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      Temperature-induced cardiac remodelling in fish

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          ABSTRACT

          Thermal acclimation causes the heart of some fish species to undergo significant remodelling. This includes changes in electrical activity, energy utilization and structural properties at the gross and molecular level of organization. The purpose of this Review is to summarize the current state of knowledge of temperature-induced structural remodelling in the fish ventricle across different levels of biological organization, and to examine how such changes result in the modification of the functional properties of the heart. The structural remodelling response is thought to be responsible for changes in cardiac stiffness, the Ca 2+ sensitivity of force generation and the rate of force generation by the heart. Such changes to both active and passive properties help to compensate for the loss of cardiac function caused by a decrease in physiological temperature. Hence, temperature-induced cardiac remodelling is common in fish that remain active following seasonal decreases in temperature. This Review is organized around the ventricular phases of the cardiac cycle – specifically diastolic filling, isovolumic pressure generation and ejection – so that the consequences of remodelling can be fully described. We also compare the thermal acclimation-associated modifications of the fish ventricle with those seen in the mammalian ventricle in response to cardiac pathologies and exercise. Finally, we consider how the plasticity of the fish heart may be relevant to survival in a climate change context, where seasonal temperature changes could become more extreme and variable.

          Abstract

          Summary: Thermal acclimation of some temperate fishes causes extensive remodelling of the heart. The resultant changes to the active and passive properties of the heart represent a highly integrated phenotypic response.

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          Most cited references110

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          Atrial remodeling and atrial fibrillation: mechanisms and implications.

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            Temperature requirements of Atlantic salmon Salmo salar, brown trout Salmo trutta and Arctic charr Salvelinus alpinus: predicting the effects of climate change.

            Atlantic salmon Salmo salar, brown trout Salmo trutta (including the anadromous form, sea trout) and Arctic charr Salvelinus alpinus (including anadromous fish) provide important commercial and sports fisheries in Western Europe. As water temperature increases as a result of climate change, quantitative information on the thermal requirements of these three species is essential so that potential problems can be anticipated by those responsible for the conservation and sustainable management of the fisheries and the maintenance of biodiversity in freshwater ecosystems. Part I compares the temperature limits for survival, feeding and growth. Salmo salar has the highest temperature tolerance, followed by S. trutta and finally S. alpinus. For all three species, the temperature tolerance for alevins is slightly lower than that for parr and smolts, and the eggs have the lowest tolerance; this being the most vulnerable life stage to any temperature increase, especially for eggs of S. alpinus in shallow water. There was little evidence to support local thermal adaptation, except in very cold rivers (mean annual temperature <6·5° C). Part II illustrates the importance of developing predictive models, using data from a long-term study (1967-2000) of a juvenile anadromous S. trutta population. Individual-based models predicted the emergence period for the fry. Mean values over 34 years revealed a large variation in the timing of emergence with c. 2 months between extreme values. The emergence time correlated significantly with the North Atlantic Oscillation Index, indicating that interannual variations in emergence were linked to more general changes in climate. Mean stream temperatures increased significantly in winter and spring at a rate of 0·37° C per decade, but not in summer and autumn, and led to an increase in the mean mass of pre-smolts. A growth model for S. trutta was validated by growth data from the long-term study and predicted growth under possible future conditions. Small increases (<2·5° C) in winter and spring would be beneficial for growth with 1 year-old smolts being more common. Water temperatures would have to increase by c. 4° C in winter and spring, and 3° C in summer and autumn before they had a marked negative effect on trout growth. © 2010 The Authors. Journal of Fish Biology © 2010 The Fisheries Society of the British Isles.
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              The variation in isometric tension with sarcomere length in vertebrate muscle fibres.

              1. The variation of isometric tetanus tension with sarcomere length in single fibres from frog striated muscle has been re-investigated with special precautions to ensure uniformity of sarcomere length within the part of the fibre being studied.2. In most respects the results of Ramsey & Street (1940) were confirmed, but (a) the peak of the curve was found to consist of a plateau between sarcomere lengths of 2.05 and 2.2 mu, (b) the decline of tension above this plateau is steeper than found by Ramsey & Street, and (c) the decline of tension below the plateau becomes suddenly steeper at a sarcomere length of about 1.67 mu.3. Many features of this length-tension relation are simply explained on the sliding-filament theory.4. It is concluded that, in the plateau and at greater lengths, the tension on each thin filament is made up of equal contributions from each bridge which it overlaps on adjacent thick filaments.5. Internal resistance to shortening is negligible in this range but becomes progressively more important with shortening below the plateau.
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                Author and article information

                Journal
                J Exp Biol
                J. Exp. Biol
                JEB
                jexbio
                The Journal of Experimental Biology
                The Company of Biologists Ltd
                0022-0949
                1477-9145
                15 January 2017
                15 January 2017
                : 220
                : 2
                : 147-160
                Affiliations
                [1 ]Division of Cardiovascular Science, School of Medicine, Faculty of Biology, Medicine and Health, University of Manchester , Manchester, M13 9NT, UK
                [2 ]Department of Rehabilitation Medicine, University of Washington , Seattle, WA 98109, USA
                [3 ]Department of Integrative Biology, University of Guelph , Guelph, Ontario, Canada N1G 2W1
                Author notes
                [* ]Author for correspondence ( tgillis@ 123456uoguelph.ca )
                Author information
                http://orcid.org/0000-0002-8585-0658
                Article
                JEB128496
                10.1242/jeb.128496
                5278617
                27852752
                f31098cf-9b39-4d1c-bf0f-da9985a67a44
                © 2017. Published by The Company of Biologists Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                Funding
                Funded by: Biotechnology and Biological Sciences Research Council, http://dx.doi.org/10.13039/501100000268;
                Funded by: Heart and Stroke Foundation of Canada;
                Funded by: Natural Sciences and Engineering Research Council of Canada, http://dx.doi.org/10.13039/501100000038;
                Funded by: Department of Fisheries and Oceans (Canada);
                Funded by: Canadian Foundation for Innovation;
                Categories
                Review

                Molecular biology
                cardiac function,cardiac histology,cardiac remodelling,connective tissue,thermal acclimation

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