Blunted Response of Pituitary Type 1 and Brown Adipose Tissue Type 2 Deiodinases to Swimming Training in Ovariectomized Rats

D. L. Ignacio; R. S. Fortunato; R.A. L. Neto; D. H. da Silva Silvestre; M. Nigro; T.G. P. Frankenfeld; J.P. S. Werneck-de-Castro; D. P. Carvalho

doi:10.1055/s-0032-1314875

Hormone and Metabolic Research, Inhaltsverzeichnis

Horm Metab Res 2012; 44(11): 797-803
DOI: 10.1055/s-0032-1314875

Original Basic

Blunted Response of Pituitary Type 1 and Brown Adipose Tissue Type 2 Deiodinases to Swimming Training in Ovariectomized Rats

D. L. Ignacio

¹Laboratório de Fisiologia Endócrina Doris Rosenthal, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

R. S. Fortunato

¹Laboratório de Fisiologia Endócrina Doris Rosenthal, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

R.A. L. Neto

²Laboratório de Biologia do Exercício, Escola de Educação Física e Desportos, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

D. H. da Silva Silvestre

²Laboratório de Biologia do Exercício, Escola de Educação Física e Desportos, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

M. Nigro

³Laboratório de Bioenergética, Instituto de Bioquímica Médica, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

T.G. P. Frankenfeld

¹Laboratório 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

²Laboratório de Biologia do Exercício, Escola de Educação Física e Desportos, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

,

D. P. Carvalho

¹Laboratório de Fisiologia Endócrina Doris Rosenthal, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

› Institutsangaben

Abstract

Ovariectomy leads to significant increase in body weight, but the possible peripheral mechanisms involved in weight gain are still unknown. Since exercise and thyroid hormones modulate energy balance, we aimed to study the effect of swimming training on body weight gain and brown adipose tissue (BAT) type 2 iodothyronine deiodinase responses in ovariectomized (Ox) or sham-operated (Sh) rats. Rats were submitted to a period of 8-week training, 5 days per week with progressive higher duration of exercise protocol. Swimming training program did not totally prevent the higher body mass gain that follows ovariectomy in rats (16.5% decrease in body mass gain in Ox trained rats compared to 22% decrease in sham operated trained animals, in relation to the respective sedentary groups), but training of Ox animals impaired the accumulation of subcutaneous fat pads. Interestingly, swimming training upregulates pituitary type 1 (p<0.001 vs. all groups) and BAT type 2 iodothyronine deiodinases (p<0.05 vs. ShS and OxS) in sham operated but not in Ox rats, indicating an impaired pituitary and peripheral response to exercise in Ox rats. However, BAT mitochondrial O₂ consumption significantly increased by swimming training in both sham and Ox groups, indicating that Ox BAT mitochondria responds normally to exercise stimulus, but does not result in a significant reduction of body weight. In conclusion, increased body mass gain produced by Ox is not completely impaired by 8 weeks of high intensity physical training, showing that these animals sustain higher rate of body mass gain independent of being submitted to higher energy expenditure.

