Submucosal enteric neurons of the cavine distal colon are sensitive to hypoosmolar stimuli
Key points Neurons of the enteric submucous plexus are challenged by osmolar fluctuations during digestion and absorption of nutrients. Central neurons are very sensitive to changes in osmolality but knowledge on that issue related to enteric neurons is sparse. The present study focuses on investiga...
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| Veröffentlicht in: | The Journal of physiology 2020-12, Vol.598 (23), p.5317-5332 |
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| creator | Kollmann, Patrick Elfers, Kristin Maurer, Stefanie Klingenspor, Martin Schemann, Michael Mazzuoli‐Weber, Gemma |
| description | Key points
Neurons of the enteric submucous plexus are challenged by osmolar fluctuations during digestion and absorption of nutrients.
Central neurons are very sensitive to changes in osmolality but knowledge on that issue related to enteric neurons is sparse.
The present study focuses on investigation of osmosensitivity of submucosal neurons including potential molecular mediating mechanisms.
Results show that submucosal neurons respond to hypoosmolar stimuli with increased activity which is partially mediated by the transient receptor potential vanilloid 4 channel.
We provided important information on osmosensitive properties of enteric neurons. These data are fundamental to better explain the nerve‐mediated control of the gastrointestinal functions during physiological and pathophysiological (diarrhoea) conditions.
Enteric neurons are located inside the gut wall, where they are confronted with changes in osmolality during (inter‐) digestive periods. In particular, neurons of the submucous plexus (SMP), located between epithelial cells and blood vessels may sense and respond to osmotic shifts. The present study was conducted to investigate osmosensitivity of enteric submucosal neurons and the potential role of the transient receptor potential vanilloid 4 channel (TRPV4) as a mediator of enteric neuronal osmosensitivity. Therefore, freshly dissected submucosal preparations from guinea pig colon were investigated for osmosensitivity using voltage‐sensitive dye and Ca2+ imaging. Acute hypoosmolar stimuli (final osmolality reached at ganglia of 94, 144 and 194 mOsm kg‐1) were applied to single ganglia using a local perfusion system. Expression of TRPV4 in the SMP was quantified using qRT‐PCR, and GSK1016790A and HC‐067047 were used to activate or block the receptor, respectively, revealing its relevance in enteric osmosensitivity. On average, 11.0 [7.0/17.0] % of submucosal neurons per ganglion responded to the hypoosmolar stimulus. The Ca2+ imaging experiments showed that glia responded to the hypoosmolar stimulus, but with a delay in comparison with neurons. mRNA expression of TRPV4 could be shown in the SMP and blockade of the receptor by HC‐067047 significantly decreased the number of responding neurons (0.0 [0.0/6.3] %) while the TRPV4 agonist GSK1016790A caused action potential discharge in a subpopulation of osmosensitive enteric neurons. The results of the present study provide insight into the osmosensitivity of submucosal enteric neurons and stron |
| doi_str_mv | 10.1113/JP280309 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7722197</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2465562430</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4392-9e96d5abfdadf81b7084deb852d05f8514ab7aa10d420b792b2c918d20ff02a13</originalsourceid><addsrcrecordid>eNp1kUuLFDEUhYMoTjsK_gIJuHFT401SValsBBnGxzDggOPGTUglt-wMqaRNqlr63xuZhw9wlcX9-Dgnh5DnDE4YY-L1-SUfQIB6QDas7VUjpRIPyQaA80bIjh2RJ6VcA7DKqMfkSPBhACX7Dfn6eR3n1aZiAsW4YPaWRlxzioWmiS5bpNbsfUTqfFkqZFNIkZqMtGAsfvF7pEui28MupTKnYDIti5_X4J-SR5MJBZ_dvsfky7uzq9MPzcWn9x9P3140thWKNwpV7zozTs64aWCjhKF1OA4dd9BNQ8daM0pjGLiWwygVH7lVbHAcpgm4YeKYvLnx7moVdLbWyCboXfazyQedjNd_X6Lf6m9pr6XknClZBa9uBTl9X7EsevbFYggmYlqL5jVn_ayeQ0Vf_oNepzXHWq9Sfdf1lYXfQptTKRmn-zAM9K_B9N1gFX3xZ_h78G6hCpzcAD98wMN_Rfrq_JK1oufiJ7XFn8o</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2465562430</pqid></control><display><type>article</type><title>Submucosal enteric neurons of the cavine distal colon are sensitive to hypoosmolar stimuli</title><source>Wiley Free Content</source><source>MEDLINE</source><source>Wiley Online Library Journals Frontfile Complete</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>PubMed Central</source><creator>Kollmann, Patrick ; Elfers, Kristin ; Maurer, Stefanie ; Klingenspor, Martin ; Schemann, Michael ; Mazzuoli‐Weber, Gemma</creator><creatorcontrib>Kollmann, Patrick ; Elfers, Kristin ; Maurer, Stefanie ; Klingenspor, Martin ; Schemann, Michael ; Mazzuoli‐Weber, Gemma</creatorcontrib><description>Key points
Neurons of the enteric submucous plexus are challenged by osmolar fluctuations during digestion and absorption of nutrients.
