Concurrent psychological stress and infectious colitis is key to sustaining enhanced peripheral sensory signaling
Background The development of postinfectious‐irritable bowel syndrome is associated with psychological stress but this relationship is poorly understood. The mouse Citrobacter rodentium model enhances the postinfectious excitability of colonic nociceptors, which can be further amplified by water‐avo...
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Veröffentlicht in: | Neurogastroenterology and motility 2015-03, Vol.27 (3), p.347-355 |
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description | Background
The development of postinfectious‐irritable bowel syndrome is associated with psychological stress but this relationship is poorly understood. The mouse Citrobacter rodentium model enhances the postinfectious excitability of colonic nociceptors, which can be further amplified by water‐avoidance stress (WAS). This study tested whether concurrent infectious colitis and chronic stress enhance and sustain nociceptor excitability more than stress after resolution of infection.
Methods
Male C57 mice were gavaged with C. rodentium. WAS (1 h/day) was performed at different time‐points relative to the infection. After the final session of WAS, T9–T13 colonic‐projecting DRG neurons were isolated, cultured overnight and patch‐clamped to assess excitability. To investigate potential mechanisms, histological damage scores and colonic cytokine production were assessed.
Key Results
WAS more than 30 days after C. rodentium infection produced no greater DRG excitability than WAS in uninfected mice. However, when overlapped with chronic stress (3 sessions of WAS; 7 days before, 9 days during and 9 days after C. rodentium or sham gavage), C. rodentium significantly enhanced DRG excitability vs saline‐gavaged chronically stressed mice. Bodyweights and colonic damage scores were unchanged. Both WAS and C. rodentium gavage were found to significantly alter colonic cytokines at postinfection day 30.
Conclusions & Inferences
Chronic stress and infectious colitis combine in an additive manner to heighten and prolong the sensitivity of visceral nociceptors. The effect relies on temporal coincidence of stress and infection, does not involve substantial exacerbation of inflammation, and may involve combined direct stress hormone and immune signaling on DRG neurons.
View the podcast on this paper at the following sites:
Youtube: https://www.youtube.com/watch?v=v-svSBQYCMs
iTunes: https://itunes.apple.com/gb/podcast/neurogastroenterology-motility/id965772477
Chronic stress and infectious colitis combine in an additive manner to heighten and prolong the sensitivity of visceral nociceptors. The effect relies on temporal coincidence of stress and infection, does not involve substantial exacerbation of inflammation, and may involve combined direct stress hormone and immune signaling on DRG neurons. |
doi_str_mv | 10.1111/nmo.12497 |
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fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_1658423815</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1658423815</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4237-38157115dccf08b53a592992f4a67b1fe355db2e08489f1c06373de9f61383263</originalsourceid><addsrcrecordid>eNp1kU1P4zAQhi0EWrplD_wBZInL7iHgj9hJjqhiPyQ-LnCOXGfSGlI79SRa5d-vS8sekLBGsg-PnhnPS8g5Z1c8nWu_CVdc5FVxRGZcapWJqhTHu7diGa-EOiVfEV8YY1rk-gs5FUoJrpmake0ieDvGCH6gPU52HbqwctZ0FIcIiNT4hjrfgh1cGJHa0LnBIU31ChMdAsURB-O88ysKfm28hYb2EF2_hrjTgMcQJ4pu5U2XqDNy0poO4dvhnpPnn7dPi9_Z3eOvP4ubu8zmQhaZLLkqOFeNtS0rl0oaVYmqEm1udLHkLUilmqUAVuZl1XLLtCxkA1WruSyl0HJOvu-9fQzbEXCoNw4tdJ3xkH5Sc63K1Cm1SejlB_QljDGN-0ZpxXIl8kT92FM2BsQIbd1HtzFxqjmrdznUKYf6LYfEXhyM43IDzX_yffEJuN4Df10H0-em-uH-ca_8B1HQkrY</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1656504524</pqid></control><display><type>article</type><title>Concurrent psychological stress and infectious colitis is key to sustaining enhanced peripheral sensory signaling</title><source>MEDLINE</source><source>Access via Wiley Online Library</source><source>Wiley Online Library (Open Access Collection)</source><creator>Spreadbury, I. ; Ochoa‐Cortes, F. ; Ibeakanma, C. ; Martin, N. ; Hurlbut, D. ; Vanner, S. J.</creator><creatorcontrib>Spreadbury, I. ; Ochoa‐Cortes, F. ; Ibeakanma, C. ; Martin, N. ; Hurlbut, D. ; Vanner, S. J.</creatorcontrib><description>Background
The development of postinfectious‐irritable bowel syndrome is associated with psychological stress but this relationship is poorly understood. The mouse Citrobacter rodentium model enhances the postinfectious excitability of colonic nociceptors, which can be further amplified by water‐avoidance stress (WAS). This study tested whether concurrent infectious colitis and chronic stress enhance and sustain nociceptor excitability more than stress after resolution of infection.
