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Quantification of sympathetic hyperinnervation and denervation after myocardial infarction by three-dimensional assessment of the cardiac sympathetic network in cleared transparent murine hearts
The sympathetic nervous system is critical in maintaining the normal physiological function of the heart. Its dysfunction in pathological states may exacerbate the substrate for arrhythmias. Obviously, knowledge of its three-dimensional (3D) structure is important, however, it has been revealed by c...
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| Published in: | PloS one 2017-07, Vol.12 (7), p.e0182072-e0182072 |
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| creator | Yokoyama, Teruki Lee, Jong-Kook Miwa, Keiko Opthof, Tobias Tomoyama, Satoki Nakanishi, Hiroyuki Yoshida, Akira Yasui, Haruyo Iida, Tadatsune Miyagawa, Shigeru Okabe, Shigeo Sawa, Yoshiki Sakata, Yasushi Komuro, Issei |
| description | The sympathetic nervous system is critical in maintaining the normal physiological function of the heart. Its dysfunction in pathological states may exacerbate the substrate for arrhythmias. Obviously, knowledge of its three-dimensional (3D) structure is important, however, it has been revealed by conventional methods only to a limited extent. In this study, a new method of tissue clearance in combination with immunostaining unravels the 3D structure of the sympathetic cardiac network as well as its changes after myocardial infarction.
Hearts isolated from adult male mice were optically cleared using the CUBIC-perfusion protocol. After making the hearts transparent, sympathetic nerves and coronary vessels were immunofluorescently labeled, and then images were acquired. The spatial distribution of sympathetic nerves was visualized not only along the epicardial surface, but also transmurally. They were distributed over the epicardial surface and penetrated into the myocardium to twist around coronary vessels, but also independent from the coronary vasculature. At 2 weeks after myocardial infarction, we were able to quantify both denervation distal from the site of infarction and nerve sprouting (hyperinnervation) at the ischemic border zone of the hearts in a 3D manner. The nerve density at the ischemic border zone was more than doubled in hearts with myocardial infarction compared to intact mice hearts (3D analyses; n = 5, p |
| doi_str_mv | 10.1371/journal.pone.0182072 |
| format | article |
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Hearts isolated from adult male mice were optically cleared using the CUBIC-perfusion protocol. After making the hearts transparent, sympathetic nerves and coronary vessels were immunofluorescently labeled, and then images were acquired. The spatial distribution of sympathetic nerves was visualized not only along the epicardial surface, but also transmurally. They were distributed over the epicardial surface and penetrated into the myocardium to twist around coronary vessels, but also independent from the coronary vasculature. At 2 weeks after myocardial infarction, we were able to quantify both denervation distal from the site of infarction and nerve sprouting (hyperinnervation) at the ischemic border zone of the hearts in a 3D manner. The nerve density at the ischemic border zone was more than doubled in hearts with myocardial infarction compared to intact mice hearts (3D analyses; n = 5, p<0.05).
There is both sympathetic hyperinnervation and denervation after myocardial infarction. Both can be visualized and quantified by a new imaging technique in transparent hearts and thereby become a useful tool in elucidating the role of the sympathetic nervous system in arrhythmias associated with myocardial infarction.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0182072</identifier><identifier>PMID: 28753665</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Arrhythmias, Cardiac - metabolism ; Arrhythmias, Cardiac - pathology ; Biology and Life Sciences ; Blood vessels ; Cardiology ; Cardiomyopathy ; Care and treatment ; Coronary artery disease ; Coronary Vessels - metabolism ; Coronary Vessels - pathology ; Denervation ; Engineering and Technology ; Fluorescent antibody technique ; Heart ; Heart - innervation ; Heart attack ; Heart attacks ; Heart diseases ; Heart surgery ; Image acquisition ; Infarction ; Ischemia ; Laboratory animals ; Male ; Medicine ; Medicine and Health Sciences ; Methods ; Mice ; Myocardial infarction ; Myocardial Infarction - metabolism ; Myocardial Infarction - pathology ; Myocardium ; Myocardium - metabolism ; Myocardium - pathology ; Nerves ; Nervous system ; Neurobiology ; Neurosciences ; Ostomy ; Perfusion ; Research and Analysis Methods ; Spatial distribution ; Substrates ; Sympathetic nerves ; Sympathetic nervous system ; Sympathetic Nervous System - metabolism ; Sympathetic Nervous System - pathology ; Three dimensional imaging ; University graduates ; Ventilators</subject><ispartof>PloS one, 2017-07, Vol.12 (7), p.e0182072-e0182072</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Yokoyama 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>2017 Yokoyama et al 2017 Yokoyama et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c842t-b5fd81fb3b9fb75407fd3824fadf6ed76a39aab6119c22e1b84368e5855db4a3</citedby><cites>FETCH-LOGICAL-c842t-b5fd81fb3b9fb75407fd3824fadf6ed76a39aab6119c22e1b84368e5855db4a3</cites><orcidid>0000-0001-9053-7781</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1991551042/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1991551042?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28753665$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Bando, Yasuko</contributor><creatorcontrib>Yokoyama, Teruki</creatorcontrib><creatorcontrib>Lee, Jong-Kook</creatorcontrib><creatorcontrib>Miwa, Keiko</creatorcontrib><creatorcontrib>Opthof, Tobias</creatorcontrib><creatorcontrib>Tomoyama, Satoki</creatorcontrib><creatorcontrib>Nakanishi, Hiroyuki</creatorcontrib><creatorcontrib>Yoshida, Akira</creatorcontrib><creatorcontrib>Yasui, Haruyo</creatorcontrib><creatorcontrib>Iida, Tadatsune</creatorcontrib><creatorcontrib>Miyagawa, Shigeru</creatorcontrib><creatorcontrib>Okabe, Shigeo</creatorcontrib><creatorcontrib>Sawa, Yoshiki</creatorcontrib><creatorcontrib>Sakata, Yasushi</creatorcontrib><creatorcontrib>Komuro, Issei</creatorcontrib><title>Quantification of sympathetic hyperinnervation and denervation after myocardial infarction by three-dimensional assessment of the cardiac sympathetic network in cleared transparent murine hearts</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The sympathetic nervous system is critical in maintaining the normal physiological function of the heart. Its dysfunction in pathological states may exacerbate the substrate for arrhythmias. Obviously, knowledge of its three-dimensional (3D) structure is important, however, it has been revealed by conventional methods only to a limited extent. In this study, a new method of tissue clearance in combination with immunostaining unravels the 3D structure of the sympathetic cardiac network as well as its changes after myocardial infarction.
Hearts isolated from adult male mice were optically cleared using the CUBIC-perfusion protocol. After making the hearts transparent, sympathetic nerves and coronary vessels were immunofluorescently labeled, and then images were acquired. The spatial distribution of sympathetic nerves was visualized not only along the epicardial surface, but also transmurally. They were distributed over the epicardial surface and penetrated into the myocardium to twist around coronary vessels, but also independent from the coronary vasculature. At 2 weeks after myocardial infarction, we were able to quantify both denervation distal from the site of infarction and nerve sprouting (hyperinnervation) at the ischemic border zone of the hearts in a 3D manner. The nerve density at the ischemic border zone was more than doubled in hearts with myocardial infarction compared to intact mice hearts (3D analyses; n = 5, p<0.05).
There is both sympathetic hyperinnervation and denervation after myocardial infarction. Both can be visualized and quantified by a new imaging technique in transparent hearts and thereby become a useful tool in elucidating the role of the sympathetic nervous system in arrhythmias associated with myocardial infarction.</description><subject>Animals</subject><subject>Arrhythmias, Cardiac - metabolism</subject><subject>Arrhythmias, Cardiac - pathology</subject><subject>Biology and Life Sciences</subject><subject>Blood vessels</subject><subject>Cardiology</subject><subject>Cardiomyopathy</subject><subject>Care and treatment</subject><subject>Coronary artery disease</subject><subject>Coronary Vessels - metabolism</subject><subject>Coronary Vessels - pathology</subject><subject>Denervation</subject><subject>Engineering and Technology</subject><subject>Fluorescent antibody technique</subject><subject>Heart</subject><subject>Heart - innervation</subject><subject>Heart attack</subject><subject>Heart attacks</subject><subject>Heart diseases</subject><subject>Heart surgery</subject><subject>Image