Central neurons are very sensitive to changes in osmolality but knowledge on that issue related to enteric neurons is sparse.
The present study focuses on investigation of osmosensitivity of submucosal neurons including potential molecular mediating mechanisms.
Results show that submucosal neurons respond to hypoosmolar stimuli with increased activity which is partially mediated by the transient receptor potential vanilloid 4 channel.
We provided important information on osmosensitive properties of enteric neurons. These data are fundamental to better explain the nerve‐mediated control of the gastrointestinal functions during physiological and pathophysiological (diarrhoea) conditions.
Enteric neurons are located inside the gut wall, where they are confronted with changes in osmolality during (inter‐) digestive periods. In particular, neurons of the submucous plexus (SMP), located between epithelial cells and blood vessels may sense and respond to osmotic shifts. The present study was conducted to investigate osmosensitivity of enteric submucosal neurons and the potential role of the transient receptor potential vanilloid 4 channel (TRPV4) as a mediator of enteric neuronal osmosensitivity. Therefore, freshly dissected submucosal preparations from guinea pig colon were investigated for osmosensitivity using voltage‐sensitive dye and Ca2+ imaging. Acute hypoosmolar stimuli (final osmolality reached at ganglia of 94, 144 and 194 mOsm kg‐1) were applied to single ganglia using a local perfusion system. Expression of TRPV4 in the SMP was quantified using qRT‐PCR, and GSK1016790A and HC‐067047 were used to activate or block the receptor, respectively, revealing its relevance in enteric osmosensitivity. On average, 11.0 [7.0/17.0] % of submucosal neurons per ganglion responded to the hypoosmolar stimulus. The Ca2+ imaging experiments showed that glia responded to the hypoosmolar stimulus, but with a delay in comparison with neurons. mRNA expression of TRPV4 could be shown in the SMP and blockade of the receptor by HC‐067047 significantly decreased the number of responding neurons (0.0 [0.0/6.3] %) while the TRPV4 agonist GSK1016790A caused action potential discharge in a subpopulation of osmosensitive enteric neurons. The results of the present study provide insight into the osmosensitivity of submucosal enteric neurons and strongly indicate the involvement of TRPV4 as an osmotransducer.
Key points
Neurons of the enteric submucous plexus are challenged by osmolar fluctuations during digestion and absorption of nutrients.
Central neurons are very sensitive to changes in osmolality but knowledge on that issue related to enteric neurons is sparse.
The present study focuses on investigation of osmosensitivity of submucosal neurons including potential molecular mediating mechanisms.
Results show that submucosal neurons respond to hypoosmolar stimuli with increased activity which is partially mediated by the transient receptor potential vanilloid 4 channel.
