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First published online May 18, 2006
Journal of Experimental Biology 209, 2114-2128 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02241

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Steroid-induced cardiac contractility requires exogenous glucose, glycolysis and the sarcoplasmic reticulum in rainbow trout

Richard S. Farrar^*, Pavan K. Battiprolu^*, Nicholas S. Pierson and Kenneth J. Rodnick

Department of Biological Sciences, Idaho State University, Pocatello, ID 83209-8007, USA

View larger version (16K): [in a new window]   Fig. 1. Experimental design involving additions of D-glucose, inotropes and metabolic inhibitors to cardiac tissue in vitro. In all experiments, ventricle strips from rainbow trout were incubated for 60 min in either glucose or glucose-free media and electrically stimulated (0.5 Hz) at 14°C. (A) Glucose dose-response. Zero glucose reflects control ventricle strips remaining in glucose-free media for the entire experiment. (B) Combined effects of glucose (5 mmol l-1) and inotropes: T (0.3 µmol l-1) in males; E2 (1 nmol l-1) in females; and Epi (1 µmol l-1) or Ca2+o (5 mmol l-1) in both sexes. (C) Effects of inotropes mentioned above and caffeine (8 mmol l-1), with and without glucose. (D) Effects of inotropes in ventricle strips pretreated with inhibitors iodoacetate (IAA) (0.4 mmol l-1) or ryanodine (10 µmol l-1). (E) Original recording of isometric twitch force in ventricular muscle strips from a male rainbow trout. After ventricle strips were stretched to optimal length (90% Lmax) and after mechanical stabilization for 60 min, glucose (5 mmol l-1) was added to one strip and the other remained glucose-free (control) for 60 min. The extent of stored Ca2+ in the sarcoplasmic reticulum was determined by post rest potentiation (PRP). Stimulation of ventricle strips was discontinued for 5 min, prior to PRP measurements. PRP was higher in glucose-treated ventricle strips when compared with the corresponding glucose-free control. Values are means ± s.e.m. (N=6-11 strips per group).

View larger version (20K): [in a new window]   Fig. 2. Effects of exogenous glucose on resting tension. In females, resting tension was maintained in media containing 5 or 10 mmol l-1 glucose but increased in glucose-free (0), 1 and 2 mmol l-1 glucose conditions (dissimilar letters denote significant differences between treatments, *P<0.05). There were no significant differences in resting tension for males at all concentrations tested. Immature females also showed higher resting tension compared with immature and sexually maturing males at 0, 1 and 2 mmol l-1 glucose. Values are means ± s.e.m. (N=8-26 strips per group).

View larger version (21K): [in a new window]   Fig. 3. Effects of exogenous glucose on twitch force (F). During the 60 min equilibration period, ventricle strips were incubated in the absence of any exogenous substrate. In sexually maturing males, F increased during the experimental period with 5 mmol l-1 glucose present, compared with 0, 1, 2 and 10 mmol l-1 glucose, and was higher than that in immature males and females at all concentrations tested. F was also higher in immature males at 5 mmol l-1 glucose compared with females and at all concentrations tested. In females, 5 mmol l-1 glucose increased F compared with 0, 1 and 10 mmol l-1 values. *P<0.05. Values are means ± s.e.m. (N=8-26 strips per group).

View larger version (20K): [in a new window]   Fig. 4. Effects of Ca2+ (5 mmol l-1), epinephrine (Epi; 1 µmol l-1), ethanol (EtOH), testosterone (T; 0.3 µmol l-1) or 17ß-estradiol (E2; 1.0 nmol l-1), in the presence (filled bars) or absence (open bars) of exogenous glucose (5 mmol l-1), on performance of ventricle strips from males (A) and females (B). All ventricle strips received exogenous glucose during the 60 min equilibration period. There were only significant differences in ventricle strips exposed to sex steroids. *P<0.05. Values are means ± s.e.m. (N=7-9 strips per group).

