Recombinant interleukin-1ß dilates steelhead trout coronary microvessels: effect of temperature and role of the endothelium, nitric oxide and prostaglandins.

Interleukin (IL)-1ß is associated with hypotension and cardiovascular collapse in mammals during heat stroke, and the mRNA expression of this pro-inflammatory cytokine increases dramatically in the blood of Atlantic cod (Gadus morhua) at high temperatures. These data suggest that release of IL-1ß at high temperatures negatively impacts fish cardiovascular function and could be a primary determinant of upper thermal tolerance in this taxa. Thus, we measured the concentration-dependent response of isolated steelhead trout (Oncorhynchus mykiss) coronary microvessels (<150 µm in diameter) to recombinant (r) IL-1ß at two temperatures (10 and 20°C). Recombinant IL-1ß induced a concentration-dependent vasodilation with vessel diameter increasing by approximately 8 and 30% at 10(-8) and 10(-7) mol l(-1), respectively. However, this effect was not temperature dependent. Both vessel denudation and cyclooxygenase blockade (by indomethacin), but not the nitric oxide (NO) antagonist L-NIO, inhibited the vasodilator effect of rIL-1ß. In contrast, the concentration-dependent dilation caused by the endothelium-dependent calcium ionophore A23187 was completely abolished by L-NIO and indomethacin, suggesting that both NO and prostaglandin signaling mechanisms exist in the trout coronary microvasculature. These data: (1) are the first to demonstrate a functional link between the immune and cardiovascular systems in fishes; (2) suggest that IL-1ß release at high temperatures may reduce systemic vascular resistance, and thus, the capacity of fish to maintain blood pressure; and (3) provide evidence that both NO and prostaglandins play a role in regulating coronary vascular tone, and thus, blood flow.

Cold-acclimation leads to differential regulation of the steelhead trout (Oncorhynchus mykiss) coronary microcirculation.

The regulation of vascular resistance in fishes has largely been studied using isolated large conductance vessels, yet changes in tissue perfusion/vascular resistance are primarily mediated by the dilation/constriction of small arterioles. Thus we adapted mammalian isolated microvessel techniques for use in fish and examined how several agents affected the tone/resistance of isolated coronary arterioles (<150 µm ID) from steelhead trout (Oncorhynchus mykiss) acclimated to 1, 5, and 10°C. At 10°C, the vessels showed a concentration-dependent dilation to adenosine (ADE; 61 ± 8%), sodium nitroprusside (SNP; 35 ± 10%), and serotonin (SER; 27 ± 2%) (all values maximum responses). A biphasic response (mild contraction then dilation) was observed in vessels exposed to increasing concentrations of epinephrine (EPI; 34 ± 9% dilation) and norepinephrine (NE; 32 ± 7% dilation), whereas the effect was less pronounced with bradykinin (BK; 12.5 ± 3.5% constriction vs. 6 ± 6% dilation). Finally, a mild constriction was observed after exposure to acetylcholine (ACh; 6.5 ± 1.4%), while endothelin (ET)-1 caused a strong dose-dependent increase in tone (79 ± 5% constriction). Acclimation temperature had varying effects on the responsiveness of vessels. The dilations induced by EPI, ADE, SER, and SNP were reduced/eliminated at 5°C and/or 1°C as compared with 10°C. In contrast, acclimation to 5 and 1°C increased the maximum constriction induced by ACh and the sensitivity of vessels to ET-1 (but not the maximum response) at 1°C was greater. Acclimation temperature had no effect on the response to NE, and responsiveness to BK was variable.

Metabolic and cardiac responses of cunner Tautogolabrus adspersus to seasonal and acute changes in temperature.

The cunner is a marine teleost that exhibits winter dormancy (i.e., becomes inactive and stops feeding) when seawater temperatures fall below 5°C. To examine whether this dormant state is also associated with active metabolic depression, the effect of season on routine metabolic rate (MR(rout)) was measured at five different times throughout the year: early spring (5°C), late spring (9°C), summer (14°C), late fall (5°C), and winter (0°C). In addition, cardiac function (cardiac output, heart rate, and stroke volume) was measured at the last three measurement time points, and the ability of fall- and winter-acclimated cunner to adjust MR(rout) and cardiac function when challenged with acute temperature changes was assessed. The cunner actively depressed MR(rout) between fall and winter as temperature fell from 5° to 0°C ([Formula: see text]). In addition, MR(rout) showed a substantial but smaller Q(10) (4.3) when the MR(rout) at 0°C (winter) was compared with the value recorded during the previous spring at ∼5°C. These seasonal changes were essentially mirrored by the response of MR(rout) to acute 5°C increases and decreases in temperature. Similar to MR(rout), cardiac output (Q) decreased dramatically as temperature fell from 5°C (fall) to 0°C (winter) in the seasonal study ([Formula: see text]) and increased substantially when temperature was acutely increased from 0° to 5°C ([Formula: see text]). However, when subjected to an acute temperature decrease (from 5° to 0°C), the Q(10) for Q was only approximately 2-3. These results show that (1) cunner actively depress their metabolism in the fall and winter and that this is associated with a large decrease in cardiac function and (2) there is a decoupling between Q and MR(rout) when 5°C seasonally acclimated cunner are exposed to an acute temperature decrease to 0°C.