Cardiac hemodynamics and ventricular stiffness of sea-run cherry salmon (Oncorhynchus masou masou) differ critically from those of landlocked masu salmon
Ventricular diastolic mechanical properties are important determinants of cardiac function and are optimized by changes in cardiac structure and physical properties. Oncorhynchus masou masou is an anadromous migratory fish of the Salmonidae family, and several ecological studies on it have been cond...
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| Veröffentlicht in: | PloS one 2022-11, Vol.17 (11), p.e0267264-e0267264 |
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| creator | Usui, Yuu Kimoto, Misaki Hanashima, Akira Hashimoto, Ken Mohri, Satoshi |
| description | Ventricular diastolic mechanical properties are important determinants of cardiac function and are optimized by changes in cardiac structure and physical properties.
Oncorhynchus masou masou
is an anadromous migratory fish of the Salmonidae family, and several ecological studies on it have been conducted; however, the cardiac functions of the fish are not well known. Therefore, we investigated ventricular diastolic function in landlocked (masu salmon) and sea-run (cherry salmon) types at 29–30 months post fertilization. Pulsed-wave Doppler echocardiography showed that the atrioventricular inflow waveforms of cherry salmon were biphasic with early diastolic filling and atrial contraction, whereas those of masu salmon were monophasic with atrial contraction. In addition, end-diastolic pressure–volume relationship analysis revealed that the dilatability per unit myocardial mass of the ventricle in cherry salmon was significantly suppressed compared to that in masu salmon, suggesting that the ventricle of the cherry salmon was relatively stiffer (relative ventricular stiffness index;
p
= 0.0263). Contrastingly, the extensibility of cardiomyocytes, characterized by the expression pattern of Connectin isoforms in their ventricles, was similar in both types. Histological analysis showed that the percentage of the collagen accumulation area in the compact layer of cherry salmon increased compared with that of the masu salmon, which may contribute to ventricle stiffness. Although the heart mass of cherry salmon was about 11-fold greater than that of masu salmon, there was no difference in the morphology of the isolated cardiomyocytes, suggesting that the heart of the cherry salmon grows by cardiomyocyte proliferation, but not cell hypertrophy. The cardiac physiological function of the teleosts varies with differences in their developmental processes and life history. Our multidimensional analysis of the
O
.
masou
heart may provide a clue to the process by which the heart acquires a biphasic blood-filling pattern, i.e., a ventricular diastolic suction. |
| doi_str_mv | 10.1371/journal.pone.0267264 |
| format | Article |
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Oncorhynchus masou masou
is an anadromous migratory fish of the Salmonidae family, and several ecological studies on it have been conducted; however, the cardiac functions of the fish are not well known. Therefore, we investigated ventricular diastolic function in landlocked (masu salmon) and sea-run (cherry salmon) types at 29–30 months post fertilization. Pulsed-wave Doppler echocardiography showed that the atrioventricular inflow waveforms of cherry salmon were biphasic with early diastolic filling and atrial contraction, whereas those of masu salmon were monophasic with atrial contraction. In addition, end-diastolic pressure–volume relationship analysis revealed that the dilatability per unit myocardial mass of the ventricle in cherry salmon was significantly suppressed compared to that in masu salmon, suggesting that the ventricle of the cherry salmon was relatively stiffer (relative ventricular stiffness index;
p
= 0.0263). Contrastingly, the extensibility of cardiomyocytes, characterized by the expression pattern of Connectin isoforms in their ventricles, was similar in both types. Histological analysis showed that the percentage of the collagen accumulation area in the compact layer of cherry salmon increased compared with that of the masu salmon, which may contribute to ventricle stiffness. Although the heart mass of cherry salmon was about 11-fold greater than that of masu salmon, there was no difference in the morphology of the isolated cardiomyocytes, suggesting that the heart of the cherry salmon grows by cardiomyocyte proliferation, but not cell hypertrophy. The cardiac physiological function of the teleosts varies with differences in their developmental processes and life history. Our multidimensional analysis of the
O
.
