Seasonality of dihydropyridine receptor binding in the heart of an anoxia-tolerant vertebrate, the crucian carp (Carassius carassius L.).

Abstract

Prolonged anoxia tolerance of facultative anaerobes is based on metabolic depression and thus on controlled reduction of energy-utilizing processes. One proposed survival mechanism is the closing of ion channels to decrease energetic cost of ion pumping (Hochachka PW. Science 231: 234-241, 1986). To test this hypothesis, the involvement of L-type Ca2+ channels in seasonal anoxia tolerance of the vertebrate heart was examined by determining the number of [methyl-3H]PN200-110 (a ligand of L-type Ca2+ channel alpha-subunit) binding sites of the cardiac tissue and the density of Ca2+ current in ventricular myocytes of an anoxia-resistant fish species, the crucian carp. In their natural environment, the fish were exposed for > 3 mo of hypoxia (O2 < 2.5 mg/l) followed by almost 8 wk of anoxia that resulted in abrupt depletion of cardiac glycogen stores in late spring. Unexpectedly, however, the number of [methyl-3H]PN200-110 binding sites did not decline in hypoxia/anoxia as predicted by the channel arrest hypothesis but remained constant for most of the year. However, in early summer, the number of [methyl-3H]PN200-110 binding sites doubled for a period of approximately 2 mo, which functionally appeared as a 74% larger Ca2+ current density. Thus the anoxia tolerance of the carp heart cannot be based on downregulation of Ca2+ channel units in myocytes but is likely to depend on suppressed heart rate, i.e., regulation of the heart at the systemic level, and direct depressive effects of low temperature on Ca2+ current to achieve savings in cardiac work load and ion pumping. The summer peak in the number of functional Ca2+ channels indicates a short period of high cardiac activity possibly associated with reproduction and active perfusion of tissues after the winter stresses.