Recurring circadian disruption alters circadian clock sensitivity to resetting
A single phase advance of the light:dark (LD) cycle can temporarily disrupt synchrony of neural circadian rhythms within the suprachiasmatic nucleus (SCN) and between the SCN and peripheral tissues. Compounding this, modern life can involve repeated disruptive light conditions. To model chronic disr...
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creator | Leise, Tanya L. Goldberg, Ariella Michael, John Montoya, Grace Solow, Sabrina Molyneux, Penny Vetrivelan, Ramalingam Harrington, Mary E. |
description | A single phase advance of the light:dark (LD) cycle can temporarily disrupt synchrony of neural circadian rhythms within the suprachiasmatic nucleus (SCN) and between the SCN and peripheral tissues. Compounding this, modern life can involve repeated disruptive light conditions. To model chronic disruption to the circadian system, we exposed male mice to more than a month of a 20‐hr light cycle (LD10:10), which mice typically cannot entrain to. Control animals were housed under LD12:12. We measured locomotor activity and body temperature rhythms in vivo, and rhythms of PER2::LUC bioluminescence in SCN and peripheral tissues ex vivo. Unexpectedly, we discovered strong effects of the time of dissection on circadian phase of PER2::LUC bioluminescent rhythms, which varied across tissues. White adipose tissue was strongly reset by dissection, while thymus phase appeared independent of dissection timing. Prior light exposure impacted the SCN, resulting in strong resetting of SCN phase by dissection for mice housed under LD10:10, and weak phase shifts by time of dissection in SCN from control LD12:12 mice. These findings suggest that exposure to circadian disruption may desynchronize SCN neurons, increasing network sensitivity to perturbations. We propose that tissues with a weakened circadian network, such as the SCN under disruptive light conditions, or with little to no coupling, for example, some peripheral tissues, will show increased resetting effects. In particular, exposure to light at inconsistent circadian times on a recurring weekly basis disrupts circadian rhythms and alters sensitivity of the SCN neural pacemaker to dissection time.
To model chronic disruption to the circadian system, we exposed male mice to more than a month of a 20‐hr light:dark cycle (LD10:10). Controls were housed under LD12:12. We measured rhythms of PER2::LUC bioluminescence in SCN and peripheral tissues ex vivo. Unexpectedly, we discovered strong effects of the time of dissection on circadian phase. Tissues with a weakened circadian network, such as the SCN under disruptive light conditions, show increased resetting to dissection. |
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To model chronic disruption to the circadian system, we exposed male mice to more than a month of a 20‐hr light:dark cycle (LD10:10). Controls were housed under LD12:12. We measured rhythms of PER2::LUC bioluminescence in SCN and peripheral tissues ex vivo. Unexpectedly, we discovered strong effects of the time of dissection on circadian phase. Tissues with a weakened circadian network, such as the SCN under disruptive light conditions, show increased resetting to dissection.</description><identifier>ISSN: 0953-816X</identifier><identifier>EISSN: 1460-9568</identifier><identifier>DOI: 10.1111/ejn.14179</identifier><identifier>PMID: 30269396</identifier><language>eng</language><publisher>France: Wiley Subscription Services, Inc</publisher><subject>adipose ; Adipose tissue ; Bioluminescence ; Body temperature ; Circadian rhythm ; Circadian rhythms ; Dissection ; jetlag ; Light ; Locomotor activity ; mice ; PER2 ; Period 2 protein ; Suprachiasmatic nucleus ; Synchronization ; thymus</subject><ispartof>The European journal of neuroscience, 2020-06, Vol.51 (12), p.2343-2354</ispartof><rights>2018 Federation of European Neuroscience Societies and John Wiley & Sons Ltd</rights><rights>2018 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.</rights><rights>Copyright © 2020 Federation of European Neuroscience Societies and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4439-69ced99f413b75808865e5f3531f73a6b1d397e60bf9bc0093421d40efe0dbd13</citedby><cites>FETCH-LOGICAL-c4439-69ced99f413b75808865e5f3531f73a6b1d397e60bf9bc0093421d40efe0dbd13</cites><orcidid>0000-0003-2266-6455</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fejn.14179$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fejn.14179$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30269396$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Leise, Tanya L.