Effect of diet and exercise on norepinephrine- induced thermogenesis in male … › ... › files › anexos › php735cda_6454.pdf · 2012-04-09 · Effect of diet and exercise

Effect of diet and exercise on norepinephrine- induced thermogenesis in male and female rats

JACQUES LEBLANC, JEAN DUSSAULT, DIANE LUPIEN, AND DENIS RICHARD Department of Physiology, School of Medicine, Lava1 University, Quebec City, Quebec, GIK 7P4, Canada

LEBLANC, JACQUES, JEAN DUSSAULT, DIANE LUPIEN, AND DENIS RICHARD. Effect of diet and exercise on norepinephrine- induced thermogenesis in male and female rats. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 52(3): 556-561, 1982.-Male and female rats were fed standard laboratory chow or a highly palatable diet (cafeteria diet) for 10 wk. The cafeteria diet caused an increase in caloric intake and in body weight, and it induced thermogenesis that was associated with elevated plasma triiodothyronine (Ta) levels, increased brown adipose tissue size, and enhanced metabolic response to norepinephrine. For a comparable caloric intake, body-weight gain was significantly greater in female than in male rats possibly because of difference in thermogenesis as suggested by the response to norepinephrine. Exercise training (swimming 2 h/day for 10 wk) reduced food intake and body-weight gain and failed to increase norepinephrine-induced thermogenesis in rats fed laboratory chow. In animals fed the cafeteria diet, food intake and body-weight gain were also reduced by exercise training, which at the same time diminished the diet-induced thermogenesis as evidenced by the diminution of 1) brown fat hypertrophy, 2) the elevation of plasma T3, and 3) the hyperthermic response to injected norepinephrine. It is suggested that the thyroid hormone and catecholamines through their actions on the brown adipose tissue are the important regulators of thermogenesis. Exercise training would reduce the diet-induced thermogenesis by preventing increased T3 production. Enhanced thermogenesis may be considerd an adaptive reaction as it serves to reduce fat deposition in animals fed cafeteria diet and to promote nonshivering heat production in the cold. On the other hand, exercise training reduces thermogenesis and thus prevents energy wasting.

thyroid hormones; brown adipose tissue

THERMOGENESIS WAS SHOWN TO BE an important factor in the control of energy balance (1, 22). Cold-induced thermogenesis has been known for some time (ll), and the participation of brown adipose tissue in the devel- opment of nonshivering thermogenesis has also been shown by various investigators (10,>13, 20, 33). Excessive food intake was also shown to produce what has been called “dietary-induced thermsgenesis” (22,32). Exercise produces an increased caloric utilization and is sometimes associated with diminution in food intake. However, no studies have been reported on the role of exercise-training in thermogenesis. Thermogenesis has been associated with brown fat hypertrophy (20, 29, 30, 33), increased triiodothyronine secretion (6,16), and enhanced response to the metabolic effect of catecholamines (14,20,29). An

experiment was designed to study the effect of prolonged exercise training on thermogenesis of male and female rats fed either standard laboratory chow or very palatable food called I&cafeteria diet,” which has been shown to induce a significant thermogenesis (29, 30). The thermogenesis measured in our study was that produced by standard norepinephrine injections. It seemed also inter- esting to examine the effect of a sexual difference in thermogenesis because female rats did not lose as much body fat as males when submitted to prolonged training periods (26, 27), and they gained more weight than the male rats when fed a cafeteria diet (31). This raises the possibility of a sexual difference in thermogenesis that was also estimated by the response to norepinephrine.