Key words

deiodinase - physical exercise - ovariectomy - body mass

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Referenzen

References
1 Richard D, Rochon L, Deshaies Y. Effects of exercise training on energy balance of ovariectomized rats. Am J Physiol 1987; 253 (5 Pt 2) R740-R745
2 Marassi MP, Fortunato RS, Matos da Silva AC, Pereira VS, Carvalho DP, Rosenthal D, Correa da Costa VM. Sexual dimorphism in thyroid function and type 1 iodothyronine deiodinase activity in pre-pubertal and adult rats. J Endocrinol 2007; 192: 121-130
3 Percegoni N, Ferreira AC, Rodrigues CF, Rosenthal D, Castelo Branco MT, Rumjane VM. Profile of serum IL-1beta and IL-10 shortly after ovariectomy and estradiol replacement in rats. Horm Metab Res 2009; 41: 50-54
4 Rogers NH, Perfield II JW, Strissel KJ, Obin MS, Greenberg AS. Reduced Energy Expenditure and Increased Inflammation Are Early Events in the Development of Ovariectomy-Induced Obesity. Endocrinology 2009; 150: 2161-2168
5 Heine PA, Taylor JA, Iwamoto GA, Lubahn DB, Cooke PS. Increased adipose tissue in male and female estrogen receptor α knockout mice. Proc Natl Acad Sci USA 2000; 97: 12729-12734
6 Wade GN, Gray JM, Bartness TJ. Gonadal influences on adiposity. Inter J Obes 1985; 9 (Suppl. 01) 83-92
7 Richard D. Effects of ovarian hormones on energy balance and brown adipose tissue thermogenesis. Am J Physiol 1986; 250 (2 Pt 2) R245-R249
8 Shimomura Y, Shimizu H, Takashashi M, Sato N, Uehara Y, Fukatsu A, Negishi M, Kobayashi I, Kobayashi S. The significance of decreased ambulatory activity during the generation by long-term observation of obesity in ovariectomized rats. Physiol Behav 1990; 47: 155-159
9 Di Pietro L, Dziura J, Blair SN. Estimated change in physical activity levels (PAL) and prediction of 5-year weight change in men: the aerobics center longitudinal study. Int J Obes Relat Metab Disord 2004; 28: 1541-1547
10 Melton SA, Hegsted M, Keenan MJ, Zhang Y, Morris S, Potter BL, O’Neil CE, Morris GS. Swimming eliminates the weight gain and abdominal fat associated with ovariectomy in the retired breeder rat despite high-fat diet selection. Appetite 2000; 35: 1-7
11 Van Do N, LeMar H, Reed HL. Thyroid hormone responses to environmental cold exposure and seasonal changes: a proposed model. Endocrinol Metab 1996; 3: 7-16
12 Himms Hagen J. Does thermoregulatory feeding occur in newborn infants? A novel view of the role of brown adipose tissue thermogenesis in control of food intake. Obes Res 1995; 3: 361-369
13 Silva JE. Thyroid hormone control of thermogenesis and energy balance. Thyroid 1995; 5: 481-492
14 McArdle WD. Metabolic stress of endurance swimming in the laboratory rat. J Appl Physiol 1967; 22: 50-54
15 Leshner AL, Litwin VA. A simple method for carcass analysis. Physiol Behav 1972; 9: 282-289
16 Bradford MM. A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the protein-dye binding. Anal Biochem 1976; 72: 248-252
17 Berry MJ, Kieffer JD, Harnet JW, Larsen PR. Selenocysteine confers the biochemical properties characteristic of the type I iodothyronine deiodinase. J Biol Chem 1991; 266: 14155-14158
18 Fortunato RS, Ignacio DL, Padron AS, Ribeiro R, Marassi M, Rosenthal D, Werneck-de-Castro JP, Carvalho DP. The effect of acute exercise session on thyroid hormone economy in rats. J Endocrinol 2008; 198: 1-8
19 de Meis L, Ketzer LA, da Costa RM, de Andrade IR, Benchimol M. Fusion of the endoplasmic reticulum and mitochondrial outer membrane in rats brown adipose tissue: activation of thermogenesis by Ca2. PLoS One 2010; 5: e9439
