Myogenic Cell Expression of Intercellular Adhesion Molecule-1 Contributes to Muscle Regeneration after Injury
This study investigated intercellular adhesion molecule-1 (ICAM-1), a membrane protein that mediates cell-to-cell adhesion and communication, as a mechanism through which the inflammatory response facilitates muscle regeneration after injury. Toxin-induced muscle injury to tibialis anterior muscles...
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| Veröffentlicht in: | The American journal of pathology 2020-10, Vol.190 (10), p.2039-2055 |
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| container_title | The American journal of pathology |
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| creator | Martin, Ryan A. Buckley, Kole H. Mankowski, Drew C. Riley, Benjamin M. Sidwell, Alena N. Douglas, Stephanie L. Worth, Randall G. Pizza, Francis X. |
| description | This study investigated intercellular adhesion molecule-1 (ICAM-1), a membrane protein that mediates cell-to-cell adhesion and communication, as a mechanism through which the inflammatory response facilitates muscle regeneration after injury. Toxin-induced muscle injury to tibialis anterior muscles of wild-type mice caused ICAM-1 to be expressed by a population of satellite cells/myoblasts and myofibers. Myogenic cell expression of ICAM-1 contributed to the restoration of muscle structure after injury, as regenerating myofibers were more abundant and myofiber size was larger for wild-type compared with Icam1−/− mice during 28 days of recovery. Contrastingly, restoration of muscle function after injury was similar between the genotypes. ICAM-1 facilitated the restoration of muscle structure after injury through mechanisms involving the regulation of myofiber branching, protein synthesis, and the organization of nuclei within myofibers after myogenic cell fusion. These findings provide support for a paradigm in which ICAM-1 expressed by myogenic cells after muscle injury augments their adhesive and fusogenic properties, which, in turn, facilitates regenerative and hypertrophic processes that restore structure to injured muscle. |
| doi_str_mv | 10.1016/j.ajpath.2020.06.009 |
| format | Article |
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Toxin-induced muscle injury to tibialis anterior muscles of wild-type mice caused ICAM-1 to be expressed by a population of satellite cells/myoblasts and myofibers. Myogenic cell expression of ICAM-1 contributed to the restoration of muscle structure after injury, as regenerating myofibers were more abundant and myofiber size was larger for wild-type compared with Icam1−/− mice during 28 days of recovery. Contrastingly, restoration of muscle function after injury was similar between the genotypes. ICAM-1 facilitated the restoration of muscle structure after injury through mechanisms involving the regulation of myofiber branching, protein synthesis, and the organization of nuclei within myofibers after myogenic cell fusion. These findings provide support for a paradigm in which ICAM-1 expressed by myogenic cells after muscle injury augments their adhesive and fusogenic properties, which, in turn, facilitates regenerative and hypertrophic processes that restore structure to injured muscle.</description><identifier>ISSN: 0002-9440</identifier><identifier>EISSN: 1525-2191</identifier><identifier>DOI: 10.1016/j.ajpath.2020.06.009</identifier><identifier>PMID: 32650005</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Cell Adhesion - physiology ; Cell Communication - physiology ; Female ; Hypertrophy - metabolism ; Intercellular Adhesion Molecule-1 - metabolism ; Male ; Mice, Inbred C57BL ; Muscle Development - physiology ; Muscle Fibers, Skeletal - metabolism ; Muscle, Skeletal - injuries ; Muscle, Skeletal - metabolism ; Regeneration - genetics ; Regular ; Satellite Cells, Skeletal Muscle - metabolism</subject><ispartof>The American journal of pathology, 2020-10, Vol.190 (10), p.2039-2055</ispartof><rights>2020 American Society for Investigative Pathology</rights><rights>Copyright © 2020 American Society for Investigative Pathology. Published by Elsevier Inc. All rights reserved.</rights><rights>2020 American Society for Investigative Pathology. Published by Elsevier Inc. All rights reserved. 