We provided important information on osmosensitive properties of enteric neurons. These data are fundamental to better explain the nerve‐mediated control of the gastrointestinal functions during physiological and pathophysiological (diarrhoea) conditions.</description><identifier>ISSN: 0022-3751</identifier><identifier>EISSN: 1469-7793</identifier><identifier>DOI: 10.1113/JP280309</identifier><identifier>PMID: 32880976</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Action potential ; Animals ; Blood vessels ; Calcium channels (voltage-gated) ; Calcium imaging ; Colon ; Dyes ; Enteric nervous system ; Epithelial cells ; Gene expression ; Guinea Pigs ; Myenteric Plexus ; Neuroglia ; Neurons ; osmosensitivity ; Perfusion ; submucosal enteric neurons ; Submucosal plexus ; Submucous Plexus ; Transient receptor potential proteins ; TRPV4</subject><ispartof>The Journal of physiology, 2020-12, Vol.598 (23), p.5317-5332</ispartof><rights>2020 The Authors. published by John Wiley & Sons Ltd on behalf of The Physiological Society.</rights><rights>2020 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.</rights><rights>2020. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4392-9e96d5abfdadf81b7084deb852d05f8514ab7aa10d420b792b2c918d20ff02a13</citedby><cites>FETCH-LOGICAL-c4392-9e96d5abfdadf81b7084deb852d05f8514ab7aa10d420b792b2c918d20ff02a13</cites><orcidid>0000-0002-4502-6664 ; 0000-0001-7803-3556</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/PMC7722197/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7722197/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,1411,1427,27903,27904,45553,45554,46387,46811,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32880976$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kollmann, Patrick</creatorcontrib><creatorcontrib>Elfers, Kristin</creatorcontrib><creatorcontrib>Maurer, Stefanie</creatorcontrib><creatorcontrib>Klingenspor, Martin</creatorcontrib><creatorcontrib>Schemann, Michael</creatorcontrib><creatorcontrib>Mazzuoli‐Weber, Gemma</creatorcontrib><title>Submucosal enteric neurons of the cavine distal colon are sensitive to hypoosmolar stimuli</title><title>The Journal of physiology</title><addtitle>J Physiol</addtitle><description>Key points
Neurons of the enteric submucous plexus are challenged by osmolar fluctuations during digestion and absorption of nutrients.
Central neurons are very sensitive to changes in osmolality but knowledge on that issue related to enteric neurons is sparse.
The present study focuses on investigation of osmosensitivity of submucosal neurons including potential molecular mediating mechanisms.
Results show that submucosal neurons respond to hypoosmolar stimuli with increased activity which is partially mediated by the transient receptor potential vanilloid 4 channel.
We provided important information on osmosensitive properties of enteric neurons. These data are fundamental to better explain the nerve‐mediated control of the gastrointestinal functions during physiological and pathophysiological (diarrhoea) conditions.
Enteric neurons are located inside the gut wall, where they are confronted with changes in osmolality during (inter‐) digestive periods. In particular, neurons of the submucous plexus (SMP), located between epithelial cells and blood vessels may sense and respond to osmotic shifts. The present study was conducted to investigate osmosensitivity of enteric submucosal neurons and the potential role of the transient receptor potential vanilloid 4 channel (TRPV4) as a mediator of enteric neuronal osmosensitivity. Therefore, freshly dissected submucosal preparations from guinea pig colon were investigated for osmosensitivity using voltage‐sensitive dye and Ca2+ imaging. Acute hypoosmolar stimuli (final osmolality reached at ganglia of 94, 144 and 194 mOsm kg‐1) were applied to single ganglia using a local perfusion system. Expression of TRPV4 in the SMP was quantified using qRT‐PCR, and GSK1016790A and HC‐067047 were used to activate or block the receptor, respectively, revealing its relevance in enteric osmosensitivity. On average, 11.0 [7.0/17.0] % of submucosal neurons per ganglion responded to the hypoosmolar stimulus. The Ca2+ imaging experiments showed that glia responded to the hypoosmolar stimulus, but with a delay in comparison with neurons. mRNA expression of TRPV4 could be shown in the SMP and blockade of the receptor by HC‐067047 significantly decreased the number of responding neurons (0.0 [0.0/6.3] %) while the TRPV4 agonist GSK1016790A caused action potential discharge in a subpopulation of osmosensitive enteric neurons. The results of the present study provide insight into the osmosensitivity of submucosal enteric neurons and strongly indicate the involvement of TRPV4 as an osmotransducer.
Key points
Neurons of the enteric submucous plexus are challenged by osmolar fluctuations during digestion and absorption of nutrients.
Central neurons are very sensitive to changes in osmolality but knowledge on that issue related to enteric neurons is sparse.
The present study focuses on investigation of osmosensitivity of submucosal neurons including potential molecular mediating mechanisms.
Results show that submucosal neurons respond to hypoosmolar stimuli with increased activity which is partially mediated by the transient receptor potential vanilloid 4 channel.