masou
heart may provide a clue to the process by which the heart acquires a biphasic blood-filling pattern, i.e., a ventricular diastolic suction.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0267264</identifier><identifier>PMID: 36331913</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>Biology and Life Sciences ; Blood pressure ; Cardiology ; Cardiomyocytes ; Catheters ; Collagen ; Connectin ; Diastolic pressure ; Doppler effect ; Echocardiography ; Ecological studies ; Electrocardiography ; Experiments ; Fertilization ; Fish ; Fish migration ; Heart ; Hemodynamic monitoring ; Hemodynamics ; Hormones ; Hypertrophy ; Isoforms ; Life history ; Mechanical properties ; Medical research ; Medicine and Health Sciences ; Methods ; Oncorhynchus masou ; Oncorhynchus masou masou ; Physical properties ; Physical Sciences ; Research and Analysis Methods ; Salmon ; Stiffness ; Suction ; Ventricle ; Waveforms</subject><ispartof>PloS one, 2022-11, Vol.17 (11), p.e0267264-e0267264</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 Usui 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. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2022 Usui et al 2022 Usui et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c636t-6fdbc6afea2bb48d93a0f2eb61b1b1f11baa6a439a596c2463078c4af6187b33</citedby><cites>FETCH-LOGICAL-c636t-6fdbc6afea2bb48d93a0f2eb61b1b1f11baa6a439a596c2463078c4af6187b33</cites><orcidid>0000-0002-0232-6421 ; 0000-0001-8400-3441</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9635730/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9635730/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids></links><search><creatorcontrib>Usui, Yuu</creatorcontrib><creatorcontrib>Kimoto, Misaki</creatorcontrib><creatorcontrib>Hanashima, Akira</creatorcontrib><creatorcontrib>Hashimoto, Ken</creatorcontrib><creatorcontrib>Mohri, Satoshi</creatorcontrib><title>Cardiac hemodynamics and ventricular stiffness of sea-run cherry salmon (Oncorhynchus masou masou) differ critically from those of landlocked masu salmon</title><title>PloS one</title><description>Ventricular diastolic mechanical properties are important determinants of cardiac function and are optimized by changes in cardiac structure and physical properties.
Oncorhynchus masou masou
is an anadromous migratory fish of the Salmonidae family, and several ecological studies on it have been conducted; however, the cardiac functions of the fish are not well known. Therefore, we investigated ventricular diastolic function in landlocked (masu salmon) and sea-run (cherry salmon) types at 29–30 months post fertilization. Pulsed-wave Doppler echocardiography showed that the atrioventricular inflow waveforms of cherry salmon were biphasic with early diastolic filling and atrial contraction, whereas those of masu salmon were monophasic with atrial contraction. In addition, end-diastolic pressure–volume relationship analysis revealed that the dilatability per unit myocardial mass of the ventricle in cherry salmon was significantly suppressed compared to that in masu salmon, suggesting that the ventricle of the cherry salmon was relatively stiffer (relative ventricular stiffness index;
p
= 0.0263). Contrastingly, the extensibility of cardiomyocytes, characterized by the expression pattern of Connectin isoforms in their ventricles, was similar in both types. Histological analysis showed that the percentage of the collagen accumulation area in the compact layer of cherry salmon increased compared with that of the masu salmon, which may contribute to ventricle stiffness. Although the heart mass of cherry salmon was about 11-fold greater than that of masu salmon, there was no difference in the morphology of the isolated cardiomyocytes, suggesting that the heart of the cherry salmon grows by cardiomyocyte proliferation, but not cell hypertrophy. The cardiac physiological function of the teleosts varies with differences in their developmental processes and life history. Our multidimensional analysis of the
O
.
masou
heart may provide a clue to the process by which the heart acquires a biphasic blood-filling pattern, i.e., a ventricular diastolic suction.</description><subject>Biology and Life Sciences</subject><subject>Blood pressure</subject><subject>Cardiology</subject><subject>Cardiomyocytes</subject><subject>Catheters</subject><subject>Collagen</subject><subject>Connectin</subject><subject>Diastolic pressure</subject><subject>Doppler effect</subject><subject>Echocardiography</subject><subject>Ecological studies</subject><subject>Electrocardiography</subject><subject>Experiments</subject><subject>Fertilization</subject><subject>Fish</subject><subject>Fish migration</subject><subject>Heart</subject><subject>Hemodynamic monitoring</subject><subject>Hemodynamics</subject><subject>Hormones</subject><subject>Hypertrophy</subject><subject>Isoforms</subject><subject>Life history</subject><subject>Mechanical properties</subject><subject>Medical research</subject><subject>Medicine and Health 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hemodynamics and ventricular stiffness of sea-run cherry salmon (Oncorhynchus masou masou) differ critically from those of landlocked masu salmon</title><author>Usui, Yuu ; Kimoto, Misaki ; Hanashima, Akira ; Hashimoto, Ken ; Mohri, Satoshi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c636t-6fdbc6afea2bb48d93a0f2eb61b1b1f11baa6a439a596c2463078c4af6187b33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Biology