acquisition</subject><subject>Infarction</subject><subject>Ischemia</subject><subject>Laboratory animals</subject><subject>Male</subject><subject>Medicine</subject><subject>Medicine and Health Sciences</subject><subject>Methods</subject><subject>Mice</subject><subject>Myocardial infarction</subject><subject>Myocardial Infarction - metabolism</subject><subject>Myocardial Infarction - pathology</subject><subject>Myocardium</subject><subject>Myocardium - metabolism</subject><subject>Myocardium - pathology</subject><subject>Nerves</subject><subject>Nervous system</subject><subject>Neurobiology</subject><subject>Neurosciences</subject><subject>Ostomy</subject><subject>Perfusion</subject><subject>Research and Analysis Methods</subject><subject>Spatial distribution</subject><subject>Substrates</subject><subject>Sympathetic nerves</subject><subject>Sympathetic nervous system</subject><subject>Sympathetic Nervous System - metabolism</subject><subject>Sympathetic Nervous System - pathology</subject><subject>Three dimensional imaging</subject><subject>University graduates</subject><subject>Ventilators</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNU9uO0zAQjRCIXQp_gCASEoKHlvia5AVpteJSaaUVsOLVmvjSuiRxsZ2F_h5fhrPtrhq0DygPsWfOOXPxTJY9R8UCkRK927jB99Autq7XiwJVuCjxg-wU1QTPOS7Iw6PzSfYkhE1RMFJx_jg7wVXJCOfsNPvzZYA-WmMlROv63Jk87LotxLWOVubr3VZ72_faX-_90Ktc6aO7idrn3c5J8MpCm9vegJc3vmaXx7XXeq5sp_uQTMkPIegQ0j2OsVKYfM-Uk7i9jr-c_5HUctlq8Frl0UMftumYmN2QktL5OnlieJo9MtAG_ezwn2VXHz9cnX-eX1x-Wp6fXcxlRXGcN8yoCpmGNLVpSkaL0ihSYWpAGa5VyYHUAA1HqJYYa9RUlPBKs4ox1VAgs-zlXnbbuiAO3Q8C1TViDBUUJ8Ryj1AONmLrbQd-JxxYcWNwfiVSvjYVJEiByrqispK0prLAFTWsBFwZQIA510nr_SHa0HRayVS1h3YiOvX0di1W7lowRgildRJ4cxDw7uegQxSdDVK3LfTaDWPemPICoTQTs-zVP9D7qzugVpAKSM_sUlw5ioozWteccMxHrcU9qPQp3VmZRtXYZJ8Q3k4ICRP177iCIQSx_Pb1_7GX36fY10fYNCltXAfXDuNkhimQ7oHSuxC8NndNRoUYN-22G2LcNHHYtER7cfxAd6Tb1SJ_AUapKlk</recordid><startdate>20170728</startdate><enddate>20170728</enddate><creator>Yokoyama, Teruki</creator><creator>Lee, Jong-Kook</creator><creator>Miwa, Keiko</creator><creator>Opthof, Tobias</creator><creator>Tomoyama, Satoki</creator><creator>Nakanishi, Hiroyuki</creator><creator>Yoshida, Akira</creator><creator>Yasui, Haruyo</creator><creator>Iida, Tadatsune</creator><creator>Miyagawa, Shigeru</creator><creator>Okabe, Shigeo</creator><creator>Sawa, Yoshiki</creator><creator>Sakata, Yasushi</creator><creator>Komuro, Issei</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-9053-7781</orcidid></search><sort><creationdate>20170728</creationdate><title>Quantification of sympathetic hyperinnervation and denervation after myocardial infarction by three-dimensional assessment of the cardiac sympathetic network in cleared transparent murine hearts</title><author>Yokoyama, Teruki ; Lee, Jong-Kook ; Miwa, Keiko ; Opthof, Tobias ; Tomoyama, Satoki ; Nakanishi, Hiroyuki ; Yoshida, Akira ; Yasui, Haruyo ; Iida, Tadatsune ; Miyagawa, Shigeru ; Okabe, Shigeo ; Sawa, Yoshiki ; Sakata, Yasushi ; Komuro, Issei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c842t-b5fd81fb3b9fb75407fd3824fadf6ed76a39aab6119c22e1b84368e5855db4a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Arrhythmias, Cardiac - 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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>Yokoyama, Teruki</au><au>Lee, Jong-Kook</au><au>Miwa, Keiko</au><au>Opthof, Tobias</au><au>Tomoyama, Satoki</au><au>Nakanishi, Hiroyuki</au><au>Yoshida, Akira</au><au>Yasui, Haruyo</au><au>Iida, Tadatsune</au><au>Miyagawa, Shigeru</au><au>Okabe, Shigeo</au><au>Sawa, Yoshiki</au><au>Sakata, Yasushi</au><au>Komuro, Issei</au><au>Bando, Yasuko</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Quantification of sympathetic hyperinnervation and denervation after myocardial infarction by three-dimensional assessment of the cardiac sympathetic network in cleared transparent murine hearts</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-07-28</date><risdate>2017</risdate><volume>12</volume><issue>7</issue><spage>e0182072</spage><epage>e0182072</epage><pages>e0182072-e0182072</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The sympathetic nervous system is critical in maintaining the normal physiological function of the heart. Its dysfunction in pathological states may exacerbate the substrate for arrhythmias. Obviously, knowledge of its three-dimensional (3D) structure is important, however, it has been revealed by conventional methods only to a limited extent. In this study, a new method of tissue clearance in combination with immunostaining unravels the 3D structure of the sympathetic cardiac network as well as its changes after myocardial infarction.