2020 American Society for Investigative Pathology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c463t-83c03c37c350a46d9fcdfa6d730d8b857d90da518baef688058e94b7af8000ca3</citedby><cites>FETCH-LOGICAL-c463t-83c03c37c350a46d9fcdfa6d730d8b857d90da518baef688058e94b7af8000ca3</cites><orcidid>0000-0002-2626-7964 ; 0000-0002-5896-553X</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/PMC7527860/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.ajpath.2020.06.009$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,3550,27924,27925,45995,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32650005$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Martin, Ryan A.</creatorcontrib><creatorcontrib>Buckley, Kole H.</creatorcontrib><creatorcontrib>Mankowski, Drew C.</creatorcontrib><creatorcontrib>Riley, Benjamin M.</creatorcontrib><creatorcontrib>Sidwell, Alena N.</creatorcontrib><creatorcontrib>Douglas, Stephanie L.</creatorcontrib><creatorcontrib>Worth, Randall G.</creatorcontrib><creatorcontrib>Pizza, Francis X.</creatorcontrib><title>Myogenic Cell Expression of Intercellular Adhesion Molecule-1 Contributes to Muscle Regeneration after Injury</title><title>The American journal of pathology</title><addtitle>Am J Pathol</addtitle><description>This study investigated intercellular adhesion molecule-1 (ICAM-1), a membrane protein that mediates cell-to-cell adhesion and communication, as a mechanism through which the inflammatory response facilitates muscle regeneration after injury. Toxin-induced muscle injury to tibialis anterior muscles of wild-type mice caused ICAM-1 to be expressed by a population of satellite cells/myoblasts and myofibers. Myogenic cell expression of ICAM-1 contributed to the restoration of muscle structure after injury, as regenerating myofibers were more abundant and myofiber size was larger for wild-type compared with Icam1−/− mice during 28 days of recovery. Contrastingly, restoration of muscle function after injury was similar between the genotypes. ICAM-1 facilitated the restoration of muscle structure after injury through mechanisms involving the regulation of myofiber branching, protein synthesis, and the organization of nuclei within myofibers after myogenic cell fusion. These findings provide support for a paradigm in which ICAM-1 expressed by myogenic cells after muscle injury augments their adhesive and fusogenic properties, which, in turn, facilitates regenerative and hypertrophic processes that restore structure to injured muscle.</description><subject>Animals</subject><subject>Cell Adhesion - physiology</subject><subject>Cell Communication - physiology</subject><subject>Female</subject><subject>Hypertrophy - metabolism</subject><subject>Intercellular Adhesion Molecule-1 - metabolism</subject><subject>Male</subject><subject>Mice, Inbred C57BL</subject><subject>Muscle Development - physiology</subject><subject>Muscle Fibers, Skeletal - metabolism</subject><subject>Muscle, Skeletal - injuries</subject><subject>Muscle, Skeletal - metabolism</subject><subject>Regeneration - genetics</subject><subject>Regular</subject><subject>Satellite Cells, Skeletal Muscle - metabolism</subject><issn>0002-9440</issn><issn>1525-2191</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kU1v1DAQhi0EokvhHyCUI5eEsZ04zgWpWhWo1BVSVc6WY0-6jrLxYjsV--_xsqXQS0_WeN555uMl5D2FigIVn8ZKj3udthUDBhWICqB7QVa0YU3JaEdfkhUAsLKrazgjb2Iccyi4hNfkjDPR5KhZkd3m4O9wdqZY4zQVl7_2AWN0fi78UFzNCYPJ_8ukQ3Fht_gns_ETmmXCkhZrP6fg-iVhLJIvNks0ExY3mJEYdDqq9ZAhGTUu4fCWvBr0FPHdw3tOfny5vF1_K6-_f71aX1yXphY8lZIb4Ia3hjega2G7wdhBC9tysLKXTWs7sLqhstc4CCmhkdjVfasHmbcymp-Tzyfuful3aA3mKfWk9sHtdDgor516mpndVt35e9U2rJUCMuDjAyD4nwvGpHYuHi-hZ_RLVKxmHETLWp6l9Ulqgo8x4PDYhoI6OqVGdXJKHZ1SIFR2Kpd9-H_Ex6K_1vzbAfOh7h0GFY3D2aB1AU1S1rvnO_wG7Uqpbg</recordid><startdate>202010</startdate><enddate>202010</enddate><creator>Martin, Ryan A.</creator><creator>Buckley, Kole H.</creator><creator>Mankowski, Drew C.</creator><creator>Riley, Benjamin M.</creator><creator>Sidwell, Alena N.</creator><creator>Douglas, Stephanie L.</creator><creator>Worth, Randall G.</creator><creator>Pizza, Francis X.</creator><general>Elsevier Inc</general><general>American Society for Investigative Pathology</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2626-7964</orcidid><orcidid>https://orcid.org/0000-0002-5896-553X</orcidid></search><sort><creationdate>202010</creationdate><title>Myogenic Cell Expression of Intercellular Adhesion Molecule-1 Contributes to Muscle Regeneration after Injury</title><author>Martin, Ryan A. ; Buckley, Kole H. ; Mankowski, Drew C. ; Riley, Benjamin M. ; Sidwell, Alena N. ; Douglas, Stephanie L. ; Worth, Randall G. ; Pizza, Francis X.