-18
26 Xu X, Ying Z, Cai M, Xu Z, Li Y, Jiang SY, Tzan K, Wang K, Parthasarathy S, He G, Rajagopalan S, Sun Q. Exercise ameliorates high-fat diet-induced metabolic and vascular dysfunction, and increases adipocyte progenitor cell population in brown adipose tissue. Am J Physiol Regul Integr Comp Physiol 2011; 300: R1115-R1125
27 Yoshioka K, Yoshida T, Wakabayashi Y, Nishioka H, Kondo M. Effects of exercise training on brown adipose tissue thermogenesis in ovariectomized obese rats. Endocrinol Jpn 1989; 36: 403-408
28 Ignacio DL, Fortunato RS, Neto RA, da Silva Silvestre DH, Nigro M, Frankenfeld TG, Werneck-de-Castro JP, Carvalho DP. Blunted Response of Pituitary Type 1 and Brown Adipose Tissue Type 2 Deiodinases to Swimming Training in Ovariectomized Rats. Horm Metab Res 2012; 44: 479-803
29 De Matteis R, Lucertini F, Guescini M, Polidori E, Zeppa S, Stocchi V, Cinti S, Cuppini R. Exercise as a new physiological stimulus for brown adipose tissue activity. Nutr Metab Cardiovasc Dis 2013; 23: 582-590
30 Sullo A, Brizzi G, Maffulli N. Deiodinating activity in the brown adipose tissue of rats following short cold exposure after strenuous exercise. Physiol Behav 2003; 80: 399-403
31 Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng YH, Doria A, Kolodny GM, Kahn CR. Identification and importance of brown adipose tissue in adult humans. N Engl J Med 2009; 360: 1509-1517
32 Lee P, Zhao JT, Swarbrick MM, Gracie G, Bova R, Greenfield JR, Freund J, Ho KK. High prevalence of brown adipose tissue in adult humans. J Clin Endocrinol Metab 2011; 96: 2450-2455
33 van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P, Teule GJ. Cold-activated brown adipose tissue in healthy men. N Engl J Med 2009; 360: 1500-1508
34 Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerback S, Nuutila P. Functional brown adipose tissue in healthy adults. N Engl J Med 2009; 360: 1518-1525