Interstitial Cells of Cajal Mediate Inhibitory Neurotransmission in the Stomach
The structural relationships between interstitial cells of Cajal (ICC), varicose nerve fibers, and smooth muscle cells in the gastrointestinal tract have led to the suggestion that ICC may be involved in or mediate enteric neurotransmission. We characterized the distribution of ICC in the murine sto...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 1996-10, Vol.93 (21), p.12008-12013 |
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| container_title | Proceedings of the National Academy of Sciences - PNAS |
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| creator | Burns, Alan J. Alan E. J. Lomax Torihashi, Shigeko Sanders, Kenton M. Ward, Sean M. |
| description | The structural relationships between interstitial cells of Cajal (ICC), varicose nerve fibers, and smooth muscle cells in the gastrointestinal tract have led to the suggestion that ICC may be involved in or mediate enteric neurotransmission. We characterized the distribution of ICC in the murine stomach and found two distinct classes on the basis of morphology and immunoreactivity to antibodies against c-Kit receptors. ICC with multiple processes formed a network in the myenteric plexus region from corpus to pylorus. Spindle-shaped ICC were found within the circular and longitudinal muscle layers (IC-IM) throughout the stomach. The density of these cells was greatest in the proximal stomach. IC-IM ran along nerve fibers and were closely associated with nerve terminals and adjacent smooth muscle cells. IC-IM failed to develop in mice with mutations in c-kit. Therefore, we used W/W$^{V}$ mutants to test whether IC-IM mediate neural inputs in muscles of the gastric fundus. The distribution of inhibitory nerves in the stomachs of c-kit mutants was normal, but NO-dependent inhibitory neuroregulation was greatly reduced. Smooth muscle tissues of W/W$^{V}$ mutants relaxed in response to exogenous sodium nitroprusside, but the membrane potential effects of sodium nitroprusside were attenuated. These data suggest that IC-IM play a critical serial role in NO-dependent neurotransmission: the cellular mechanism(s) responsible for transducing NO into electrical responses may be expressed in IC-IM. Loss of these cells causes loss of electrical responsiveness and greatly reduces responses to nitrergic nerve stimulation. |
| doi_str_mv | 10.1073/pnas.93.21.12008 |
| format | Article |
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J. Lomax ; Torihashi, Shigeko ; Sanders, Kenton M. ; Ward, Sean M.</creator><creatorcontrib>Burns, Alan J. ; Alan E. J. Lomax ; Torihashi, Shigeko ; Sanders, Kenton M. ; Ward, Sean M.</creatorcontrib><description>The structural relationships between interstitial cells of Cajal (ICC), varicose nerve fibers, and smooth muscle cells in the gastrointestinal tract have led to the suggestion that ICC may be involved in or mediate enteric neurotransmission. We characterized the distribution of ICC in the murine stomach and found two distinct classes on the basis of morphology and immunoreactivity to antibodies against c-Kit receptors. ICC with multiple processes formed a network in the myenteric plexus region from corpus to pylorus. Spindle-shaped ICC were found within the circular and longitudinal muscle layers (IC-IM) throughout the stomach. The density of these cells was greatest in the proximal stomach. IC-IM ran along nerve fibers and were closely associated with nerve terminals and adjacent smooth muscle cells. IC-IM failed to develop in mice with mutations in c-kit. Therefore, we used W/W$^{V}$ mutants to test whether IC-IM mediate neural inputs in muscles of the gastric fundus. The distribution of inhibitory nerves in the stomachs of c-kit mutants was normal, but NO-dependent inhibitory neuroregulation was greatly reduced. Smooth muscle tissues of W/W$^{V}$ mutants relaxed in response to exogenous sodium nitroprusside, but the membrane potential effects of sodium nitroprusside were attenuated. These data suggest that IC-IM play a critical serial role in NO-dependent neurotransmission: the cellular mechanism(s) responsible for transducing NO into electrical responses may be expressed in IC-IM. Loss of these cells causes loss of electrical responsiveness and greatly reduces responses to nitrergic nerve stimulation.