The air-breathing Alaska blackfish (Dallia pectoralis) remodels ventricular Ca2+ cycling with chronic hypoxic submergence to maintain ventricular contractility

• Published in: Current Research in Physiology
• Main Authors: Shiels, Holly A., White, Ed, Couturier, Christine S., Hall, Diarmid, Royal, Shannon, Galli, Gina L.j., Stecyk, Jonathan A.w.
• Format: Article in Journal/Newspaper
• Language: English
• Published: 2022
• Subjects: Calcium; Cardiomyocyte; Force-frequency relationship; Fura-2; Oxygen; Temperature; Alaska blackfish; Dallia pectoralis; Alaska
• Online Access: https://research.manchester.ac.uk/en/publications/c85c9bd9-6f39-4bb9-a98f-4f942d078164; https://doi.org/10.1016/j.crphys.2022.01.001; http://www.scopus.com/inward/record.url?scp=85131202386&partnerID=8YFLogxK; https://www.mendeley.com/catalogue/3879e282-6400-3b72-8963-e17cd6fa0e8e/; https://linkinghub.elsevier.com/retrieve/pii/S2665944122000013

The Alaska blackfish (Dallia pectoralis) is a facultative air-breather endemic to northern latitudes where it remains active in winter under ice cover in cold hypoxic waters. To understand the changes in cellular Ca2+ cycling that allow the heart to function in cold hypoxic water, we acclimated Alaska blackfish to cold (5 °C) normoxia or cold hypoxia (2.1–4.2 kPa; no air access) for 5–8 weeks. We then assessed the impact of the acclimation conditions on intracellular Ca2+ transients (Δ[Ca2+]i) of isolated ventricular myocytes and contractile performance of isometrically-contracting ventricular strips. Measurements were obtained at various contractile frequencies (0.2–0.6 Hz) in normoxia, during acute exposure to hypoxia, and reoxygenation at 5 °C. The results show that hypoxia-acclimated Alaska blackfish compensate against the depressive effects of hypoxia on excitation-contraction coupling by remodelling cellular Δ[Ca2+]i to maintain ventricular contractility. When measured at 0.2 Hz in normoxia, hypoxia-acclimated ventricular myocytes had a 3.8-fold larger Δ[Ca2+]i peak amplitude with a 4.1-fold faster rate of rise, compared to normoxia-acclimated ventricular myocytes. At the tissue level, maximal developed force was 2.1-fold greater in preparations from hypoxia-acclimated animals. However, maximal attainable contraction frequencies in hypoxia were lower in hypoxia-acclimated myocytes and strips than preparations from normoxic animals. Moreover, the inability of hypoxia-acclimated ventricular myocytes and strips to contract at high frequency persisted upon reoxygenation. Overall, the findings indicate that hypoxia alters aspects of Alaska blackfish cardiac myocyte Ca2+ cycling, and that there may be consequences for heart rate elevation during hypoxia, which may impact cardiac output in vivo.