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c463t-83c03c37c350a46d9fcdfa6d730d8b857d90da518baef688058e94b7af8000ca3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Cell Adhesion - physiology</topic><topic>Cell Communication - physiology</topic><topic>Female</topic><topic>Hypertrophy - metabolism</topic><topic>Intercellular Adhesion Molecule-1 - metabolism</topic><topic>Male</topic><topic>Mice, Inbred C57BL</topic><topic>Muscle Development - physiology</topic><topic>Muscle Fibers, Skeletal - metabolism</topic><topic>Muscle, Skeletal - injuries</topic><topic>Muscle, Skeletal - metabolism</topic><topic>Regeneration - genetics</topic><topic>Regular</topic><topic>Satellite Cells, Skeletal Muscle - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Martin, Ryan A.</creatorcontrib><creatorcontrib>Buckley, Kole H.</creatorcontrib><creatorcontrib>Mankowski, Drew C.</creatorcontrib><creatorcontrib>Riley, Benjamin M.</creatorcontrib><creatorcontrib>Sidwell, Alena N.</creatorcontrib><creatorcontrib>Douglas, Stephanie L.</creatorcontrib><creatorcontrib>Worth, Randall G.</creatorcontrib><creatorcontrib>Pizza, Francis X.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The American journal of pathology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Martin, Ryan A.</au><au>Buckley, Kole H.</au><au>Mankowski, Drew C.</au><au>Riley, Benjamin M.</au><au>Sidwell, Alena N.</au><au>Douglas, Stephanie L.</au><au>Worth, Randall G.</au><au>Pizza, Francis X.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Myogenic Cell Expression of Intercellular Adhesion Molecule-1 Contributes to Muscle Regeneration after Injury</atitle><jtitle>The American journal of pathology</jtitle><addtitle>Am J Pathol</addtitle><date>2020-10</date><risdate>2020</risdate><volume>190</volume><issue>10</issue><spage>2039</spage><epage>2055</epage><pages>2039-2055</pages><issn>0002-9440</issn><eissn>1525-2191</eissn><abstract>This study investigated intercellular adhesion molecule-1 (ICAM-1), a membrane protein that mediates cell-to-cell adhesion and communication, as a mechanism through which the inflammatory response facilitates muscle regeneration after injury. Toxin-induced muscle injury to tibialis anterior muscles of wild-type mice caused ICAM-1 to be expressed by a population of satellite cells/myoblasts and myofibers. Myogenic cell expression of ICAM-1 contributed to the restoration of muscle structure after injury, as regenerating myofibers were more abundant and myofiber size was larger for wild-type compared with Icam1−/− mice during 28 days of recovery. Contrastingly, restoration of muscle function after injury was similar between the genotypes. ICAM-1 facilitated the restoration of muscle structure after injury through mechanisms involving the regulation of myofiber branching, protein synthesis, and the organization of nuclei within myofibers after myogenic cell fusion. These findings provide support for a paradigm in which ICAM-1 expressed by myogenic cells after muscle injury augments their adhesive and fusogenic properties, which, in turn, facilitates regenerative and hypertrophic processes that restore structure to injured muscle.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>32650005</pmid><doi>10.1016/j.ajpath.2020.06.009</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-2626-7964</orcidid><orcidid>https://orcid.org/0000-0002-5896-553X</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; ScienceDirect Journals (5 years ago - present); PubMed Central |
| subjects | Animals Cell Adhesion - physiology Cell Communication - physiology Female Hypertrophy - metabolism Intercellular Adhesion Molecule-1 - metabolism Male Mice, Inbred C57BL Muscle Development - physiology Muscle Fibers, Skeletal - metabolism Muscle, Skeletal - injuries Muscle, Skeletal - metabolism Regeneration - genetics Regular Satellite Cells, Skeletal Muscle - metabolism |
| title | Myogenic Cell Expression of Intercellular Adhesion Molecule-1 Contributes to Muscle Regeneration after Injury |
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