PROTOCOL

Effects of exercise and diet on hormonal and growth changes. Sedentary and exercise-trained Wistar rats were fed either normal laboratory stock diet (Purina chow) or a special regimen called cafeteria diet (29). A total of four groups of male and four groups of female rats were used and were kept at 27OC throughout the experiment. The average initial body weight of the male rats was 213 g and that of the female rats was 197 g. All groups initially included a total of 15 animals. For two male and two female groups, the exercise training program was the same as the one described previously (27). The rats swam for 2 h, 6 days/wk in an agitated water tank kept at 36OC. During the swimming session the rats carried small loads on their backs corresponding to 2% of their body weight. This period of training lasted 10 wk. When not swimming, these rats were kept in individual cages, along with the other four sedentary groups in a room maintained at 27OC, The four groups of rats on stock diet were fed Purina chow ad libitum. The following procedure was adopted for the groups of rats on the cafeteria diet. These animals were given various food items in excess of predicted requirements. Twice a week all food items consumed by the animals were measured, and this allowed transformation of grams of food into calories consumed. For the other 5 days of the week food consumed per animal was weighted in bulk, and the transformation of grams of food into calories was made on the basis of results obtained for the other 2 days. Consequently the caloric uptake was measured for 2 days and estimated for the other 5 days. The cafeteria diet included two meals that were fed on alternate days. One

556 0161-7567/82/0000-~0$01.25 Copyright 0 1982 the American Physiological Society

DIET, EXERCISE, AND THERMOGENESIS

meal consisted of bologna, fruitcake, popcorn, and laboratory chow and the other of p&G, chocolate chip cookies, sunflower seeds, and laboratory chow. The p&t6 is a mixture of ground pork meat, bread crumbs, and season- ings. The cafeteria diet correspond to an average caloric content of 19.8 kJ/g of wet weight derived from fat (60%), carbohydrate (30%), and protein (10%). The corresponding values for the Purina chow were 14.4 kJ/g derived from fat (Es), carbohydrate (60%), and proteins (28%). The various food items that were very palatable proved to be most efficient in promoting food intake and gain in body weight as was previously described (29, 31). Two days before the end of the experiment, all animals were given a subcutaneous injection of norepinephrine (300 pg/kg) in saline, and colonic temperature was measured before and 1 h after the injection. This allowed a quali- tative estimate of the thermogenic effect of norepinephrine (22). At the end of the experiment, the animals were decapitated and plasma was kept at -40°C for later thyroxine and triiodothyronine determinations. At au- topsy, epididymal fat pads and interscapular brown adipose tissue were dissected and weighed.

Effect of exercise on catecholamines of trained and untrained animals. In a previous unpublished experiment, sedentary and exercise-trained male rats fed stock diet were cannulated in order to draw blood for catecholamine determination. For that purpose, a polyeth- ylene tube was placed permanently into the jugular vein. This tube was exteriorized through a neck incision that allowed blood sampling at rest and during exercise bouts without unduly disturbing the animal. Blood samples (0.4 ml) for determination of epinephrine and norepinephrine were obtained while the animals rested quietly in their cage and while they were swimming at 1.5 h after the beginning of exercise. The catecholamines were de- termined by the radioenzymatic method (B), the thyroxine by the method of Murphy and Jachan (24), and the triiodothyronine by the radioimmunological method of Mitsuma et al. (23). The statistical analysis was per- formed by using the Student’s t test to compare two sets of results and the Duncan multiple-range test for more than two groups (9).

RESULTS

Daily exercise was shown to reduce food intake in male rats fed standard chow or cafeteria diet especially between the 2nd and 8th wks of the experiment (Fig. 1). In the female rats this effect was observed only with the cafeteria diet (Fig. 2). The average body weight of exercised male rats was 75 g less than that of the sedentary animals (Fig. 3). The equivalent difference in the female rats was only, 25 g (Fig. 4). In an attempt to verify these differences in body weight in terms of changes at the level of the white adipose tissue, weights of epididymal and parametrial fat pads were measured. On that basis, the difference in body weight between male and female rats could not be related to these changes in the white adipose tissue because a comparable reduction of ap- proximately 50% in epididymal or parametrial fat pads was found in the exercised animals in spite of a marked difference due to sex with regard to the total body weight (Fig. 5), Body weight increase was greatlv enhanced by

557

the cafeteria diet in both male and female rats, and this was accompanied by a threefold increase in epididymal and parametrial pads. When exercise was combined with the cafeteria diet, the body weight increase was reduced as were the body fat pads in both male and female rats (Figs. 34, Food intake was significantly increased by the cafeteria diet, but this effect was reduced in exercise- trained animals. The difference in weight gain among rats fed the cafeteria and the stock diet was larger in the

MALE RATS

H standard chow (s 1 1

0-0 cafeteria (c)

H s t exercise

m c t exercise

1 I 1 1 1 I I I I I I I80 I 2 3 4 5 6 7 8 9 IO

TIME IN WEEKS

FIG, I, Daily food intake and mean food intake over IO-wk period in male rats fed standard laboratory chow (S) and cafeteria diet (C) with and without exercise (E). For daily food intake, C groups show greater values than S groups (P < O.Ol), For mean food intake C group values are also greater than S groups (P < 0.01) while S > (S + E) and C > (C + E) both with P < 0.01.

