Recurrent heat shock impairs the proliferation and differentiation of C2C12 myoblasts
Heat-related illness and injury are becoming a growing safety concern for the farmers, construction workers, miners, firefighters, manufacturing workers, and other outdoor workforces who are exposed to heat stress in their routine lives. A primary response by a cell to an acute heat shock (HS) expos...
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| Veröffentlicht in: | Cell stress & chaperones 2018-05, Vol.23 (3), p.399-410 |
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| creator | Bolus, Daniel J. Shanmugam, Gobinath Narasimhan, Madhusudhanan Rajasekaran, Namakkal S. |
| description | Heat-related illness and injury are becoming a growing safety concern for the farmers, construction workers, miners, firefighters, manufacturing workers, and other outdoor workforces who are exposed to heat stress in their routine lives. A primary response by a cell to an acute heat shock (HS) exposure is the induction of heat-shock proteins (HSPs), which chaperone and facilitate cellular protein folding and remodeling processes. While acute HS is well studied, the effect of repeated bouts of hyperthermia and the sustained production of HSPs in the myoblast-myotube model system of C2C12 cells are poorly characterized. In C2C12 myoblasts, we found that robust HS (43 °C, dose/time) significantly decreased the proliferation by 50% as early as on day 1 and maintained at the same level on days 2 and 3 of HS. This was accompanied by an accumulation of cells at G2 phase with reduced cell number in G1 phase indicating cell cycle arrest. FACS analysis indicates that there was no apparent change in apoptosis (markers) and cell death upon repeated HS. Immunoblot analysis and qPCR demonstrated a significant increase in the baseline expression of HSP25, 70, and 90 (among others) in cells after a single HS (43 °C) for 60 min as a typical HS response. Importantly, the repeated HS for 60 min each on days 2 and 3 maintained the elevated levels of HSPs compared to the control cells. Further, the continuous HS exposure resulted in significant inhibition of the differentiation of C2C12 myocytes to myotubes and only 1/10th of the cells underwent differentiation in HS relative to control. This was associated with significantly higher levels of HSPs and reduced expression of myogenin and Myh2 (P < 0.05), the genes involved in the differentiation process. Finally, the cell migration (scratch) assay indicated that the wound closure was significantly delayed in HS cells relative to the control cells. Overall, these results suggest that a repeated HS may perturb the active process of proliferation, motility, and differentiation processes in an in vitro murine myoblast-myotube model. |
| doi_str_mv | 10.1007/s12192-017-0851-4 |
| format | Article |
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A primary response by a cell to an acute heat shock (HS) exposure is the induction of heat-shock proteins (HSPs), which chaperone and facilitate cellular protein folding and remodeling processes. While acute HS is well studied, the effect of repeated bouts of hyperthermia and the sustained production of HSPs in the myoblast-myotube model system of C2C12 cells are poorly characterized. In C2C12 myoblasts, we found that robust HS (43 °C, dose/time) significantly decreased the proliferation by 50% as early as on day 1 and maintained at the same level on days 2 and 3 of HS. This was accompanied by an accumulation of cells at G2 phase with reduced cell number in G1 phase indicating cell cycle arrest. FACS analysis indicates that there was no apparent change in apoptosis (markers) and cell death upon repeated HS. Immunoblot analysis and qPCR demonstrated a significant increase in the baseline expression of HSP25, 70, and 90 (among others) in cells after a single HS (43 °C) for 60 min as a typical HS response. Importantly, the repeated HS for 60 min each on days 2 and 3 maintained the elevated levels of HSPs compared to the control cells. Further, the continuous HS exposure resulted in significant inhibition of the differentiation of C2C12 myocytes to myotubes and only 1/10th of the cells underwent differentiation in HS relative to control. This was associated with significantly higher levels of HSPs and reduced expression of myogenin and Myh2 (P < 0.05), the genes involved in the differentiation process. Finally, the cell migration (scratch) assay indicated that the wound closure was significantly delayed in HS cells relative to the control cells. Overall, these results suggest that a repeated HS may perturb the active process of proliferation, motility, and differentiation processes in an in vitro murine myoblast-myotube model.