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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

Author for correspondence (e-mail: rodnkenn{at}isu.edu)

Accepted 28 March 2006

Recent data from our laboratory suggest that sex steroids promote contractile function in cardiac muscle of rainbow trout (Oncorhynchus mykiss Walbaum), and there are sex differences in hormone signaling and cardiac function. The current study investigated whether steroid-induced inotropism in electrically paced (0.5 Hz, 14°C) ventricle strips at 90% L_max (1) has a metabolic requirement for exogenous glucose and (2) is associated with enhanced intracellular Ca²⁺ storage and release from the sarcoplasmic reticulum (SR). We also explored whether sex differences exist in extracellular Ca²⁺ (Ca²⁺_o) or cardiac sensitivity to Ca²⁺_o. In the absence or at low concentrations (1 or 2 mmol l^-1) of exogenous glucose, resting tension and relaxation time were increased selectively in cardiac tissue from females. Increasing glucose promoted twitch force in a bell-shaped manner, with 5 mmol l^-1 representing the optimal concentration for both sexes. The positive inotropic effects of physiological concentrations of testosterone (T) and 17ß-estradiol (E2) in male and female trout ventricle strips, respectively, developed slowly (10-45 min) and were not apparent in glucose-free medium, in medium containing iodoacetate (IAA), an inhibitor of glycolysis, or medium containing 5 mmol l^-1 lactate or pyruvate. Male ventricle strips had increased inotropic responses to glucose and T compared with female strips exposed to glucose and E2. Furthermore, sexually maturing males showed a greater inotropic response than immature males or females. Pretreatment with ryanodine (a specific blocker of SR Ca²⁺ release) also eliminated the inotropic effects of sex steroids and exogenous glucose and reduced the post-rest potentiation of contractile force (a marker of SR Ca²⁺ storage). By contrast, the inotropic effects of epinephrine (Epi) or elevated Ca²⁺_o were faster (developing within 1-3 min) and were not diminished by the presence or absence of glucose or by pretreatment with IAA or ryanodine. Sex differences were also found in responsiveness to caffeine (males > females) and the relationship between Ca²⁺ concentration and force development above baseline. The Ca²⁺₅₀ was lower in female cardiac tissue than males, suggesting greater Ca²⁺ sensitivity, and although plasma albumin was higher in females, total and ionized plasma Ca²⁺ did not differ between the sexes. For the first time, our study highlights the importance of extracellular glucose, glycolytic activity and SR Ca²⁺ storage and release for sex steroid-induced inotropism in the trout ventricle. Conversely, the inotropes Epi and elevated [Ca²⁺_o] do not require the presence or metabolism of exogenous glucose or the SR for signaling their positive effects on contractility. These results also demonstrate novel sex-related differences in cardiac reliance on exogenous glucose, Ca²⁺ sensitivity and SR function and thus should be considered in future studies.

Key words: glucose, glycolysis, steroid hormone, cardiac function, inotropism, calcium, sarcoplasmic reticulum, rainbow trout, Oncorhynchus mykiss

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This article has been cited by other articles:

				P. K. Battiprolu, K. J. Harmon, and K. J. Rodnick Sex differences in energy metabolism and performance of teleost cardiac tissue Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2007; 292(2): R827 - R836. [Abstract] [Full Text] [PDF]