View larger version (14K): [in a new window]   Fig. 5. Effects of glycolytic inhibitor iodoactetate (IAA; 0.4 mmol l-1) on immature male (A) and female (B) cardiac tissue. After a 15 min incubation with IAA, ventricle strips were exposed to either increased Ca2+ (5 mmol l-1), testosterone (T; 0.3 µmol l-1), 17ß-estradiol (E2; 1 nmol l-1) or epinephrine (Epi; 1 µmol l-1). Plus (+) and minus (-) denote presence and absence, respectively, of specific compounds in the incubation medium. For immature males and females, elevated Ca2+ or Epi, but not sex steroids, increased twitch force when glucose (5 mmol l-1) was present. *P<0.05. Values are means ± s.e.m. (N=9-11 strips per group).

View larger version (13K): [in a new window]   Fig. 6. Effects of ryanodine (Ryn; 10 µmol l-1) in immature male (A) and female (B) cardiac tissue. Ventricle strips were incubated with Ryn 15 min prior to the addition of either increased Ca2+ (5 mmol l-1), testosterone (T; 0.3 µmol l-1), 17ß-estradiol (E2; 1 nmol l-1) or epinephrine (Epi; 1 µmol l-1). Plus (+) and minus (-) denote presence and absence, respectively, of specific compounds in the incubation medium. For immature males and females, elevated Ca2+ or Epi, but not sex steroids, increased twitch force when glucose (5 mmol l-1) was present. *P<0.05. Values are means ± s.e.m. (N=6-8 strips per group).

View larger version (15K): [in a new window]   Fig. 7. Effects of various compounds (iodoacetate, (IAA; 0.4 mmol l-1); ryanodine, (Ryn; 10 µmol l-1); caffeine (8 mmol l-1); Ca2+ (5 mmol l-1); epinephrine (Epi; 1 µmol l-1); testosterone (T; males; 0.3 µmol l-1); or 17ß-estradiol (E2; females; 1.0 nmol l-1) on post-rest potentiation (PRP) in immature males (A) and females (B). In both sexes, ventricle strips receiving glucose had higher PRP than strips without glucose (*P<0.05). Control strips containing glucose also exhibited higher PRP than all other treatments when glucose was present (a denotes P<0.05). PRP for glucose-free, control strips were higher than all other treatments (b denotes P<0.05). However, other than control strips, no significance was observed between glucose vs glucose-free treatments (P=0.34). Values are means ± s.e.m. (N=6-11 strips per group).

View larger version (17K): [in a new window]   Fig. 8. Effects of caffeine (8 mmol l-1) on contractile performance of cardiac tissue in the presence or absence of elevated Ca2+ (5 mmol l-1), epinephrine (Epi; 1 µmol l-1), testosterone (T; males; 0.3 µmol l-1) or 17ß-estradiol (E2; females; 1.0 nmol l-1). All ventricle strips were exposed to 5 mmol l-1 glucose for 1 h prior to addition of caffeine. After a 15 min exposure to caffeine, each strip received one of the inotropes. Within a sex there were no differences between treatments; however, the increase in twitch force was greater in immature males than females (*P<0.05). Values are means ± s.e.m. (N=7 strips per group).

View larger version (18K): [in a new window]   Fig. 9. The relationship between extracellular Ca2+ and contractile force. Twitch force is expressed as a percentage of the difference between maximum force development and baseline force at 1.5 mmol l-1 Ca2+ for (A) male and female ventricle strips receiving 5 mmol l-1 glucose; (B) female ventricle strips, glucose vs glucose-free and (C) male ventricle strips, glucose vs glucose-free. In the presence of glucose, the EC50 for Ca2+-dependent force production was lower in females than males (P<0.01). Compared with tissue receiving glucose, glucose-free ventricle strips from both sexes were less sensitive to Ca2+ (P<0.05) but sex differences were not evident. Values are means ± s.e.m. (N=8-9 strips per curve).