Hearts isolated from adult male mice were optically cleared using the CUBIC-perfusion protocol. After making the hearts transparent, sympathetic nerves and coronary vessels were immunofluorescently labeled, and then images were acquired. The spatial distribution of sympathetic nerves was visualized not only along the epicardial surface, but also transmurally. They were distributed over the epicardial surface and penetrated into the myocardium to twist around coronary vessels, but also independent from the coronary vasculature. At 2 weeks after myocardial infarction, we were able to quantify both denervation distal from the site of infarction and nerve sprouting (hyperinnervation) at the ischemic border zone of the hearts in a 3D manner. The nerve density at the ischemic border zone was more than doubled in hearts with myocardial infarction compared to intact mice hearts (3D analyses; n = 5, p<0.05).
There is both sympathetic hyperinnervation and denervation after myocardial infarction. Both can be visualized and quantified by a new imaging technique in transparent hearts and thereby become a useful tool in elucidating the role of the sympathetic nervous system in arrhythmias associated with myocardial infarction.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28753665</pmid><doi>10.1371/journal.pone.0182072</doi><tpages>e0182072</tpages><orcidid>https://orcid.org/0000-0001-9053-7781</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2017-07, Vol.12 (7), p.e0182072-e0182072 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1991551042 |
| source | PubMed (Medline); ProQuest - Publicly Available Content Database |
| subjects | Animals Arrhythmias, Cardiac - metabolism Arrhythmias, Cardiac - pathology Biology and Life Sciences Blood vessels Cardiology Cardiomyopathy Care and treatment Coronary artery disease Coronary Vessels - metabolism Coronary Vessels - pathology Denervation Engineering and Technology Fluorescent antibody technique Heart Heart - innervation Heart attack Heart attacks Heart diseases Heart surgery Image acquisition Infarction Ischemia Laboratory animals Male Medicine Medicine and Health Sciences Methods Mice Myocardial infarction Myocardial Infarction - metabolism Myocardial Infarction - pathology Myocardium Myocardium - metabolism Myocardium - pathology Nerves Nervous system Neurobiology Neurosciences Ostomy Perfusion Research and Analysis Methods Spatial distribution Substrates Sympathetic nerves Sympathetic nervous system Sympathetic Nervous System - metabolism Sympathetic Nervous System - pathology Three dimensional imaging University graduates Ventilators |
| title | Quantification of sympathetic hyperinnervation and denervation after myocardial infarction by three-dimensional assessment of the cardiac sympathetic network in cleared transparent murine hearts |
| url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-01T06%3A45%3A50IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Quantification%20of%20sympathetic%20hyperinnervation%20and%20denervation%20after%20myocardial%20infarction%20by%20three-dimensional%20assessment%20of%20the%20cardiac%20sympathetic%20network%20in%20cleared%20transparent%20murine%20hearts&rft.jtitle=PloS%20one&rft.au=Yokoyama,%20Teruki&rft.date=2017-07-28&rft.volume=12&rft.issue=7&rft.spage=e0182072&rft.epage=e0182072&rft.pages=e0182072-e0182072&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0182072&rft_dat=%3Cgale_plos_%3EA499636265%3C/gale_plos_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c842t-b5fd81fb3b9fb75407fd3824fadf6ed76a39aab6119c22e1b84368e5855db4a3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=1991551042&rft_id=info:pmid/28753665&rft_galeid=A499636265&rfr_iscdi=true |