Methods
Male C57 mice were gavaged with C. rodentium. WAS (1 h/day) was performed at different time‐points relative to the infection. After the final session of WAS, T9–T13 colonic‐projecting DRG neurons were isolated, cultured overnight and patch‐clamped to assess excitability. To investigate potential mechanisms, histological damage scores and colonic cytokine production were assessed.
Key Results
WAS more than 30 days after C. rodentium infection produced no greater DRG excitability than WAS in uninfected mice. However, when overlapped with chronic stress (3 sessions of WAS; 7 days before, 9 days during and 9 days after C. rodentium or sham gavage), C. rodentium significantly enhanced DRG excitability vs saline‐gavaged chronically stressed mice. Bodyweights and colonic damage scores were unchanged. Both WAS and C. rodentium gavage were found to significantly alter colonic cytokines at postinfection day 30.
Conclusions & Inferences
Chronic stress and infectious colitis combine in an additive manner to heighten and prolong the sensitivity of visceral nociceptors. The effect relies on temporal coincidence of stress and infection, does not involve substantial exacerbation of inflammation, and may involve combined direct stress hormone and immune signaling on DRG neurons.
View the podcast on this paper at the following sites:
Youtube: https://www.youtube.com/watch?v=v-svSBQYCMs
iTunes: https://itunes.apple.com/gb/podcast/neurogastroenterology-motility/id965772477
Chronic stress and infectious colitis combine in an additive manner to heighten and prolong the sensitivity of visceral nociceptors. The effect relies on temporal coincidence of stress and infection, does not involve substantial exacerbation of inflammation, and may involve combined direct stress hormone and immune signaling on DRG neurons.</description><identifier>ISSN: 1350-1925</identifier><identifier>EISSN: 1365-2982</identifier><identifier>DOI: 10.1111/nmo.12497</identifier><identifier>PMID: 25521605</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Animals ; Cells, Cultured ; Citrobacter rodentium ; Colitis - complications ; Colitis - metabolism ; Colitis - physiopathology ; Cytokines - analysis ; dorsal root ganglia ; Enterobacteriaceae Infections - complications ; Enterobacteriaceae Infections - physiopathology ; Ganglia, Spinal - physiopathology ; IBS ; Male ; Mice ; Mice, Inbred C57BL ; Neurons - physiology ; nociceptor ; psychological stress ; Stress, Psychological - complications ; Stress, Psychological - physiopathology ; water‐avoidance stress</subject><ispartof>Neurogastroenterology and motility, 2015-03, Vol.27 (3), p.347-355</ispartof><rights>2014 John Wiley & Sons Ltd</rights><rights>2014 John Wiley & Sons Ltd.</rights><rights>Copyright © 2015 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4237-38157115dccf08b53a592992f4a67b1fe355db2e08489f1c06373de9f61383263</citedby><cites>FETCH-LOGICAL-c4237-38157115dccf08b53a592992f4a67b1fe355db2e08489f1c06373de9f61383263</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fnmo.12497$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnmo.12497$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25521605$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Spreadbury, I.</creatorcontrib><creatorcontrib>Ochoa‐Cortes, F.</creatorcontrib><creatorcontrib>Ibeakanma, C.</creatorcontrib><creatorcontrib>Martin, N.</creatorcontrib><creatorcontrib>Hurlbut, D.</creatorcontrib><creatorcontrib>Vanner, S. J.</creatorcontrib><title>Concurrent psychological stress and infectious colitis is key to sustaining enhanced peripheral sensory signaling</title><title>Neurogastroenterology and motility</title><addtitle>Neurogastroenterol Motil</addtitle><description>Background
The development of postinfectious‐irritable bowel syndrome is associated with psychological stress but this relationship is poorly understood. The mouse Citrobacter rodentium model enhances the postinfectious excitability of colonic nociceptors, which can be further amplified by water‐avoidance stress (WAS). This study tested whether concurrent infectious colitis and chronic stress enhance and sustain nociceptor excitability more than stress after resolution of infection.