and Life Sciences</topic><topic>Blood pressure</topic><topic>Cardiology</topic><topic>Cardiomyocytes</topic><topic>Catheters</topic><topic>Collagen</topic><topic>Connectin</topic><topic>Diastolic pressure</topic><topic>Doppler effect</topic><topic>Echocardiography</topic><topic>Ecological studies</topic><topic>Electrocardiography</topic><topic>Experiments</topic><topic>Fertilization</topic><topic>Fish</topic><topic>Fish migration</topic><topic>Heart</topic><topic>Hemodynamic monitoring</topic><topic>Hemodynamics</topic><topic>Hormones</topic><topic>Hypertrophy</topic><topic>Isoforms</topic><topic>Life history</topic><topic>Mechanical properties</topic><topic>Medical research</topic><topic>Medicine and Health Sciences</topic><topic>Methods</topic><topic>Oncorhynchus masou</topic><topic>Oncorhynchus masou masou</topic><topic>Physical properties</topic><topic>Physical Sciences</topic><topic>Research and Analysis Methods</topic><topic>Salmon</topic><topic>Stiffness</topic><topic>Suction</topic><topic>Ventricle</topic><topic>Waveforms</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Usui, Yuu</creatorcontrib><creatorcontrib>Kimoto, Misaki</creatorcontrib><creatorcontrib>Hanashima, Akira</creatorcontrib><creatorcontrib>Hashimoto, Ken</creatorcontrib><creatorcontrib>Mohri, Satoshi</creatorcontrib><collection>CrossRef</collection><collection>ProQuest Central 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Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Usui, Yuu</au><au>Kimoto, Misaki</au><au>Hanashima, Akira</au><au>Hashimoto, Ken</au><au>Mohri, Satoshi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cardiac hemodynamics and ventricular stiffness of sea-run cherry salmon (Oncorhynchus masou masou) differ critically from those of landlocked masu salmon</atitle><jtitle>PloS one</jtitle><date>2022-11-04</date><risdate>2022</risdate><volume>17</volume><issue>11</issue><spage>e0267264</spage><epage>e0267264</epage><pages>e0267264-e0267264</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Ventricular diastolic mechanical properties are important determinants of cardiac function and are optimized by changes in cardiac structure and physical properties.
Oncorhynchus masou masou
is an anadromous migratory fish of the Salmonidae family, and several ecological studies on it have been conducted; however, the cardiac functions of the fish are not well known. Therefore, we investigated ventricular diastolic function in landlocked (masu salmon) and sea-run (cherry salmon) types at 29–30 months post fertilization. Pulsed-wave Doppler echocardiography showed that the atrioventricular inflow waveforms of cherry salmon were biphasic with early diastolic filling and atrial contraction, whereas those of masu salmon were monophasic with atrial contraction. In addition, end-diastolic pressure–volume relationship analysis revealed that the dilatability per unit myocardial mass of the ventricle in cherry salmon was significantly suppressed compared to that in masu salmon, suggesting that the ventricle of the cherry salmon was relatively stiffer (relative ventricular stiffness index;
p
= 0.0263). Contrastingly, the extensibility of cardiomyocytes, characterized by the expression pattern of Connectin isoforms in their ventricles, was similar in both types. Histological analysis showed that the percentage of the collagen accumulation area in the compact layer of cherry salmon increased compared with that of the masu salmon, which may contribute to ventricle stiffness. Although the heart mass of cherry salmon was about 11-fold greater than that of masu salmon, there was no difference in the morphology of the isolated cardiomyocytes, suggesting that the heart of the cherry salmon grows by cardiomyocyte proliferation, but not cell hypertrophy. The cardiac physiological function of the teleosts varies with differences in their developmental processes and life history. Our multidimensional analysis of the
O
.
masou
heart may provide a clue to the process by which the heart acquires a biphasic blood-filling pattern, i.e., a ventricular diastolic suction.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><pmid>36331913</pmid><doi>10.1371/journal.pone.0267264</doi><orcidid>https://orcid.org/0000-0002-0232-6421</orcidid><orcidid>https://orcid.org/0000-0001-8400-3441</orcidid><oa>free_for_read</oa></addata></record> |
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| issn | 1932-6203 1932-6203 |
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| recordid | cdi_plos_journals_2731999601 |
| source | DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Biology and Life Sciences Blood pressure Cardiology Cardiomyocytes Catheters Collagen Connectin Diastolic pressure Doppler effect Echocardiography Ecological studies Electrocardiography Experiments Fertilization Fish Fish migration Heart Hemodynamic monitoring Hemodynamics Hormones Hypertrophy Isoforms Life history Mechanical properties Medical research Medicine and Health Sciences Methods Oncorhynchus masou Oncorhynchus masou masou Physical properties Physical Sciences Research and Analysis Methods Salmon Stiffness Suction Ventricle Waveforms |
| title | Cardiac hemodynamics and ventricular stiffness of sea-run cherry salmon (Oncorhynchus masou masou) differ critically from those of landlocked masu salmon |
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