Thyroid hormones and the energetics of active sodium‐potassium transport in mammalian skeletal muscles.

Abstract

SUMMARY1. The steady-state heat production rate (1) of soleus muscles obtained from adult mice in various thyroid states was measured in a perfused microcalorimeter. The ouabain-suppressible fractions of E and 42K influx were compared and the energetic efficiency of active Na-K transport assessed.2. Hypothyroidism with plasma thyroxine concentrations below 1 jug/100 ml. was induced by pretreatment with 131I or perchlorate. In soleus muscles isolated from treated animals, mean E9 values were 2541 + 0 7 and 24-2 + 0 5 mcal.g wet wt.-'. min-for the 1311 and the perchlorate series respectively, i.e. about 30 % lower than the control level (36.3 + 1t5 mcal.g wetwt.-l.min-1). Followingtriiodothyronine treatment, X was increased by about 45 %.3. In muscles from hypothyroid (1311 and perchlorate series), euthyroid and hyperthyroid mice ouabain (10-3 M) induced a rapid decrease in ER of 1-6 + 0.1 and 1-4 + 0*1 2-5 + 0-2, and 4-3 + 0-6 mcal.g wet wt.-'.min-' respectively, i.e. between 6 and 8 % of1E.4. In muscles obtained from hypothyroid, euthyroid and hyperthyroid mice, the ouabain-suppressible component of 42K influx was 0-17 + 0 04, 031 + 0-02 and 0-45 + 0-02 Itmole. g wet wt.-. min-respectively. Whereas the total number of ouabain binding sites varied appreciably with the thyroid status, the Na-K contents of soleus or diaphragm muscles showed no significant changes.5. Notwithstanding the parallelism between the changes in basal X and ouabainsensitive components of E and K influx with the thyroid status, it is concluded that active Na-K transport cannot be considered a primary effector of thyroid thermogenesis in intact mammalian skeletal muscle. The direct contribution of active Na-K transport to this thermogenesis was indeed small compared with the over-all cellular energy dissipation.6. The minimum over-all energetic efficiency of the transport process in the intact muscle (30-35 %) was not dependent on the thyroid status.

ROLE OF NA+, K+-ATPase IN MUSCULAR ENERGY EXPENDITURE OF WARM- AND COLD-EXPOSED SHEEP

“…Utilis6 ir la concentration molaire de 10 (Folke and Sestoft 1977), isolated rat soleus muscle and adipose tissue (Chinet et al 1977). and mouse soleus and diaphragm muscles (Biron et al 1979;Gregg and Milligan 1980 (Kleiber 1961 l"C (cold exposed) or 25"C (warm exposed) for 5 wk prior to muscle sampling. Warm-and cold-exposed sheep were fed to maintain body weight.…”

Intracellular sodium and potassium activities of skeletal muscle fibres of hypothyroid rats

“…A decrease in aK is compatible with the decrease in the ouabain-suppressible fraction of 42K uptake in hypothyroid mouse soleus (Biron et al 1979), and with the reduction in the intracellular K+ concentration of hypothyroid rat diaphragm (Ismail-Beigi & Edelman, 1973). (n = 61) (n = 57) n, number of fibres; P, significance of difference from untreated controls; n.s., not significant.…”

“…The number of Na+-K+ pump units decreases significantly in the skeletal muscles of hypothyroid mice (Biron, Burger, Chinet, Clausen & Dubois-Ferriere, 1979) and rats (Kjeldsen, Everts & Clausen, 1986;Everts & Clausen, 1988). Whether hypothyroidism and the resultant decrease in pump units is associated with changes in membrane potential (Vm) and intracellular sodium and potassium activities (a'a and a') of the muscles is not clear.…”

The effect of ouabain on metabolic rate in guinea-pigs: estimation of energy cost of sodium pump activity

“…For instance, McBride & Milligan (1985 a ) estimated that in sheep the ouabain-sensitive respiration of hepatocytes was about 35 YO, whereas Clark et al (1982) reported that in rat hepatocytes the ouabain-suppressible oxygen uptake was 2-8 '10. Similar discrepancies have been reported for muscle tissue (Asano et al 1976;Biron et al 1979;Gregg & Milligan, 1982). Furthermore, there are no estimates for the contribution of the Na pump to the basal or resting metabolic rate in the whole animal.…”

“…reported that injection of ouabain into mice decreased 0, consumption by 20-25 YO, which is in agreement with our findings. Previous in vitro studies on the energy cost of the Na pump have been made on isolated tissues or cells and the results have been conflicting (Asano et al 1976;Biron et al 1979;Guernsey & Morishige, 1979;Gstraunthaler et al 1985;Milligan & McBride, 1985). Some of these conflicting results could be due to differences in the concentration of ouabain used.…”