We provided important information on osmosensitive properties of enteric neurons. These data are fundamental to better explain the nerve‐mediated control of the gastrointestinal functions during physiological and pathophysiological (diarrhoea) conditions.</description><subject>Action potential</subject><subject>Animals</subject><subject>Blood vessels</subject><subject>Calcium channels (voltage-gated)</subject><subject>Calcium imaging</subject><subject>Colon</subject><subject>Dyes</subject><subject>Enteric nervous system</subject><subject>Epithelial cells</subject><subject>Gene expression</subject><subject>Guinea Pigs</subject><subject>Myenteric Plexus</subject><subject>Neuroglia</subject><subject>Neurons</subject><subject>osmosensitivity</subject><subject>Perfusion</subject><subject>submucosal enteric neurons</subject><subject>Submucosal plexus</subject><subject>Submucous Plexus</subject><subject>Transient receptor potential proteins</subject><subject>TRPV4</subject><issn>0022-3751</issn><issn>1469-7793</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kUuLFDEUhYMoTjsK_gIJuHFT401SValsBBnGxzDggOPGTUglt-wMqaRNqlr63xuZhw9wlcX9-Dgnh5DnDE4YY-L1-SUfQIB6QDas7VUjpRIPyQaA80bIjh2RJ6VcA7DKqMfkSPBhACX7Dfn6eR3n1aZiAsW4YPaWRlxzioWmiS5bpNbsfUTqfFkqZFNIkZqMtGAsfvF7pEui28MupTKnYDIti5_X4J-SR5MJBZ_dvsfky7uzq9MPzcWn9x9P3140thWKNwpV7zozTs64aWCjhKF1OA4dd9BNQ8daM0pjGLiWwygVH7lVbHAcpgm4YeKYvLnx7moVdLbWyCboXfazyQedjNd_X6Lf6m9pr6XknClZBa9uBTl9X7EsevbFYggmYlqL5jVn_ayeQ0Vf_oNepzXHWq9Sfdf1lYXfQptTKRmn-zAM9K_B9N1gFX3xZ_h78G6hCpzcAD98wMN_Rfrq_JK1oufiJ7XFn8o</recordid><startdate>20201201</startdate><enddate>20201201</enddate><creator>Kollmann, Patrick</creator><creator>Elfers, Kristin</creator><creator>Maurer, Stefanie</creator><creator>Klingenspor, Martin</creator><creator>Schemann, Michael</creator><creator>Mazzuoli‐Weber, Gemma</creator><general>Wiley Subscription Services, Inc</general><scope>24P</scope><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>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TS</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4502-6664</orcidid><orcidid>https://orcid.org/0000-0001-7803-3556</orcidid></search><sort><creationdate>20201201</creationdate><title>Submucosal enteric neurons of the cavine distal colon are sensitive to hypoosmolar stimuli</title><author>Kollmann, Patrick ; Elfers, Kristin ; Maurer, Stefanie ; Klingenspor, Martin ; Schemann, Michael ; Mazzuoli‐Weber, Gemma</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4392-9e96d5abfdadf81b7084deb852d05f8514ab7aa10d420b792b2c918d20ff02a13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Action potential</topic><topic>Animals</topic><topic>Blood vessels</topic><topic>Calcium channels (voltage-gated)</topic><topic>Calcium imaging</topic><topic>Colon</topic><topic>Dyes</topic><topic>Enteric nervous system</topic><topic>Epithelial cells</topic><topic>Gene expression</topic><topic>Guinea Pigs</topic><topic>Myenteric Plexus</topic><topic>Neuroglia</topic><topic>Neurons</topic><topic>osmosensitivity</topic><topic>Perfusion</topic><topic>submucosal enteric neurons</topic><topic>Submucosal plexus</topic><topic>Submucous Plexus</topic><topic>Transient receptor potential proteins</topic><topic>TRPV4</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kollmann, Patrick</creatorcontrib><creatorcontrib>Elfers, Kristin</creatorcontrib><creatorcontrib>Maurer, Stefanie</creatorcontrib><creatorcontrib>Klingenspor, Martin</creatorcontrib><creatorcontrib>Schemann, Michael</creatorcontrib><creatorcontrib>Mazzuoli‐Weber, Gemma</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Physical Education Index</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 Journal of physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kollmann, Patrick</au><au>Elfers, Kristin</au><au>Maurer, Stefanie</au><au>Klingenspor, Martin</au><au>Schemann, Michael</au><au>Mazzuoli‐Weber, Gemma</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Submucosal enteric neurons of the cavine distal colon are sensitive to hypoosmolar stimuli</atitle><jtitle>The Journal of physiology</jtitle><addtitle>J Physiol</addtitle><date>2020-12-01</date><risdate>2020</risdate><volume>598</volume><issue>23</issue><spage>5317</spage><epage>5332</epage><pages>5317-5332</pages><issn>0022-3751</issn><eissn>1469-7793</eissn><abstract>Key points
Neurons of the enteric submucous plexus are challenged by osmolar fluctuations during digestion and absorption of nutrients.