</description><identifier>ISSN: 1355-8145</identifier><identifier>EISSN: 1466-1268</identifier><identifier>DOI: 10.1007/s12192-017-0851-4</identifier><identifier>PMID: 29063376</identifier><language>eng</language><publisher>Dordrecht: Springer</publisher><subject>Animals ; Apoptosis ; Apoptosis - genetics ; Biochemistry ; Biomedical and Life Sciences ; Biomedicine ; Boluses ; Cancer Research ; Cell adhesion & migration ; Cell Biology ; Cell cycle ; Cell Cycle - genetics ; Cell death ; Cell Differentiation ; Cell growth ; Cell migration ; Cell Movement - genetics ; Cell number ; Cell Proliferation ; Cells, Cultured ; Cellular differentiation ; Construction industry ; Differentiation ; Exposure ; Firefighters ; Flow cytometry ; G1 phase ; G2 phase ; Gene expression ; Heat shock ; Heat shock proteins ; Heat stress ; Heat tolerance ; Heat-Shock Proteins - genetics ; Heat-Shock Proteins - metabolism ; Heat-Shock Response ; Hsp25 protein ; Hyperthermia ; Immunology ; Messenger RNA ; Mice ; Miners ; Mining ; Muscle fibers ; Myoblasts ; Myoblasts - metabolism ; Myoblasts - pathology ; Myocytes ; Myogenin ; Myotubes ; Neurosciences ; Occupational exposure ; Occupational health ; Original Paper ; Protein Biosynthesis ; Protein folding ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Transcription, Genetic ; Working conditions</subject><ispartof>Cell stress & chaperones, 2018-05, Vol.23 (3), p.399-410</ispartof><rights>Cell Stress Society International 2018</rights><rights>Cell Stress Society International 2017</rights><rights>Cell Stress and Chaperones is a copyright of Springer, (2017). All Rights Reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c492t-aee7d64049ec15c71f69ab1aad4db26c53ff0c501b9ecfa1f55d30c9a77c77803</citedby><cites>FETCH-LOGICAL-c492t-aee7d64049ec15c71f69ab1aad4db26c53ff0c501b9ecfa1f55d30c9a77c77803</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/44851641$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/44851641$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,41464,42533,51294,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29063376$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bolus, Daniel J.</creatorcontrib><creatorcontrib>Shanmugam, Gobinath</creatorcontrib><creatorcontrib>Narasimhan, Madhusudhanan</creatorcontrib><creatorcontrib>Rajasekaran, Namakkal S.</creatorcontrib><title>Recurrent heat shock impairs the proliferation and differentiation of C2C12 myoblasts</title><title>Cell stress & chaperones</title><addtitle>Cell Stress and Chaperones</addtitle><addtitle>Cell Stress Chaperones</addtitle><description>Heat-related illness and injury are becoming a growing safety concern for the farmers, construction workers, miners, firefighters, manufacturing workers, and other outdoor workforces who are exposed to heat stress in their routine lives. A primary response by a cell to an acute heat shock (HS) exposure is the induction of heat-shock proteins (HSPs), which chaperone and facilitate cellular protein folding and remodeling processes. While acute HS is well studied, the effect of repeated bouts of hyperthermia and the sustained production of HSPs in the myoblast-myotube model system of C2C12 cells are poorly characterized. In C2C12 myoblasts, we found that robust HS (43 °C, dose/time) significantly decreased the proliferation by 50% as early as on day 1 and maintained at the same level on days 2 and 3 of HS. This was accompanied by an accumulation of cells at G2 phase with reduced cell number in G1 phase indicating cell cycle arrest. FACS analysis indicates that there was no apparent change in apoptosis (markers) and cell death upon repeated HS. Immunoblot analysis and qPCR demonstrated a significant increase in the baseline expression of HSP25, 70, and 90 (among others) in cells after a single HS (43 °C) for 60 min as a typical HS response. Importantly, the repeated HS for 60 min each on days 2 and 3 maintained the elevated levels of HSPs compared to the control cells. Further, the continuous HS exposure resulted in significant inhibition of the differentiation of C2C12 myocytes to myotubes and only 1/10th of the cells underwent differentiation in HS relative to control. This was associated with significantly higher levels of HSPs and reduced expression of myogenin and Myh2 (P < 0.05), the genes involved in the differentiation process. Finally, the cell migration (scratch) assay indicated that the wound closure was significantly delayed in HS cells relative to the control cells. Overall, these results suggest that a repeated HS may perturb the active process of proliferation, motility, and differentiation processes in an in vitro murine myoblast-myotube model.