FEMALE RATS

stondord chow (s )

cafeteria tc)

s + exercise

c + exercise

I 1 1 1 1 1 1 1 1 1

1 1 2 3 4 5 6 7 8 9 10

TIME IN WEEKS

FIG. 2. Daily food intake and mean food intake over a lo-wk period in female rats fed standard laboratory chow (S) and cafeteria diet (C) with and without exercise (E). For daily food intake, C groups show greater values than S groups (P c 0.01). For mean food intake C group values are also meater than S groups while C > (C + E) with P < 0.01.

558 LEBLANC, DUSSAULT, LUPIEN, AND RICHARD

MALE RATS

H standard chow (s 1

m cofetorio [cl

M s + exercise a c + exercise

20 1 t 1 I 1 I 1 1 t 1 o I 2 3 4 5 6 7 8 9 IO

TIME IN WEEKS

FIG. 3. Variations of body weight of male rats over lo-wk period for 4 groups.

FEMALE RATS

n m stondord chow (s) m cafeteria (c )

M s + exerci

H c + exerci

150 t t 1 1 I k 1 1 t I 0 1 2 3 4 5 6 7 8 9 IO

TtME IN WEEKS

FIG. 4. Variations for 4 groups.

of body weight of female rats over IO-wk period

female (92 g) than in the male rats (51 g), although the equivalent difference in caloric intake, expressed in total kJ for the lo-wk period, was not significantly different between the female (14,700O kJ) and the male rats (13,850 kJ) (Fig. 6).

The size of the brown adipose tissue was significantly increased in both male and female rats fed the cafeteria diet (P < O.Ol), but this increase was reduced in exercised animals (P < 0.01). In addition, exercise had no effect on the brown adipose tissue of either male or female animals fed the stock diet (Fig. 5). The injection of norepinephrine failed to modify body temperature significantly in male or female rats fed the stock diet whether they were sedentary or on the exercise program. All animals fed the cafeteria diet showed an increase in body temperature after norepinephrine injection. This increase was larger in male than in female rats, and it was somewhat reduced by exercise training in male rats only (P < 0.05) (Fig. 5). Measurements of plasma thyroid hormones gave the

following results (Fig. 7). Cafeteria diet increased the plasma levels of triiodothyronine (Ta) in both male and female rats (P c O.Ol), whereas exercise reduced these levels in both males (P c 0.05) and females (P < 0.01) fed either the stock or the cafeteria diet. On the contrary, cafeteria diet had no effect on thyroxine (Td) concentrations. The only significant change observed in Td concentrations was a decrease in exercising male rats (P < 0.01) fed the standard chow diet,

Plasma catecholamine determinations gave the following results. There was a sixfold increase in norepinephrine when the rats swam for the first time, and this increase was not diminished after rats had been swimming for 10 wk. A fivefold increase in plasma epinephrine was observed in rats after swimming for the first time, but this effect was significantly reduced after 10 wk of swimming (Fig. 8).

MALE FEMALE

r r

0.8- .

0.6- .

0*4-

B standard chow (s )

3 s + exercise

c + exercise m

FIG. 5. Variations in epididymal and parametrial fat pads in male and female rats as affected by various diets. C diets increased size of fat deposit (P < 0.01) and exercise caused drop in both C and S groups (P < 0.01). C diets increased size of interscapular brown fat (P < 0.01), which was reduced in male and female exercise groups (P c 0.01). C diets increased response to norepinephrine (0.3 pg/loO g body wt), but this effect is more pronounced in male than in female rats (P < 0.01). Exercise training reduced effect observed with C diet in male rats.

