Acute exhaustive aerobic exercise training impair cardiomyocyte function and calcium handling in Sprague-Dawley rats

Recent data from long-distance endurance participants suggest that cardiac function is impaired after completion. Existing data further indicate that right ventricular function is more affected than left ventricular function. The cellular mechanisms underpinning cardiac deterioration are limited and...

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Veröffentlicht in:PloS one 2017-03, Vol.12 (3), p.e0173449-e0173449
Hauptverfasser: Ljones, Kristine, Ness, Henning Ofstad, Solvang-Garten, Karin, Gaustad, Svein Erik, Høydal, Morten Andre
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Ness, Henning Ofstad
Solvang-Garten, Karin
Gaustad, Svein Erik
Høydal, Morten Andre
description Recent data from long-distance endurance participants suggest that cardiac function is impaired after completion. Existing data further indicate that right ventricular function is more affected than left ventricular function. The cellular mechanisms underpinning cardiac deterioration are limited and therefore the aim of this study was to examine cardiomyocyte and molecular responses of the right and left ventricle to an acute bout of exhaustive endurance exercise. Male Sprague-Dawley rats were assigned to sedentary controls or acute exhaustive endurance exercise consisting of a 120 minutes long forced treadmill run. The contractile function and Ca2+ handling properties in isolated cardiomyocytes, protein expression levels of sarcoplasmic reticulum Ca2+-ATPase and phospholamban including two of its phosphorylated states (serine 16 and threonine 17), and the mitochondrial respiration in permeabilized cardiac muscle fibers were analyzed. The exercise group showed a significant reduction in cardiomyocyte fractional shortening (right ventricle 1 Hz and 3 Hz p
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Existing data further indicate that right ventricular function is more affected than left ventricular function. The cellular mechanisms underpinning cardiac deterioration are limited and therefore the aim of this study was to examine cardiomyocyte and molecular responses of the right and left ventricle to an acute bout of exhaustive endurance exercise. Male Sprague-Dawley rats were assigned to sedentary controls or acute exhaustive endurance exercise consisting of a 120 minutes long forced treadmill run. The contractile function and Ca2+ handling properties in isolated cardiomyocytes, protein expression levels of sarcoplasmic reticulum Ca2+-ATPase and phospholamban including two of its phosphorylated states (serine 16 and threonine 17), and the mitochondrial respiration in permeabilized cardiac muscle fibers were analyzed. The exercise group showed a significant reduction in cardiomyocyte fractional shortening (right ventricle 1 Hz and 3 Hz p<0.001; left ventricle 1 Hz p<0.05), intracellular Ca2+ amplitude (right ventricle 1 and 3 Hz p<0.001; left ventricle 1 Hz p<0.01 and 3 Hz p<0.05) and rate of diastolic Ca2+ decay (right ventricle 1 Hz p<0.001 and 3 Hz p<0.01; left ventricle 1 and 3 Hz p<0.01). Cardiomyocyte relaxation during diastole was only significantly prolonged at 3 Hz in the right ventricle (p<0.05) compared to sedentary controls. We found an increase in phosphorylation of phospholamban at serine 16 and threonine 17 in the left (p<0.05), but not the right, ventricle from exhaustively exercised animals. The protein expression levels of sarcoplasmic reticulum Ca2+-ATPase and phospholamban was not changed. Furthermore, we found a reduction in maximal oxidative phosphorylation and electron transport system capacities of mitochondrial respiration in the right (p<0.01 and p<0.05, respectively), but not the left ventricle from rats subjected to acute exhaustive treadmill exercise. Acute exhaustive treadmill exercise is associated with impairment of cardiomyocyte Ca2+ handling and mitochondrial respiration that causes depression in both contraction and diastolic relaxation of cardiomyocytes.]]></description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0173449</identifier><identifier>PMID: 28273177</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adenosine triphosphatase ; Aerobic exercises ; Aerobics ; Animals ; Bioenergetics ; Biology and Life Sciences ; Biomarkers ; Ca2+-transporting ATPase ; Calcium ; Calcium (intracellular) ; Calcium (mitochondrial) ; Calcium (reticular) ; Calcium - metabolism ; Calcium ions ; Cardiac muscle ; Cardiology ; Cardiomyocytes ; Cell Membrane Permeability ; Cell Respiration ; Cells, Cultured ; Contraction ; Diastole ; Durability ; Electron transport ; Endurance ; Exercise ; Fitness equipment ; Handling ; Heart ; Heart - physiopathology ; Heart cells ; Heart diseases ; Ion transport ; Male ; Medical imaging ; Medicine ; Medicine and Health Sciences ; Mental depression ; Mitochondria ; Mitochondria, Heart - metabolism ; Muscle contraction ; Muscles ; Myocardial Contraction ; Myocardium - metabolism ; Myocytes, Cardiac - metabolism ; Observations ; Oxidative phosphorylation ; Phospholamban ; Phosphorylation ; Physical Conditioning, Animal ; Physical fitness ; Physical Sciences ; Physiological aspects ; Physiology ; Properties ; Pulmonary arteries ; Rats ; Rats, Sprague-Dawley ; Reduction ; Rehabilitation ; Research and Analysis Methods ; Respiration ; Rodents ; Running ; Sarcoplasmic reticulum ; Science ; Serine ; Studies ; Threonine ; Ventricle ; Working groups ; Workloads</subject><ispartof>PloS one, 2017-03, Vol.12 (3), p.e0173449-e0173449</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Ljones et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Existing data further indicate that right ventricular function is more affected than left ventricular function. The cellular mechanisms underpinning cardiac deterioration are limited and therefore the aim of this study was to examine cardiomyocyte and molecular responses of the right and left ventricle to an acute bout of exhaustive endurance exercise. Male Sprague-Dawley rats were assigned to sedentary controls or acute exhaustive endurance exercise consisting of a 120 minutes long forced treadmill run. The contractile function and Ca2+ handling properties in isolated cardiomyocytes, protein expression levels of sarcoplasmic reticulum Ca2+-ATPase and phospholamban including two of its phosphorylated states (serine 16 and threonine 17), and the mitochondrial respiration in permeabilized cardiac muscle fibers were analyzed. The exercise group showed a significant reduction in cardiomyocyte fractional shortening (right ventricle 1 Hz and 3 Hz p<0.001; left ventricle 1 Hz p<0.05), intracellular Ca2+ amplitude (right ventricle 1 and 3 Hz p<0.001; left ventricle 1 Hz p<0.01 and 3 Hz p<0.05) and rate of diastolic Ca2+ decay (right ventricle 1 Hz p<0.001 and 3 Hz p<0.01; left ventricle 1 and 3 Hz p<0.01). Cardiomyocyte relaxation during diastole was only significantly prolonged at 3 Hz in the right ventricle (p<0.05) compared to sedentary controls. We found an increase in phosphorylation of phospholamban at serine 16 and threonine 17 in the left (p<0.05), but not the right, ventricle from exhaustively exercised animals. The protein expression levels of sarcoplasmic reticulum Ca2+-ATPase and phospholamban was not changed. Furthermore, we found a reduction in maximal oxidative phosphorylation and electron transport system capacities of mitochondrial respiration in the right (p<0.01 and p<0.05, respectively), but not the left ventricle from rats subjected to acute exhaustive treadmill exercise. Acute exhaustive treadmill exercise is associated with impairment of cardiomyocyte Ca2+ handling and mitochondrial respiration that causes depression in both contraction and diastolic relaxation of cardiomyocytes.]]></description><subject>Adenosine triphosphatase</subject><subject>Aerobic exercises</subject><subject>Aerobics</subject><subject>Animals</subject><subject>Bioenergetics</subject><subject>Biology and Life Sciences</subject><subject>Biomarkers</subject><subject>Ca2+-transporting ATPase</subject><subject>Calcium</subject><subject>Calcium (intracellular)</subject><subject>Calcium (mitochondrial)</subject><subject>Calcium (reticular)</subject><subject>Calcium - metabolism</subject><subject>Calcium ions</subject><subject>Cardiac muscle</subject><subject>Cardiology</subject><subject>Cardiomyocytes</subject><subject>Cell Membrane Permeability</subject><subject>Cell Respiration</subject><subject>Cells, 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phosphorylation</subject><subject>Phospholamban</subject><subject>Phosphorylation</subject><subject>Physical Conditioning, Animal</subject><subject>Physical fitness</subject><subject>Physical Sciences</subject><subject>Physiological aspects</subject><subject>Physiology</subject><subject>Properties</subject><subject>Pulmonary arteries</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Reduction</subject><subject>Rehabilitation</subject><subject>Research and Analysis Methods</subject><subject>Respiration</subject><subject>Rodents</subject><subject>Running</subject><subject>Sarcoplasmic reticulum</subject><subject>Science</subject><subject>Serine</subject><subject>Studies</subject><subject>Threonine</subject><subject>Ventricle</subject><subject>Working 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exhaustive aerobic exercise training impair cardiomyocyte function and calcium handling in Sprague-Dawley rats</title><author>Ljones, Kristine ; Ness, Henning Ofstad ; Solvang-Garten, Karin ; Gaustad, Svein Erik ; Høydal, Morten Andre</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c791t-645d26eed563aabe9add24421f3f35b2d965ce5cfc217e4f48f31fe957d3e74d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Adenosine