</description><subject>Animals</subject><subject>Apoptosis</subject><subject>Apoptosis - genetics</subject><subject>Biochemistry</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Boluses</subject><subject>Cancer Research</subject><subject>Cell adhesion & migration</subject><subject>Cell Biology</subject><subject>Cell cycle</subject><subject>Cell Cycle - genetics</subject><subject>Cell death</subject><subject>Cell Differentiation</subject><subject>Cell growth</subject><subject>Cell migration</subject><subject>Cell Movement - genetics</subject><subject>Cell number</subject><subject>Cell Proliferation</subject><subject>Cells, Cultured</subject><subject>Cellular differentiation</subject><subject>Construction industry</subject><subject>Differentiation</subject><subject>Exposure</subject><subject>Firefighters</subject><subject>Flow cytometry</subject><subject>G1 phase</subject><subject>G2 phase</subject><subject>Gene expression</subject><subject>Heat shock</subject><subject>Heat shock proteins</subject><subject>Heat stress</subject><subject>Heat tolerance</subject><subject>Heat-Shock Proteins - genetics</subject><subject>Heat-Shock Proteins - metabolism</subject><subject>Heat-Shock Response</subject><subject>Hsp25 protein</subject><subject>Hyperthermia</subject><subject>Immunology</subject><subject>Messenger RNA</subject><subject>Mice</subject><subject>Miners</subject><subject>Mining</subject><subject>Muscle fibers</subject><subject>Myoblasts</subject><subject>Myoblasts - metabolism</subject><subject>Myoblasts - pathology</subject><subject>Myocytes</subject><subject>Myogenin</subject><subject>Myotubes</subject><subject>Neurosciences</subject><subject>Occupational exposure</subject><subject>Occupational health</subject><subject>Original Paper</subject><subject>Protein Biosynthesis</subject><subject>Protein folding</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Transcription, Genetic</subject><subject>Working conditions</subject><issn>1355-8145</issn><issn>1466-1268</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp9kUtv1TAQhS0Eog_4ASxAkdiwCcz4mWyQ0BUUpEqVKrq2HMfu9SWJL3aC1H-Pr1Iu0EVXfsx3zszoEPIK4T0CqA8ZKba0BlQ1NAJr_oScIpeyRiqbp-XOhKgb5OKEnOW8g6JRCp-TE9qCZEzJU3Jz7eySkpvmauvMXOVttD-qMO5NSLmat67apzgE75KZQ5wqM_VVH3x5F0lY_6KvNnSDtBrvYjeYPOcX5Jk3Q3Yv789zcvPl8_fN1_ry6uLb5tNlbXlL59o4p3rJgbfOorAKvWxNh8b0vO-otIJ5D1YAdgXwBr0QPQPbGqWsUg2wc_Jx9d0v3eh6W2ZKZtD7FEaT7nQ0Qf9fmcJW38ZfWrTAoeHF4N29QYo_F5dnPYZs3TCYycUla2yFAMUAZUHfPkB3cUlTWU9ToJIhpfJgiCtlU8w5OX8cBkEfQtNraLqEpg-h6YPmzb9bHBV_UioAXYFcStOtS39bP-b6ehXt8hzT0ZTzUpYc2W9X4Kzx</recordid><startdate>20180501</startdate><enddate>20180501</enddate><creator>Bolus, Daniel J.</creator><creator>Shanmugam, Gobinath</creator><creator>Narasimhan, Madhusudhanan</creator><creator>Rajasekaran, Namakkal S.</creator><general>Springer</general><general>Springer Netherlands</general><general>Springer Nature B.V</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>3V.</scope><scope>7QL</scope><scope>7QP</scope><scope>7T7</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</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>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20180501</creationdate><title>Recurrent heat shock impairs the proliferation and differentiation of C2C12 myoblasts</title><author>Bolus, Daniel J. ; Shanmugam, Gobinath ; Narasimhan, Madhusudhanan ; Rajasekaran, Namakkal S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c492t-aee7d64049ec15c71f69ab1aad4db26c53ff0c501b9ecfa1f55d30c9a77c77803</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Animals</topic><topic>Apoptosis</topic><topic>Apoptosis - genetics</topic><topic>Biochemistry</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Boluses</topic><topic>Cancer Research</topic><topic>Cell adhesion & migration</topic><topic>Cell Biology</topic><topic>Cell cycle</topic><topic>Cell Cycle - genetics</topic><topic>Cell death</topic><topic>Cell Differentiation</topic><topic>Cell growth</topic><topic>Cell migration</topic><topic>Cell Movement - genetics</topic><topic>Cell number</topic><topic>Cell Proliferation</topic><topic>Cells, Cultured</topic><topic>Cellular differentiation</topic><topic>Construction industry</topic><topic>Differentiation</topic><topic>Exposure</topic><topic>Firefighters</topic><topic>Flow cytometry</topic><topic>G1 phase</topic><topic>G2 phase</topic><topic>Gene expression</topic><topic>Heat shock</topic><topic>Heat shock proteins</topic><topic>Heat stress</topic><topic>Heat tolerance</topic><topic>Heat-Shock Proteins - genetics</topic><topic>Heat-Shock Proteins - metabolism</topic><topic>Heat-Shock Response</topic><topic>Hsp25 protein</topic><topic>Hyperthermia</topic><topic>Immunology</topic><topic>Messenger RNA</topic><topic>Mice</topic><topic>Miners</topic><topic>Mining</topic><topic>Muscle fibers</topic><topic>Myoblasts</topic><topic>Myoblasts - metabolism</topic><topic>Myoblasts - pathology</topic><topic>Myocytes</topic><topic>Myogenin</topic><topic>Myotubes</topic><topic>Neurosciences</topic><topic>Occupational exposure</topic><topic>Occupational health</topic><topic>Original Paper</topic><topic>Protein Biosynthesis</topic><topic>Protein folding</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Transcription, Genetic</topic><topic>Working conditions</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bolus, Daniel J.