DIET, EXERCISE, AND THERMOGENESIS

DISCUSSION

The marked influence of palatable food, termed cafeteria diet by Rothwell and Stock (29,30), on body growth has been confirmed in both male and female rats. In the males the cafeteria diet increased caloric intake by 13,850 kJ; the animals gained 51 g more than the Purina-fed

I s,ooc

13,ooc

DIFFERENCE BETWEEN C AND S

CALORIC INTAKE (k3) BODY WEIGHT GAIN Ig)

r IO&

I L 1 + c I I

so- c r

L II

I

DIFFERENCE BETWEEN CE AND SE m

I00 - I c

I femalss

m males

I

C= cafeteria I

S= standard chm ’

E= exercise - trained i

FIG. 6. Difference in body-weight gain between cafeteria (C) and standard chow diet (S) was greater in female than in male rats (P < 0.05), although difference in caloric intake between C and S groups was not affected by sex.

Q z6O t

FEMALE

559

animals during the lo-wk period, and epididymal fat pads were three times larger. In the female rats caloric intake increased by 14,770 kJ, the extra weight gain amounted to 92 g, and the parametrial fat pads were also three times larger. Thus although the effect of cafeteria diet on caloric intake is somewhat comparable for both sexes, the body-growth increase was significantly larger in the female than in the male rats. The extra weight gain observed in the females is due to either a facilitation of body-weight increase or a reduced thermogenic action of cafeteria diet in female compared with male rats. The results obtained when norepinephrine was injected tend to support a reduced thermogenesis in female rats. In- deed, the increase in body temperature in response to norepinephrine was greater in males (2.8 -t O.WC) than in females (1.2 -f- 0.15”C) (P < 0.01). Thus reduced thermogenesis could explain why female rats gained more weight than male rats while the food intake was comparable for both sexes. It should be mentioned however that the size of the brown adipose tissue (BAT), which was markedly increased by the cafeteria diet, was not

2OQC ’ I control 500 n @xercise- twined

F

NOREPINEPHRlI+JE EPINEPHRIIE

AT REST DURING AT REST DURING EXERCISE EXERCISE

FIG. 8. Both plasma epinephrine and norepinephrine were significantly increased in acute exercise (P c 0.01). This effect persisted in trained rats for norepinephrine but is reduced for epinephrine (P < 0.01).

FEMALE

standard chow (s ) caf etdria (c ) s + exercise c + exercise ,

FIG. 7. Plasma levels of triiodothyronine were increased by cafeteria feeding in male and female rats (P < 0.01). This effect was reduced by exercise training (P < 0.01). No change in plasma thyroxine was observed except that it decreased in exercised animals fed standard chow diet (P < 0.01).

560 LEBLANC, DUSSAULT, LUPIEN, AND RICHARD

different when male and female rats were compared. However, this finding does not exclude the possibility for a role of the BAT in explaining the difference in thermogenesis between male and female rats. Indeed, it is possible that the metabolically active tissue present in the BAT is not related exclusively to its size. For example, growth of BAT accompanied by a marked increase in the total number of ,&adrenergic receptor sites can be con- sidered an important factor in thermogenesis (3),