Methods
Male C57 mice were gavaged with C. rodentium. WAS (1 h/day) was performed at different time‐points relative to the infection. After the final session of WAS, T9–T13 colonic‐projecting DRG neurons were isolated, cultured overnight and patch‐clamped to assess excitability. To investigate potential mechanisms, histological damage scores and colonic cytokine production were assessed.
Key Results
WAS more than 30 days after C. rodentium infection produced no greater DRG excitability than WAS in uninfected mice. However, when overlapped with chronic stress (3 sessions of WAS; 7 days before, 9 days during and 9 days after C. rodentium or sham gavage), C. rodentium significantly enhanced DRG excitability vs saline‐gavaged chronically stressed mice. Bodyweights and colonic damage scores were unchanged. Both WAS and C. rodentium gavage were found to significantly alter colonic cytokines at postinfection day 30.
Conclusions & Inferences
Chronic stress and infectious colitis combine in an additive manner to heighten and prolong the sensitivity of visceral nociceptors. The effect relies on temporal coincidence of stress and infection, does not involve substantial exacerbation of inflammation, and may involve combined direct stress hormone and immune signaling on DRG neurons.
View the podcast on this paper at the following sites:
Youtube: https://www.youtube.com/watch?v=v-svSBQYCMs
iTunes: https://itunes.apple.com/gb/podcast/neurogastroenterology-motility/id965772477
Chronic stress and infectious colitis combine in an additive manner to heighten and prolong the sensitivity of visceral nociceptors. The effect relies on temporal coincidence of stress and infection, does not involve substantial exacerbation of inflammation, and may involve combined direct stress hormone and immune signaling on DRG neurons.</description><subject>Animals</subject><subject>Cells, Cultured</subject><subject>Citrobacter rodentium</subject><subject>Colitis - complications</subject><subject>Colitis - metabolism</subject><subject>Colitis - physiopathology</subject><subject>Cytokines - analysis</subject><subject>dorsal root ganglia</subject><subject>Enterobacteriaceae Infections - complications</subject><subject>Enterobacteriaceae Infections - physiopathology</subject><subject>Ganglia, Spinal - physiopathology</subject><subject>IBS</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Neurons - physiology</subject><subject>nociceptor</subject><subject>psychological stress</subject><subject>Stress, Psychological - complications</subject><subject>Stress, Psychological - physiopathology</subject><subject>water‐avoidance stress</subject><issn>1350-1925</issn><issn>1365-2982</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kU1P4zAQhi0EWrplD_wBZInL7iHgj9hJjqhiPyQ-LnCOXGfSGlI79SRa5d-vS8sekLBGsg-PnhnPS8g5Z1c8nWu_CVdc5FVxRGZcapWJqhTHu7diGa-EOiVfEV8YY1rk-gs5FUoJrpmake0ieDvGCH6gPU52HbqwctZ0FIcIiNT4hjrfgh1cGJHa0LnBIU31ChMdAsURB-O88ysKfm28hYb2EF2_hrjTgMcQJ4pu5U2XqDNy0poO4dvhnpPnn7dPi9_Z3eOvP4ubu8zmQhaZLLkqOFeNtS0rl0oaVYmqEm1udLHkLUilmqUAVuZl1XLLtCxkA1WruSyl0HJOvu-9fQzbEXCoNw4tdJ3xkH5Sc63K1Cm1SejlB_QljDGN-0ZpxXIl8kT92FM2BsQIbd1HtzFxqjmrdznUKYf6LYfEXhyM43IDzX_yffEJuN4Df10H0-em-uH-ca_8B1HQkrY</recordid><startdate>201503</startdate><enddate>201503</enddate><creator>Spreadbury, I.</creator><creator>Ochoa‐Cortes, F.</creator><creator>Ibeakanma, C.</creator><creator>Martin, N.</creator><creator>Hurlbut, D.</creator><creator>Vanner, S. J.</creator><general>Wiley Subscription Services, Inc</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>7TK</scope><scope>K9.</scope><scope>7X8</scope></search><sort><creationdate>201503</creationdate><title>Concurrent psychological stress and infectious colitis is key to sustaining enhanced peripheral sensory signaling</title><author>Spreadbury, I. ; Ochoa‐Cortes, F. ; Ibeakanma, C. ; Martin, N. ; Hurlbut, D. ; Vanner, S. J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4237-38157115dccf08b53a592992f4a67b1fe355db2e08489f1c06373de9f61383263</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Cells, Cultured</topic><topic>Citrobacter rodentium</topic><topic>Colitis - complications</topic><topic>Colitis - metabolism</topic><topic>Colitis - physiopathology</topic><topic>Cytokines - analysis</topic><topic>dorsal root ganglia</topic><topic>Enterobacteriaceae Infections - complications</topic><topic>Enterobacteriaceae Infections - physiopathology</topic><topic>Ganglia, Spinal - physiopathology</topic><topic>IBS</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Neurons - physiology</topic><topic>nociceptor</topic><topic>psychological stress</topic><topic>Stress, Psychological - complications</topic><topic>Stress, Psychological - physiopathology</topic><topic>water‐avoidance stress</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Spreadbury, I.