20 Shabalina IG, Ost M, Petrovic N, Vrbacky M, Nedergaard J, Cannon B. Uncoupling protein-1 is not leaky. Biochim Biophys Acta. 2010 1797. 773-784
21 Haufe S, Engeli S, Budziarek P, Utz W, Schulz-Menger J, Hermsdorf M, Wiesner S, Otto C, Fuhrmann JC, Luft FC, Boschmann M, Jordan J. Determinants of exercise-induced fat oxidation in obese women and men. Horm Metab Res 2010; 42: 215-221
22 Meredidt CN, Frontera WR, Fisher EC, Hughes VA, Herland JC, Edwards J, Evans WJ. Peripheral effects of endurance training in young and old subjects. J Appl Physiol 1989; 66: 2844-2849
23 Hashimoto T, Brooks GA. Mitochondrial lactate oxidation complex and an adaptive role for lactate production. Med Sci Sports Exerc 2008; 40: 486-494
24 Campbell SE, Febbraio MA. Effect of ovarian hormones on mitochondrial enzyme activity in the fat oxidation pathway of skeletal muscle. Am J Physiol Endocrinol Metab 2001; 281: E803-E808
25 Shinoda M, Latour MG, Lavoie J-M. Effects of physical training on body composition and organ weights in ovariectomized and hyperestrogenic rats. Int J Obes 2002; 26: 335-343
26 Klem ML, Wing RR, McGuire MT, Seagle HM, Hill JO. Psychological symptoms in individuals successful at long-term maintenance of weight loss. Health Psychol 1998; 17: 336-345
27 Gwinup G. Weight loss without dietary restriction: efficacy of different forms of aerobic exercise. Am J Sports Med 1987; 15: 275-279
28 Sene-Fiorese M, Duarte FO, Scarmagnani FR, Cheik NC, Manzoni MS, Nonaka KO, Rossi EA, de Oliveira Duarte AC, Dâmaso AR. Efficiency of intermittent exercise on adiposity and fatty liver in rats fed with high-fat diet. Obesity 2008; 16: 2217-2222
29 Després JP, Lemieux I, Bergeron J, Pibarot P, Mathieu P, Larose E, Rodés-Cabau J, Bertrand OF, Poirier P. Abdominal obesity and the metabolic syndrome: contribution to global cardiometabolic risk. Arterioscler Thromb Vasc Biol 2008; 28: 1039-1049
30 Ricquier D. Respiration uncoupling and metabolism in the control of energy expenditure. Proc Nutr Soc 2005; 64: 47-52
31 Lowell BB, Spiegelman BM. Towards a molecular understanding of adaptive thermogenesis. Nature 2000; 404 (6778) 652-660
32 Pedersen SB, Bruun JM, Kristensen K, Richelsen B. Regulation of UCP1, UCP2, and UCP3 m RNA expression in brown adipose tissue, white adipose tissue and skeletal muscle in rats by estrogen. Biochem Biophys Res Commun 2001; 288: 191-197
33 Yoshioka K, Yoshida T, Wakabayashi Y, Nishioka H, Kondo M. Reduced Brown Adipose Tissue Thermogenesis of Obese Rats After Ovariectomy. Endocrinol Jpn 1988; 35: 537-543
34 Boss O, Samec S, Desplanches D, Mayet MH, Seydoux J, Muzzin P, Giacobino JP. Effect of endurance training on mRNA expression of uncoupling proteins 1, 2 and 3 in the rat. FASEB J 1988; 12: 335-339
35 Larue-Achagiotis C, Rieth N, Goubern M, Laury MC, Louis-Sylvestre J. Exercise-Training Reduced BAT Thermogenesis in Rat. Physiol Behav 1994; 57: 1013-1017
36 Sullo A, Brizzi G, Maffulli N. Triiodothyronine deiodinating activity in brown adipose tissue after short cold stimulation test in trained and untrained rats. Physiol Res 2004; 53: 69-76
37 Yoshioka K, Yoshida T, Wakabayashi Y, Nishioka H, Kondo M. Effect of Exercise Training on Brown Adipose Tissue Thermogenesis in Ovariectomized Obese Rats. Endocrinol Jpn 1989; 36: 403-408
38 Hirata K. Blood flow to brown adipose tissue and norepinephrine-induced calorigenesis in physically trained rats. Jpn J Physiol 1982; 32: 279-291
39 Bianco AC, Maia AL, da Silva WS, Christoffolete MA. Adaptive activation of thyroid hormone and energy expenditure. Biosci Rep 2005; 25: 191-208
40 Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr Rev 2002; 23: 38-89