</creatorcontrib><creatorcontrib>Shanmugam, Gobinath</creatorcontrib><creatorcontrib>Narasimhan, Madhusudhanan</creatorcontrib><creatorcontrib>Rajasekaran, Namakkal S.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Cell stress & chaperones</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bolus, Daniel J.</au><au>Shanmugam, Gobinath</au><au>Narasimhan, Madhusudhanan</au><au>Rajasekaran, Namakkal S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Recurrent heat shock impairs the proliferation and differentiation of C2C12 myoblasts</atitle><jtitle>Cell stress & chaperones</jtitle><stitle>Cell Stress and Chaperones</stitle><addtitle>Cell Stress Chaperones</addtitle><date>2018-05-01</date><risdate>2018</risdate><volume>23</volume><issue>3</issue><spage>399</spage><epage>410</epage><pages>399-410</pages><issn>1355-8145</issn><eissn>1466-1268</eissn><abstract>Heat-related illness and injury are becoming a growing safety concern for the farmers, construction workers, miners, firefighters, manufacturing workers, and other outdoor workforces who are exposed to heat stress in their routine lives. A primary response by a cell to an acute heat shock (HS) exposure is the induction of heat-shock proteins (HSPs), which chaperone and facilitate cellular protein folding and remodeling processes. While acute HS is well studied, the effect of repeated bouts of hyperthermia and the sustained production of HSPs in the myoblast-myotube model system of C2C12 cells are poorly characterized. In C2C12 myoblasts, we found that robust HS (43 °C, dose/time) significantly decreased the proliferation by 50% as early as on day 1 and maintained at the same level on days 2 and 3 of HS. This was accompanied by an accumulation of cells at G2 phase with reduced cell number in G1 phase indicating cell cycle arrest. FACS analysis indicates that there was no apparent change in apoptosis (markers) and cell death upon repeated HS. Immunoblot analysis and qPCR demonstrated a significant increase in the baseline expression of HSP25, 70, and 90 (among others) in cells after a single HS (43 °C) for 60 min as a typical HS response. Importantly, the repeated HS for 60 min each on days 2 and 3 maintained the elevated levels of HSPs compared to the control cells. Further, the continuous HS exposure resulted in significant inhibition of the differentiation of C2C12 myocytes to myotubes and only 1/10th of the cells underwent differentiation in HS relative to control. This was associated with significantly higher levels of HSPs and reduced expression of myogenin and Myh2 (P < 0.05), the genes involved in the differentiation process. Finally, the cell migration (scratch) assay indicated that the wound closure was significantly delayed in HS cells relative to the control cells. Overall, these results suggest that a repeated HS may perturb the active process of proliferation, motility, and differentiation processes in an in vitro murine myoblast-myotube model.</abstract><cop>Dordrecht</cop><pub>Springer</pub><pmid>29063376</pmid><doi>10.1007/s12192-017-0851-4</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Cell stress & chaperones, 2018-05, Vol.23 (3), p.399-410 |
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| subjects | Animals Apoptosis Apoptosis - genetics Biochemistry Biomedical and Life Sciences Biomedicine Boluses Cancer Research Cell adhesion & migration Cell Biology Cell cycle Cell Cycle - genetics Cell death Cell Differentiation Cell growth Cell migration Cell Movement - genetics Cell number Cell Proliferation Cells, Cultured Cellular differentiation Construction industry Differentiation Exposure Firefighters Flow cytometry G1 phase G2 phase Gene expression Heat shock Heat shock proteins Heat stress Heat tolerance Heat-Shock Proteins - genetics Heat-Shock Proteins - metabolism Heat-Shock Response Hsp25 protein Hyperthermia Immunology Messenger RNA Mice Miners Mining Muscle fibers Myoblasts Myoblasts - metabolism Myoblasts - pathology Myocytes Myogenin Myotubes Neurosciences Occupational exposure Occupational health Original Paper Protein Biosynthesis Protein folding RNA, Messenger - genetics RNA, Messenger - metabolism Transcription, Genetic Working conditions |
| title | Recurrent heat shock impairs the proliferation and differentiation of C2C12 myoblasts |
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