</creatorcontrib><creatorcontrib>Ochoa‐Cortes, F.</creatorcontrib><creatorcontrib>Ibeakanma, C.</creatorcontrib><creatorcontrib>Martin, N.</creatorcontrib><creatorcontrib>Hurlbut, D.</creatorcontrib><creatorcontrib>Vanner, S. J.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Neurogastroenterology and motility</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Spreadbury, I.</au><au>Ochoa‐Cortes, F.</au><au>Ibeakanma, C.</au><au>Martin, N.</au><au>Hurlbut, D.</au><au>Vanner, S. J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Concurrent psychological stress and infectious colitis is key to sustaining enhanced peripheral sensory signaling</atitle><jtitle>Neurogastroenterology and motility</jtitle><addtitle>Neurogastroenterol Motil</addtitle><date>2015-03</date><risdate>2015</risdate><volume>27</volume><issue>3</issue><spage>347</spage><epage>355</epage><pages>347-355</pages><issn>1350-1925</issn><eissn>1365-2982</eissn><abstract>Background
The development of postinfectious‐irritable bowel syndrome is associated with psychological stress but this relationship is poorly understood. The mouse Citrobacter rodentium model enhances the postinfectious excitability of colonic nociceptors, which can be further amplified by water‐avoidance stress (WAS). This study tested whether concurrent infectious colitis and chronic stress enhance and sustain nociceptor excitability more than stress after resolution of infection.
Methods
Male C57 mice were gavaged with C. rodentium. WAS (1 h/day) was performed at different time‐points relative to the infection. After the final session of WAS, T9–T13 colonic‐projecting DRG neurons were isolated, cultured overnight and patch‐clamped to assess excitability. To investigate potential mechanisms, histological damage scores and colonic cytokine production were assessed.
Key Results
WAS more than 30 days after C. rodentium infection produced no greater DRG excitability than WAS in uninfected mice. However, when overlapped with chronic stress (3 sessions of WAS; 7 days before, 9 days during and 9 days after C. rodentium or sham gavage), C. rodentium significantly enhanced DRG excitability vs saline‐gavaged chronically stressed mice. Bodyweights and colonic damage scores were unchanged. Both WAS and C. rodentium gavage were found to significantly alter colonic cytokines at postinfection day 30.
Conclusions & Inferences
Chronic stress and infectious colitis combine in an additive manner to heighten and prolong the sensitivity of visceral nociceptors. The effect relies on temporal coincidence of stress and infection, does not involve substantial exacerbation of inflammation, and may involve combined direct stress hormone and immune signaling on DRG neurons.
View the podcast on this paper at the following sites:
Youtube: https://www.youtube.com/watch?v=v-svSBQYCMs
iTunes: https://itunes.apple.com/gb/podcast/neurogastroenterology-motility/id965772477
Chronic stress and infectious colitis combine in an additive manner to heighten and prolong the sensitivity of visceral nociceptors. The effect relies on temporal coincidence of stress and infection, does not involve substantial exacerbation of inflammation, and may involve combined direct stress hormone and immune signaling on DRG neurons.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>25521605</pmid><doi>10.1111/nmo.12497</doi><tpages>9</tpages></addata></record> |
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subjects | Animals Cells, Cultured Citrobacter rodentium Colitis - complications Colitis - metabolism Colitis - physiopathology Cytokines - analysis dorsal root ganglia Enterobacteriaceae Infections - complications Enterobacteriaceae Infections - physiopathology Ganglia, Spinal - physiopathology IBS Male Mice Mice, Inbred C57BL Neurons - physiology nociceptor psychological stress Stress, Psychological - complications Stress, Psychological - physiopathology water‐avoidance stress |
title | Concurrent psychological stress and infectious colitis is key to sustaining enhanced peripheral sensory signaling |
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