triphosphatase</topic><topic>Aerobic exercises</topic><topic>Aerobics</topic><topic>Animals</topic><topic>Bioenergetics</topic><topic>Biology and Life Sciences</topic><topic>Biomarkers</topic><topic>Ca2+-transporting ATPase</topic><topic>Calcium</topic><topic>Calcium (intracellular)</topic><topic>Calcium (mitochondrial)</topic><topic>Calcium (reticular)</topic><topic>Calcium - metabolism</topic><topic>Calcium ions</topic><topic>Cardiac 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Ofstad</au><au>Solvang-Garten, Karin</au><au>Gaustad, Svein Erik</au><au>Høydal, Morten Andre</au><au>González, Germán E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Acute exhaustive aerobic exercise training impair cardiomyocyte function and calcium handling in Sprague-Dawley rats</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-03-08</date><risdate>2017</risdate><volume>12</volume><issue>3</issue><spage>e0173449</spage><epage>e0173449</epage><pages>e0173449-e0173449</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract><![CDATA[Recent data from long-distance endurance participants suggest that cardiac function is impaired after completion. Existing data further indicate that right ventricular function is more affected than left ventricular function. The cellular mechanisms underpinning cardiac deterioration are limited and therefore the aim of this study was to examine cardiomyocyte and molecular responses of the right and left ventricle to an acute bout of exhaustive endurance exercise. Male Sprague-Dawley rats were assigned to sedentary controls or acute exhaustive endurance exercise consisting of a 120 minutes long forced treadmill run. The contractile function and Ca2+ handling properties in isolated cardiomyocytes, protein expression levels of sarcoplasmic reticulum Ca2+-ATPase and phospholamban including two of its phosphorylated states (serine 16 and threonine 17), and the mitochondrial respiration in permeabilized cardiac muscle fibers were analyzed. The exercise group showed a significant reduction in cardiomyocyte fractional shortening (right ventricle 1 Hz and 3 Hz p<0.001; left ventricle 1 Hz p<0.05), intracellular Ca2+ amplitude (right ventricle 1 and 3 Hz p<0.001; left ventricle 1 Hz p<0.01 and 3 Hz p<0.05) and rate of diastolic Ca2+ decay (right ventricle 1 Hz p<0.001 and 3 Hz p<0.01; left ventricle 1 and 3 Hz p<0.01). Cardiomyocyte relaxation during diastole was only significantly prolonged at 3 Hz in the right ventricle (p<0.05) compared to sedentary controls. We found an increase in phosphorylation of phospholamban at serine 16 and threonine 17 in the left (p<0.05), but not the right, ventricle from exhaustively exercised animals. The protein expression levels of sarcoplasmic reticulum Ca2+-ATPase and phospholamban was not changed. Furthermore, we found a reduction in maximal oxidative phosphorylation and electron transport system capacities of mitochondrial respiration in the right (p<0.01 and p<0.05, respectively), but not the left ventricle from rats subjected to acute exhaustive treadmill exercise. Acute exhaustive treadmill exercise is associated with impairment of cardiomyocyte Ca2+ handling and mitochondrial respiration that causes depression in both contraction and diastolic relaxation of cardiomyocytes.]]></abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28273177</pmid><doi>10.1371/journal.pone.0173449</doi><tpages>e0173449</tpages><oa>free_for_read</oa></addata></record>
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1932-6203
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subjects Adenosine triphosphatase
Aerobic exercises
Aerobics
Animals
Bioenergetics
Biology and Life Sciences
Biomarkers
Ca2+-transporting ATPase
Calcium
Calcium (intracellular)
Calcium (mitochondrial)
Calcium (reticular)
Calcium - metabolism
Calcium ions
Cardiac muscle
Cardiology
Cardiomyocytes
Cell Membrane Permeability
Cell Respiration
Cells, Cultured
Contraction
Diastole
Durability
Electron transport
Endurance
Exercise
Fitness equipment
Handling
Heart
Heart - physiopathology
Heart cells
Heart diseases
Ion transport
Male
Medical imaging
Medicine
Medicine and Health Sciences
Mental depression
Mitochondria
Mitochondria, Heart - metabolism
Muscle contraction
Muscles
Myocardial Contraction
Myocardium - metabolism
Myocytes, Cardiac - metabolism
Observations
Oxidative phosphorylation
Phospholamban
Phosphorylation
Physical Conditioning, Animal
Physical fitness
Physical Sciences
Physiological aspects
Physiology
Properties
Pulmonary arteries
Rats
Rats, Sprague-Dawley
Reduction
Rehabilitation
Research and Analysis Methods
Respiration
Rodents
Running
Sarcoplasmic reticulum
Science
Serine
Studies
Threonine
Ventricle
Working groups
Workloads
title Acute exhaustive aerobic exercise training impair cardiomyocyte function and calcium handling in Sprague-Dawley rats
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