The reduction of adiposity due to exercise training in rats fed standard laboratory food, which was reported by other investigators (5, 26, 27), was confirmed in the present study. Exercise training was also found to significantly modify the effects of the cafeteria diet in both male and female rats. Caloric intake in relation to energy expenditure was reduced by exercise, and this explained the reduced body-weight gain especially in cafeteria-fed animals. This reduction in body weight parallels a significant decrease in white adipose tissue size of exercise- trained animals compared with their sedentary controls. In these same animals it was found that exercise pre- vented some of the BAT hypertrophy and reduced the hyperthermic effect of norepinephrine in cafeteria-fed male and female rats. In other words, exercise training reduced the thermogenesis produced by the cafeteria diet. This finding is somewhat unexpected. Indeed, we have shown that the level of exercise used in the present study produced a marked activation of the sympathetic nervous system as evidenced by the large increase in plasma cpinephrine and norepinephrine. Previous studies have demonstrated that such an increase in sympathetic nervous system activity as produced by cold exposure or repeated daily injections of catecholamines results in BAT enlargement and enhanced response to the metabolic effect of norepinephrine, both phenomena being associated with an increased thermogenesis (19). At this point, the role of the thyroid hormones in the genesis of thermogenesis would seem to be relevant in the present discussion. In cold-induced thermogenesis the plasma level of T3 is increased as shown previously (16). In diet- induced thermogenesis the levels of T3 are also increased in humans (6) and in rats (30)) and these results are confirmed by the present study. In exercise-trained male or female rats, the levels of T3 are reduced compared with the levels in sedentary animals; this difference is observed whether the animals are fed stock diet or cafeteria diet. Moderate exercise in humans has also been shown to decrease plasma T3 levels (25), These results are in agreement with previous findings showing that thyroid stimulating hormone response is reduced by many stressing situations (17) but not by cold exposure (4). Kinetic techniques have shown that the increase in plasma Ts observed with overeating in humans is associated with a greater production rate of Ta (23). Similar findings were reported during prolonged cold exposure in the rats (16). We have shown that repeated thyroid hormone injections increase the size of the BAT and the response to norepinephrine (20). Thus cold exposure and overeating increase the level of T3 in the blood, indicating that this metabolic hormone is concerned with the induction of enhanced thermogenesis. Following the same reasoning it can be argued that the reduction of diet-

induced thermogenesis by exercise could be related to a concomitant reduction of T3 production.

The BAT is accepted as the important site of thermogenesis of nonmuscular origin (10, 13, 30, 33). What are the factors involved in the transformation of BAT into a highly metabolic tissue? The fact that daily injections of norepinephrine (18, 19) or isoproterenol produce a BAT hypertrophy and promote thermogenesis may indicate the importance of these substances in cold- and diet-induced thermogenesis, because these two condi- tions are characterized by an enhanced catecholamine secretion (21,35). However exercise training, as described in the present experiment, also causes a marked increase in plasma catecholamines, and yet no evidence of thermogenesis was found in rats fed a standard laboratory diet, whereas in rats fed the cafeteria diet the induced therrnogenesis was partly reduced by training. Another substance that might be suggested as a factor in thermogenesis induction and in BAT metabolic activation is the thyroid hormone. Indeed T4 and T3 have been shown to stimulate mitochondrial protein synthesis in vitro and to induce an increased respiratory activity in the mitochondria (9, 34). Yet we have shown that repeated injections of Td failed to increase respiratory enzyme activity in the BAT (12, 28). However, cold exposure and isoproterenol injections produced significant increases in the activity of these enzymes. Just the same Td injections resulted in an increased thermogenesis comparable with that observed after repeated injections of isoproterenol. Obviously different mechanisms are involved in Tq- and catecholamine-induced thermogenesis; for catecholamines the important factor may be the increased activity of mitochondrial enzymes, whereas the effect of Tq could be explained by an increase in the Na’-K’-ATPase activity (15). In cold-adapted rats the activity of respiratory enzymes in BAT is increased but no more than in isoproterenol-injected rats, and yet cold-adapted animals are much more resistant to cold. Because not only catecholamine but also thyroid hormones are secreted in larger quantities in cold-adapted animals, it is possible that the marked thermogenesis observed is due to an increase of both Na’-K’-ATPase and respiratory enzyme activity in the BAT. For the same reasons the same situation may prevail in the diet-induced thermogenesis. Thus the diminution, but not the complete abolition, of thermogenesis by exercise training could be explained by the suppression of the increase in plasma T3 levels nor- m dY

Fee observed in diet-induced thermogenesis. ding palatable food stimulates caloric intake and

increases body-weight gain. At the same time plasma T3 is increased, the BAT hypertrophies and the animals become more sensitive to the thermogenic effect of norepinephrine . This enhanced heat production would have a corrective action on this excessive food intake and serve a useful purpose in helping to prevent fat deposition (I, 22, 32). In that sense thermogenesis is an adaptive reaction. Exercise training has no such effect per se. When assocrated with palatable food, the habit of exercise diminished excessive food intake and reduced the increase in plasma T3 and the hypertrophy of the BAT. This results in a diminution of the norepinephrine-induced thermogenesis. It is also suggested that the sexual

DIET, EXERCISE, AND THERMOGENESIS 561

difference in norepinephrine thermogenesis observed in animals fed palatable food contributes to the caloric- sparing effect observed in female rats, wh ich by consum- ing quantities of food similar to male rats were found to

REFERENCES

1. APFELBAUM, M., J, BOSTSARRON, AND D. LACATIS. Effect of calorie restriction and excessive calorie intake on energy expenditure. Am, J, CZin, Nutr. 24: 1405-1409, 1971.