</creatorcontrib><creatorcontrib>Goldberg, Ariella</creatorcontrib><creatorcontrib>Michael, John</creatorcontrib><creatorcontrib>Montoya, Grace</creatorcontrib><creatorcontrib>Solow, Sabrina</creatorcontrib><creatorcontrib>Molyneux, Penny</creatorcontrib><creatorcontrib>Vetrivelan, Ramalingam</creatorcontrib><creatorcontrib>Harrington, Mary E.</creatorcontrib><title>Recurring circadian disruption alters circadian clock sensitivity to resetting</title><title>The European journal of neuroscience</title><addtitle>Eur J Neurosci</addtitle><description>A single phase advance of the light:dark (LD) cycle can temporarily disrupt synchrony of neural circadian rhythms within the suprachiasmatic nucleus (SCN) and between the SCN and peripheral tissues. Compounding this, modern life can involve repeated disruptive light conditions. To model chronic disruption to the circadian system, we exposed male mice to more than a month of a 20‐hr light cycle (LD10:10), which mice typically cannot entrain to. Control animals were housed under LD12:12. We measured locomotor activity and body temperature rhythms in vivo, and rhythms of PER2::LUC bioluminescence in SCN and peripheral tissues ex vivo. Unexpectedly, we discovered strong effects of the time of dissection on circadian phase of PER2::LUC bioluminescent rhythms, which varied across tissues. White adipose tissue was strongly reset by dissection, while thymus phase appeared independent of dissection timing. Prior light exposure impacted the SCN, resulting in strong resetting of SCN phase by dissection for mice housed under LD10:10, and weak phase shifts by time of dissection in SCN from control LD12:12 mice. These findings suggest that exposure to circadian disruption may desynchronize SCN neurons, increasing network sensitivity to perturbations. We propose that tissues with a weakened circadian network, such as the SCN under disruptive light conditions, or with little to no coupling, for example, some peripheral tissues, will show increased resetting effects. In particular, exposure to light at inconsistent circadian times on a recurring weekly basis disrupts circadian rhythms and alters sensitivity of the SCN neural pacemaker to dissection time.
To model chronic disruption to the circadian system, we exposed male mice to more than a month of a 20‐hr light:dark cycle (LD10:10). Controls were housed under LD12:12. We measured rhythms of PER2::LUC bioluminescence in SCN and peripheral tissues ex vivo. Unexpectedly, we discovered strong effects of the time of dissection on circadian phase. Tissues with a weakened circadian network, such as the SCN under disruptive light conditions, show increased resetting to dissection.</description><subject>adipose</subject><subject>Adipose tissue</subject><subject>Bioluminescence</subject><subject>Body temperature</subject><subject>Circadian rhythm</subject><subject>Circadian rhythms</subject><subject>Dissection</subject><subject>jetlag</subject><subject>Light</subject><subject>Locomotor activity</subject><subject>mice</subject><subject>PER2</subject><subject>Period 2 protein</subject><subject>Suprachiasmatic nucleus</subject><subject>Synchronization</subject><subject>thymus</subject><issn>0953-816X</issn><issn>1460-9568</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNp1kU1r3DAQhkVJaTZpD_0DwZBLcvBGsj5sXQphySchhdJCb0KWx4m2XmkjyQn776PNJkta6Fx0mIdnZvQi9JXgKcl1AnM3JYzU8gOaECZwKblodtAES07Lhojfu2gvxjnGuBGMf0K7FFdCUikm6PYHmDEE6-4KY4PRndWu6GwM4zJZ7wo9JAjxXc8M3vwpIrhok320aVUkXwSIkFKWfEYfez1E-PL67qNf52c_Z5flzfeLq9npTWkYo7IU0kAnZc8IbWve4KYRHHhPOSV9TbVoSUdlDQK3vWwNxpKyinQMQw-4aztC99G3jXc5tgvoDLgU9KCWwS50WCmvrfq74-y9uvOPSrA8s1kLjl4FwT-MEJNa2GhgGLQDP0ZVEcLzHxFWZ_TwH3Tux-DyeapiWIqqoXwtPN5QJvgYA_TbZQhW65RUTkm9pJTZg_fbb8m3WDJwsgGe7ACr_5vU2fXtRvkMutedUA</recordid><startdate>202006</startdate><enddate>202006</enddate><creator>Leise, Tanya L.</creator><creator>Goldberg, Ariella</creator><creator>Michael, John</creator><creator>Montoya, Grace</creator><creator>Solow, Sabrina</creator><creator>Molyneux, Penny</creator><creator>Vetrivelan, Ramalingam</creator><creator>Harrington, Mary E.