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Ryanodine and dihydropyridine receptor binding in ventricular cardiac muscle of fish with different temperature preferences

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Abstract

Ca2+-induced Ca2+ release (CICR) mechanism of cardiac excitation–contraction (e–c) coupling is dependent on the close apposition between the sarcolemmal dihydropyridine receptors (DHPR) and the sarcoplasmic reticulum (SR) ryanodine receptors (RyR). In particular, high RyR/DHPR ratio is considered to reflect strong dependence on SR Ca2+ stores for the intracellular Ca2+ transient. To indirectly evaluate the significance of CICR in fish hearts, densities of cardiac DHPRs and RyRs were compared in ventricular homogenates of three fish species (burbot, rainbow trout, and crucian carp) and adult rat by [3H] PN200–110 and [3H] ryanodine binding. The density of RyRs was significantly (P<0.05) higher in the adult rat (124±10 channels/μm3 myocyte volume) than in any of the fish species. Among the fish species, cold-acclimated (4 °C) trout had more RyRs than burbot, and crucian carp. The density of DHPRs was highest in the trout heart. RyR/DHPR ratio was significantly (P<0.05) higher in rat (4.1±0.5) than in the fish hearts (varying from 0.97±0.16 to 1.91±0.49) suggesting that "mammalian type" CICR is less important during e–c coupling in fish ventricular myocytes. In rainbow trout, acclimation to cold did not affect the RyR/DHPR ratio, while in crucian carp it was depressed in cold-acclimated animals (4 °C; 0.97±0.16) when compared to warm-acclimated fish (23 °C; 1.91±0.49). Although RyR/DHPR ratios were relatively low in fish hearts, there was a close correlation (r 2=0.78) between the RyR/DHPR ratio and the magnitude of the Ry-sensitive component of contraction in ventricular muscle among the fish species examined in this study.

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Abbreviations

AP :

action potential

B max :

number of DHPR or RyR sites (pmol mg−1)

CA :

cold-acclimated

CICR :

Ca2+-induced Ca2+ release

DHPR :

dihydropyridine receptor

ICa:

Ca2+ current

Kd :

affinity of DHPR or RyR sites (nmol l−1)

PMSF :

phenylmethylsulfonyl fluoride

RyR :

ryanodine receptor

Ry :

ryanodine

SL :

sarcolemma

SR :

sarcoplasmic reticulum

WA :

warm-acclimated

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Acknowledgements

This work was supported by the Academy of Finland (Project Nos. 63090 and 78045). We would like to thank the Kontiolahti fish farm for donating the trout. In addition, we would like to thank local fisherman, Terho Laitinen, for supplying the burbot and Anita Kervinen for technical assistance in binding studies. The experiments comply with the current legislation for animal protection in Finland.

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Correspondence to M. Vornanen.

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Communicated by G. Heldmaier

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Tiitu, V., Vornanen, M. Ryanodine and dihydropyridine receptor binding in ventricular cardiac muscle of fish with different temperature preferences. J Comp Physiol B 173, 285–291 (2003). https://doi.org/10.1007/s00360-003-0334-z

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