2. BUCHANAN, J. L., M. P. PRIMAX, AND D. F. TAPLEY. Effect of inhibition of mitochondrial protein synthesis in vitro upon thyroxine stimulation of oxygen consumption. EndocrinoZogy 89: 534-541, 1971.

3. BUKOWIECKX, L., N. FOLLI~A, J. VALLII~RES, AND J. LEBLANC. Beta receptors in brown adipose tissue: characterization and alterations during acclimation of rats to cold. Eur. 9. Biochem. 92: 189-196, 1978.

4. BROWN-GRANT, K. The hypothalamus and the thyroid gland. Br. Med. BUZZ. 16: 165169, 1960.

5. CREWS, E, L, III, K. W. FUGE, L. B. OSCAI, J. 0. HOLLOSZY, AND R. E. SHANK. Weight, food intake, and body composition: effects of exercise and of protein deficiency. Am. J. PhysioZ. 216: 359-366, 1969.

6. DANFORTH, E., JR., E. A. H. SIMMS, E. S. HORTON, AND R. F. GOLDMAN. Correlation of serum triiodothyronine concentrations with dietary composition, gain in weight and thermogenesis in man. Diabetes 24: 406-411, 1975.

7, DA PRADA, M., AND G, ZURCHER. Simultaneous radioenzymologic determination of plasma and tissue adrenaline, noradrenaline and dopamine in the femtomole range. Life Sci, 19: 1163-1174, 1976.

8. DESAUTZLS, M., G. ZAROR-BEHRENS, AND J. HIMMS-HAGEN. In- creased purine nucleotide binding, altered polypeptide composition and thermogenesis in brown adipose tissue mitochondria of cold- acclimated rats. Can. J. Biochem. 56: 378-383, 1978.

9. DUNCAN, D, B. Multiple range and multiple F test. Biometrics 11: l-42, 1967.

10. FOSTER, D., AND M. L. FRYDMAN, Non-shivering thermogenesis in the rat. II. Measurements of blood flow with microspheres point to brown fat tissue as the dominant site of the calorigenesis induced by noradrenaline. Can. J. PhysioZ. PharmacoZ. 56: 110-123, 1978.

11. HART, J* S. Physiological responses to cold in non-hibernating homeotherms. In: Temperature, its Measurements and ControZ in Science and Industry, edited by J. D. Hardy. New York: Reinhold, 1963, vol. 3, part 3, p. 376-406.

12. HEICK, H. M. C,, C. VACHON, M. A. KALLAI, N. B&GIN-HEICKS, AND J, LEBLANC. The effects of thyroxine and isopropylnoradren- aline on cytochrome activity in brown adipose tissue. Can. J. PhysioL Biochem. 51: 751-758, 1973.

13, HIMMS-HAGEN, J. Sympathetic regulation of metabolism. Phar- macol. Rev. 19: 367-461, 1967.

14, HSIEH, A. C, L., AND L. D. CARLSON. Role of adrenaline and noradrenaline in chemical regulation of heat production. Am. J. Physiol. 190: 243-246, 1957.

15. ISMAIL-BEIGH, F., AND I. EDELMAN. Mechanism of thyroid calorigenesis: role of active sodium transport. Proc. NatZ. Acad. Sci. USA 67: 1071-1078, 1970.

16. JOBIN, M., S. DULAC, AND C. FORTIER. Effect of cold exposure on thyroxine and triiodothyronine secretion q in the rat (Abstract). Federation Proc. 32: 110, 1973.

17. KRAICER, J., P. DUCOMMUN, M. JOBIN, C. RERUP, G. P, VAN REES,

gain significantly more weight during the experimental period.

Received 7 April 1981; accepted in final form 28 September 1981.