</creator><general>Wiley Subscription Services, Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-2266-6455</orcidid></search><sort><creationdate>202006</creationdate><title>Recurring circadian disruption alters circadian clock sensitivity to resetting</title><author>Leise, Tanya L. ; Goldberg, Ariella ; Michael, John ; Montoya, Grace ; Solow, Sabrina ; Molyneux, Penny ; Vetrivelan, Ramalingam ; Harrington, Mary E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4439-69ced99f413b75808865e5f3531f73a6b1d397e60bf9bc0093421d40efe0dbd13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>adipose</topic><topic>Adipose tissue</topic><topic>Bioluminescence</topic><topic>Body temperature</topic><topic>Circadian rhythm</topic><topic>Circadian rhythms</topic><topic>Dissection</topic><topic>jetlag</topic><topic>Light</topic><topic>Locomotor activity</topic><topic>mice</topic><topic>PER2</topic><topic>Period 2 protein</topic><topic>Suprachiasmatic nucleus</topic><topic>Synchronization</topic><topic>thymus</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Leise, Tanya L.</creatorcontrib><creatorcontrib>Goldberg, Ariella</creatorcontrib><creatorcontrib>Michael, John</creatorcontrib><creatorcontrib>Montoya, Grace</creatorcontrib><creatorcontrib>Solow, Sabrina</creatorcontrib><creatorcontrib>Molyneux, Penny</creatorcontrib><creatorcontrib>Vetrivelan, Ramalingam</creatorcontrib><creatorcontrib>Harrington, Mary E.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The European journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Leise, Tanya L.</au><au>Goldberg, Ariella</au><au>Michael, John</au><au>Montoya, Grace</au><au>Solow, Sabrina</au><au>Molyneux, Penny</au><au>Vetrivelan, Ramalingam</au><au>Harrington, Mary E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Recurring circadian disruption alters circadian clock sensitivity to resetting</atitle><jtitle>The European journal of neuroscience</jtitle><addtitle>Eur J Neurosci</addtitle><date>2020-06</date><risdate>2020</risdate><volume>51</volume><issue>12</issue><spage>2343</spage><epage>2354</epage><pages>2343-2354</pages><issn>0953-816X</issn><eissn>1460-9568</eissn><abstract>A single phase advance of the light:dark (LD) cycle can temporarily disrupt synchrony of neural circadian rhythms within the suprachiasmatic nucleus (SCN) and between the SCN and peripheral tissues. Compounding this, modern life can involve repeated disruptive light conditions. To model chronic disruption to the circadian system, we exposed male mice to more than a month of a 20‐hr light cycle (LD10:10), which mice typically cannot entrain to. Control animals were housed under LD12:12. We measured locomotor activity and body temperature rhythms in vivo, and rhythms of PER2::LUC bioluminescence in SCN and peripheral tissues ex vivo. Unexpectedly, we discovered strong effects of the time of dissection on circadian phase of PER2::LUC bioluminescent rhythms, which varied across tissues. White adipose tissue was strongly reset by dissection, while thymus phase appeared independent of dissection timing. Prior light exposure impacted the SCN, resulting in strong resetting of SCN phase by dissection for mice housed under LD10:10, and weak phase shifts by time of dissection in SCN from control LD12:12 mice. These findings suggest that exposure to circadian disruption may desynchronize SCN neurons, increasing network sensitivity to perturbations. We propose that tissues with a weakened circadian network, such as the SCN under disruptive light conditions, or with little to no coupling, for example, some peripheral tissues, will show increased resetting effects. In particular, exposure to light at inconsistent circadian times on a recurring weekly basis disrupts circadian rhythms and alters sensitivity of the SCN neural pacemaker to dissection time.
To model chronic disruption to the circadian system, we exposed male mice to more than a month of a 20‐hr light:dark cycle (LD10:10). Controls were housed under LD12:12. We measured rhythms of PER2::LUC bioluminescence in SCN and peripheral tissues ex vivo. Unexpectedly, we discovered strong effects of the time of dissection on circadian phase. Tissues with a weakened circadian network, such as the SCN under disruptive light conditions, show increased resetting to dissection.</abstract><cop>France</cop><pub>Wiley Subscription Services, Inc</pub><pmid>30269396</pmid><doi>10.1111/ejn.14179</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-2266-6455</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | adipose Adipose tissue Bioluminescence Body temperature Circadian rhythm Circadian rhythms Dissection jetlag Light Locomotor activity mice PER2 Period 2 protein Suprachiasmatic nucleus Synchronization thymus |
title | Recurring circadian disruption alters circadian clock sensitivity to resetting |
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