Central neurons are very sensitive to changes in osmolality but knowledge on that issue related to enteric neurons is sparse.
The present study focuses on investigation of osmosensitivity of submucosal neurons including potential molecular mediating mechanisms.
Results show that submucosal neurons respond to hypoosmolar stimuli with increased activity which is partially mediated by the transient receptor potential vanilloid 4 channel.
We provided important information on osmosensitive properties of enteric neurons. These data are fundamental to better explain the nerve‐mediated control of the gastrointestinal functions during physiological and pathophysiological (diarrhoea) conditions.
Enteric neurons are located inside the gut wall, where they are confronted with changes in osmolality during (inter‐) digestive periods. In particular, neurons of the submucous plexus (SMP), located between epithelial cells and blood vessels may sense and respond to osmotic shifts. The present study was conducted to investigate osmosensitivity of enteric submucosal neurons and the potential role of the transient receptor potential vanilloid 4 channel (TRPV4) as a mediator of enteric neuronal osmosensitivity. Therefore, freshly dissected submucosal preparations from guinea pig colon were investigated for osmosensitivity using voltage‐sensitive dye and Ca2+ imaging. Acute hypoosmolar stimuli (final osmolality reached at ganglia of 94, 144 and 194 mOsm kg‐1) were applied to single ganglia using a local perfusion system. Expression of TRPV4 in the SMP was quantified using qRT‐PCR, and GSK1016790A and HC‐067047 were used to activate or block the receptor, respectively, revealing its relevance in enteric osmosensitivity. On average, 11.0 [7.0/17.0] % of submucosal neurons per ganglion responded to the hypoosmolar stimulus. The Ca2+ imaging experiments showed that glia responded to the hypoosmolar stimulus, but with a delay in comparison with neurons. mRNA expression of TRPV4 could be shown in the SMP and blockade of the receptor by HC‐067047 significantly decreased the number of responding neurons (0.0 [0.0/6.3] %) while the TRPV4 agonist GSK1016790A caused action potential discharge in a subpopulation of osmosensitive enteric neurons. The results of the present study provide insight into the osmosensitivity of submucosal enteric neurons and strongly indicate the involvement of TRPV4 as an osmotransducer.
Key points
Neurons of the enteric submucous plexus are challenged by osmolar fluctuations during digestion and absorption of nutrients.
Central neurons are very sensitive to changes in osmolality but knowledge on that issue related to enteric neurons is sparse.
The present study focuses on investigation of osmosensitivity of submucosal neurons including potential molecular mediating mechanisms.
Results show that submucosal neurons respond to hypoosmolar stimuli with increased activity which is partially mediated by the transient receptor potential vanilloid 4 channel.
We provided important information on osmosensitive properties of enteric neurons. These data are fundamental to better explain the nerve‐mediated control of the gastrointestinal functions during physiological and pathophysiological (diarrhoea) conditions.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>32880976</pmid><doi>10.1113/JP280309</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-4502-6664</orcidid><orcidid>https://orcid.org/0000-0001-7803-3556</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Action potential Animals Blood vessels Calcium channels (voltage-gated) Calcium imaging Colon Dyes Enteric nervous system Epithelial cells Gene expression Guinea Pigs Myenteric Plexus Neuroglia Neurons osmosensitivity Perfusion submucosal enteric neurons Submucosal plexus Submucous Plexus Transient receptor potential proteins TRPV4 |
| title | Submucosal enteric neurons of the cavine distal colon are sensitive to hypoosmolar stimuli |
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