AND C. FORTIER, Pituitary and plasma TSH response to stress (Abstract). Federation Proc. 22: 507, 1963.

18, LEBLANC, J. Man in the CoZd. (Am. Lectures in Environ. Studies Ser.) Springfield, IL: Thomas, 1975.

19. LEBLANC, J,, AND M. POULIOT. Importance of noradrenaline in cold adaptation, Am. J, PhysioZ. 207: 853-857, 1964.

20. LEBLANC, J., AND A. VILLEMAIRE. Thyroxine and noradrenaline on noradrenaline sensitivity, cold resistance, and brown fat. Am. J. Physiol. 218: 1742-1745, 1970,

21. LEDUC, J. Catecholamine production and release in exposure and acclimation to cold. Acta Physiol. Stand. Suppl. 183: l-UN, 1961.

22. MILLER, P. S., P. M. MUNFORD, AND M. J. STOCK. Gluttony. II. Thermogenesis in overeating man. Am. J. CZin. Nutr. 20: 1223- 1229, 1967.

23, MITSUMA, T., M. GERSHENOGORN, J. COLUCCI, AND C, S. HOL- LANDER, Radioimmunoassay of triiodothyronine in enextracted human serum. J. CZin, Endocrinol. Metab. 33: 364-367, 1971.

24. MURPHY, B. P., AND C, JACHAN, The determination of thyroxine by competitive protein binding analysis employing an ion-exchange resin and radiothyroxine. J. Lab. CZin. Med. 66: 161-167, 1965.

25. O’CONNEL, M., D. C. ROBBINS, E. S. HORTON, E. A, H. SIMS, AND E, DANFORTH, JR. Changes in serum concentrations of 3,3’,5’-triiodothyronine and 3,5,3’-triiodothyronine during moderate prolonged exercise. J. CZin. Endocrinol, Metab. 49: 242-248, 1979.

26. OSCAI, L. B., S. P. BABZRAK, J. A. MCGARR, AND C. N. SPIRAKIS. Effect of exercise on adipose tissue cellularity. Federation Proc. 33: 1956-1958, 1974.

27. RICHARD, D., AND 5. LEBLANC. Effects of physical training and food restriction on insulin secretion and glucose tolerance in male and female rats. Am. J. Chin. Nutr. 33: 2588-2594, 1980.

28, RICQUIER, D., AND J. C. KADER. Mitochondrial protein alteration in active brown fat, Biochem. Biophys. Res* Commun. 73: 577-583, 1976.

29. ROTHWELL, N. J., AND M. J. STOCK. A role for brown adipose tissue in diet-induced thermogenesis. Nature London 281: 31-35, 1979.

30. ROTHWELL, N. J., AND M. J. STOCK. Similarities between cold- and diet-induced thermogenesis in the rat. Can. J. Physiol. Pharmacol. 58: 842-848, 1980,

31. SCLAFANI, A., AND D. SPRINGER. Dietary obesity in adult rats: similarities to hypothalamic and human obesity syndromes. Phys- ioZ. Behavior 17: 461-471, 1976.

32. SIMS, E. A. H., E. DANFORTH, E, S. HORTON, G. A. BRAY, J. A. GLENNON, AND L. B. SALAND. Endocrine and metabolic effects of experimental obesity in man. Rec. Prog. Harm. Res. 29: 457-496, 1973.

33. SMITH, R, E,, AND B. A. HORWITZ. Brown fat and thermogenesis. Physiol. Rev. 49: 330-425, 1969.

34. VOLFIN, P., S. S. KAPLAY, AND D. R. SANADI. Early effect of thyroxine in vivo on rapidly labelled mitochondrial protein fractions and respiratory control. J. Biol. Chem. 244: 5631-5639, 1969.

35. YOUNG, J. B., AND L, LANDSBERG, Effect of diet on cold exposure on norepinephrine turnover in pancreas and liver. Am. J. Physiol. 236 (Endocrinol. Metab. Gastrointestinal Physiol. 5): E524-E533, 1979.

Documents

Effect of diet and exercise on norepinephrine- induced thermogenesis in male … › ... › files › anexos › php735cda_6454.pdf · 2012-04-09 · Effect of diet and exercise