Elsevier

Physiology & Behavior

Volume 80, Issues 2–3, November 2003, Pages 399-403
Physiology & Behavior

Deiodinating activity in the brown adipose tissue of rats following short cold exposure after strenuous exercise

https://doi.org/10.1016/j.physbeh.2003.09.005Get rights and content

Abstract

Interscapular brown adipose tissue (IBAT) activity is controlled by the sympathetic nervous system, and factors that influence thermogenesis appear to act centrally to modify the sympathetic outflow to IBAT. Cold exposure produces a rise in IBAT temperature as a result of the increase in sympathetic outflow to IBAT. This is associated with an increased thyroid activity. 3,5,3′-triiodothyronine (T3) and T4 levels increase during strenuous exercise, and, at the end of the exercise bout, a decrease of T3 and T4 levels, with an increase in TSH during the following 4–5 days, is seen. We evaluated the effect of strenuous exercise on 5′-deiodinase (5′-D) activity in IBAT in normal environmental conditions and after short (30 min) cold exposure. 5′-D activity is lower in rats at basal condition. Short cold exposure (SCE) increases 5′-D in IBAT both in exercising rats and in sedentary rats. However, this increase is lower in exercising animals. Strenuous exercise can reduce 5′-D activity in normal environmental conditions and after SCE. Probably, other compensatory mechanisms of heat production are active in exercising rodents.

Introduction

Brown adipose tissue (BAT) is responsible for most of the increase in metabolic heat following various experimental manipulations in rodents [5], [7]. Interscapular BAT (IBAT) is supplied by a mixed nerve, which provides five separate branches to the individual lobes of IBAT. The thermogenic activity of IBAT is controlled by the sympathetic nervous system [14], and factors that influence thermogenesis appear to act centrally to modify the sympathetic outflow to IBAT [22]. Thyroid hormones closely regulate thermogenesis in BAT. Cold exposure and cafeteria diet produce a rise in the temperature of BAT. This is associated with increased thyroid activity, elevated serum level of 3,5,3′-triiodothyronine (T3), and increased rate of T3 production.

There is a close synergistic relationship between sympathetic nervous system and thyroid hormone metabolism in BAT. Indeed, type II 5′-deiodinase (5′-D) found in BAT is under the control of the sympathetic nervous system [24]. Type II 5′-D is different from the 5′-D found in the kidney and the liver, and is similar to the 5′-D found in the brain and the heart [1]. An injection of neostigmine in the hippocampus causes increased thermogenesis, with raised 5′-D activity in IBAT, but not in the liver and kidneys [18]. This suggests that the higher serum levels of T3 result from T4-to-T3 conversion in BAT, and confirms that T3 produced in BAT stimulates the thermogenic response of that tissue [8]. Also, the activation of type II 5′-D is probably dependent specifically on the sympathetic innervation in BAT. Cold-induced stimulation of 5′-D might modify thermogenesis in tissues other than BAT by providing T3 [13].

We have recently demonstrated that cold exposure (4 °C) increases 5′-D activity of BAT maximally after 4 h. This effect was already evident after just 30 min, confirming the key role of BAT in rapid cold adaptive mechanism to produce supplementary heat [3].

The effects of exercise on thermogenesis induced by increased rate of T4-to-T3 conversion are unclear. Strenuous exercise increases T3 and T4 levels during the exercise bout. At the end of the exercise, T3 and T4 levels decrease, and TSH increases for 4–5 days [21]. There are controversies about the changes of TSH levels induced by exercise. During and after low-intensity submaximal exercise, there are no variations of TSH levels [6], [25]. Another study showed a continuous increment of TSH levels both during long duration submaximal exercise and after 15 min, contrasting with a decrease during maximal exercise [23].

Short cold exposure (SCE) (30 min) by fast transfer of experimental animals from an adaptation room at 30 °C to a cold room at 4 °C for 30 min [4], [11] rapidly increases TRH production, thus enhancing thyroid function by stimulating TSH production. SCE up-regulates the hypothalamus–pituitary–thyroid axis, increasing the production of TRH. Through it, the thyroid is stimulated to produce T3. In these conditions, it is possible to better ascertain the influence of cold or other factors on this regulation system.

Moriya [19] studied the effects of exercise on the disappearance of cold adaptability in rats. He found that exercising animals showed no decrease in enhanced nonshivering thermogenesis, but did show a decrease in BAT weight as compared with sedentary rats. Also, plasma levels of T3 were higher in cold-adapted animals than in de-adapted rats with or without exercise load [19]. Also, functional TSH receptors have been demonstrated in BAT, and may be involved in the regulation of the expression of type II 5′-D [20].

In general, the separate effects of exercise and cold exposure have been examined in detail concerning the effect of each stressor on, for example, thermoregulation, hormone secretion and various substrates. However, there is still information lacking of the interaction between these two stressors and of the more precise mechanisms controlling for thermoregulation. Therefore, in this study, we hypothesised that strenuous exercise modifies T3 production in IBAT through changes in 5′-D activity in normal environmental conditions and after SCE (30 min).

Section snippets

Material and methods

All procedures were carried out according to the policy statement of the American College of Medicine after approval of the Ethics Committee of the Second University of Naples, Faculty of Medicine and Surgery.

Results

Fig. 1 shows that the serum levels of T3 were significantly lower in exercising than in nonexercising rats. However, this decrease was more evident in control animals than in the rats treated with SCE. Two-way analysis of variance showed significant effects for SCE [F(1,10)=77.146, P<.01], for exercise [F(1,10)=77.278, P<0.01] and for the interaction Exercise×SCE [F(8,80)=19.934, P<.01]. The post hoc test showed a significant difference between NT and ET (P<.01), NT and EC (P<.01), ET and NC (P

Discussion

Swimming is stressful and causes marked functional changes. In thermoneutral water, swimming produces adaptive changes similar to running and those produced by cold acclimatisation [10]. Also, the adaptations in thermoneutral water are similar to those from swimming in cold water [10]. This suggests that changes are due to the physical activity per se, and only partially depend on the temperature. For example, Harri et al. [9] examined the separate and combined effects of exercise and cold

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