Seasonal changes of cholinergic response in the atrium of Arctic navaga cod (Eleginus navaga)

Abstract

Fishes of north-temperate latitudes exhibit marked seasonal changes in electrical excitability of the heart partly as an outcome of temperature-dependent changes in the density of major K ion currents: delayed rectifiers (I, I) and background inward rectifier (I). In the arctic teleost, navaga cod (Eleginus navaga), I and I are strongly up-regulated in winter. The current study tests the hypothesis that the ligand-gated K current, the acetylcholine-activated inward rectifier, I, is also modified by seasonal acclimatization in atrial myocytes of navaga. In sinoatrial preparations of the summer-acclimatized (SA) navaga, 10 M carbamylcholine chloride (CCh) caused slowing of heart rate, shortening of atrial action potential (AP) duration and a drastic reduction of AP amplitude, eventually resulting in inexcitability. In winter-acclimatized (WA) atria CCh slowed HR and reduced AP duration, but reduction of AP amplitude was modest and never resulted in inexcitability. The difference in cholinergic response between SA and WA navaga is explained by seasonal changes in I density. The peak density of I, induced by 10 M CCh, at the common experimental temperature (+6 °C) was 0.97 ± 0.28 pA/pF in SA navaga but only 0.183 ± 0.013 pA/pF in WA navaga (a 5.3-fold difference, P < 0.05). At acclimatization temperatures of the fish I density was 2.8 ± 0.50 (at +12 °C) and 0.11 ± 0.06 pA/pF (at +3 °C) (a 26-fold difference, P< 0.05) for SA and WA navaga, respectively. Thus, acclimatization to summer induces a drastic up-regulation of the atrial I, which effectively shortens atrial AP. The reverse temperature compensation of the atrial I may be advantageous in summer under variable water temperatures and oxygen concentrations by reducing workload of the heart.

Feeling the heat: source–sink mismatch as a mechanism underlying the failure of thermal tolerance

“…The favorable I Na :I K1 ratio (large safety factor) makes the atrial myocytes easily excitable and protects them against heat-dependent deterioration of excitability. It is noteworthy that EE of atrial myocytes can be depressed by inducing an outward K + current by acetylcholine (I KAch ) (Abramochkin and Vornanen, 2017). However, the temperature-induced increase in I KAch is not large enough to prevent atrial excitability in vivo, as shown by the persistence of P waves in the ECG (Fig.…”

Phenanthrene alters the electrical activity of atrial and ventricular myocytes of a polar fish, the Navaga cod

“…Thus, it appears that unlike more northern temperate species ( Haverinen and Vornanen, 2020 ; Badr et al., 2018 ), excitability due to resting membrane potential in the ventricle of this polar fish is resistant to both temperature and a key petroleum pollutant. In vivo, the resting membrane potential of navaga atrial myocytes is maintained, at least in part, through vagal tone which activates the ACh-dependent inward rectifier I KACh ( Abramochkin and Vornanen, 2017 ). Once the atrial myocytes are isolated and lose this tone, they depolarise as the density of their inward rectifier current I K1 is very small ( Abramochkin and Vornanen, 2015 ).…”

“…The bulbus arteriosus was cannulated and myocytes were isolated by retrograde perfusion of the heart with isolation solution [(mmol L −1 ): NaCl 100, KCl 10, KH 2 PO 4 ∙2H 2 O 1.2, MgSO 4 ∙7H 2 O 4, taurine 50, glucose 10 and HEPES 10 at pH of 6.9], containing proteolytic enzymes. The concentration of enzymes (collagenase type IA, 0.5 mg ml −1 ; trypsin type IX, 0.33 mg ml −1 ; fatty acid free bovine serum albumin, 0.33 mg ml −1 ) were selected in accordance with earlier studies on navaga ( Abramochkin and Vornanen, 2017 , 2015 ). Isolated atrial and ventricular myocytes were obtained by mincing and triturating of ventricular and atrial myocardium after 10–12 min of heart perfusion.…”

“…The pipette solution for I Na contained (in mmol l −1 ): 5 NaCl, 130 CsCl, 1 MgCl 2 , 5 EGTA, 5 Mg 2 ATP, 5 HEPES, pH adjusted to 7.2 with CsOH ( Vornanen et al., 2011 ). During recordings of K + currents, the Na + channel blocker tetrodotoxin (300 nM) and the Ca 2+ channel blocker nifedipine (20 µM) were constantly present in external solution providing complete block ( Abramochkin and Vornanen, 2017 , 2015 ). During experiments with inward rectifier K + currents, selective I Kr blocker E-4031 (5 µM) was also added to external solution ( Abramochkin and Vornanen, 2017 , 2015 ).…”

“…Navaga are eurythermal fish that spawn in winter in shallow waters close to the ice at sub-zero temperatures, whilst in summer they move off shore where they have a preferred water temperature of about 7 °C but can experience temperatures up to 15 °C ( DeVries and Steffensen, 2005 ). Considering the warming of Arctic waters, previous studies have investigated the thermal plasticity of electrical excitability in navaga hearts ( Abramochkin and Vornanen, 2017 , 2015 ) and seasonal changes in the expression of the cardiac K + channels ( Hassinen et al., 2014 ). Thus, navaga are a suitable model for cardiotoxicology as their basic (healthy) electrophysiology is known, and they are living in regions vulnerable to toxicant exposure from oil and gas exploration.…”