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.93.21.12008</identifier><identifier>PMID: 8876253</identifier><language>eng</language><publisher>United States: National Academy of Sciences of the United States of America</publisher><subject>Anatomy & physiology ; Animals ; Atropine - pharmacology ; Connective Tissue - physiology ; Connective Tissue - ultrastructure ; Connective Tissue Cells ; Dihydrolipoamide Dehydrogenase - analysis ; Female ; Gastric Fundus ; Gastrointestinal tract ; Heterozygote ; In Vitro Techniques ; Interstitial cells ; Isometric Contraction ; Male ; Membrane potential ; Membrane Potentials - drug effects ; Mice ; Mice, Inbred C57BL ; Mice, Mutant Strains ; Muscle, Smooth - drug effects ; Muscle, Smooth - innervation ; Muscle, Smooth - physiology ; Muscles ; Nerves ; Neurons ; Neurons - cytology ; Neurons - physiology ; Neurons - ultrastructure ; Neurotransmission ; NG-Nitroarginine Methyl Ester - pharmacology ; Nitroprusside - pharmacology ; Phentolamine - pharmacology ; Propranolol - pharmacology ; Pyloric Antrum ; Small intestine ; Smooth muscle myocytes ; Stem Cell Factor - analysis ; Stomach ; Stomach - drug effects ; Stomach - innervation ; Stomach - physiology ; Synaptic Transmission - drug effects ; Vasoactive Intestinal Peptide - pharmacology</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 1996-10, Vol.93 (21), p.12008-12013</ispartof><rights>Copyright 1996 National Academy of Sciences</rights><rights>Copyright National Academy of Sciences Oct 15, 1996</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c589t-ff9f27e6eace46e3bf04278cbbdab947c379d2603d5d29e2e77f6eda5bf91bff3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/93/21.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/40552$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/40552$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,724,777,781,800,882,27905,27906,53772,53774,57998,58231</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/8876253$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Burns, Alan J.</creatorcontrib><creatorcontrib>Alan E. J. Lomax</creatorcontrib><creatorcontrib>Torihashi, Shigeko</creatorcontrib><creatorcontrib>Sanders, Kenton M.</creatorcontrib><creatorcontrib>Ward, Sean M.</creatorcontrib><title>Interstitial Cells of Cajal Mediate Inhibitory Neurotransmission in the Stomach</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The structural relationships between interstitial cells of Cajal (ICC), varicose nerve fibers, and smooth muscle cells in the gastrointestinal tract have led to the suggestion that ICC may be involved in or mediate enteric neurotransmission. We characterized the distribution of ICC in the murine stomach and found two distinct classes on the basis of morphology and immunoreactivity to antibodies against c-Kit receptors. ICC with multiple processes formed a network in the myenteric plexus region from corpus to pylorus. Spindle-shaped ICC were found within the circular and longitudinal muscle layers (IC-IM) throughout the stomach. The density of these cells was greatest in the proximal stomach. IC-IM ran along nerve fibers and were closely associated with nerve terminals and adjacent smooth muscle cells. IC-IM failed to develop in mice with mutations in c-kit. Therefore, we used W/W$^{V}$ mutants to test whether IC-IM mediate neural inputs in muscles of the gastric fundus. The distribution of inhibitory nerves in the stomachs of c-kit mutants was normal, but NO-dependent inhibitory neuroregulation was greatly reduced. Smooth muscle tissues of W/W$^{V}$ mutants relaxed in response to exogenous sodium nitroprusside, but the membrane potential effects of sodium nitroprusside were attenuated. These data suggest that IC-IM play a critical serial role in NO-dependent neurotransmission: the cellular mechanism(s) responsible for transducing NO into electrical responses may be expressed in IC-IM. Loss of these cells causes loss of electrical responsiveness and greatly reduces responses to nitrergic nerve stimulation.</description><subject>Anatomy & physiology</subject><subject>Animals</subject><subject>Atropine - pharmacology</subject><subject>Connective Tissue - physiology</subject><subject>Connective Tissue - ultrastructure</subject><subject>Connective Tissue Cells</subject><subject>Dihydrolipoamide Dehydrogenase - analysis</subject><subject>Female</subject><subject>Gastric Fundus</subject><subject>Gastrointestinal tract</subject><subject>Heterozygote</subject><subject>In Vitro Techniques</subject><subject>Interstitial cells</subject><subject>Isometric Contraction</subject><subject>Male</subject><subject>Membrane potential</subject><subject>Membrane Potentials - drug effects</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Mutant Strains</subject><subject>Muscle, Smooth - drug effects</subject><subject>Muscle, Smooth - innervation</subject><subject>Muscle, Smooth - physiology</subject><subject>Muscles</subject><subject>Nerves</subject><subject>Neurons</subject><subject>Neurons - cytology</subject><subject>Neurons - physiology</subject><subject>Neurons - ultrastructure</subject><subject>Neurotransmission</subject><subject>NG-Nitroarginine Methyl Ester - pharmacology</subject><subject>Nitroprusside - pharmacology</subject><subject>Phentolamine - pharmacology</subject><subject>Propranolol - pharmacology</subject><subject>Pyloric Antrum</subject><subject>Small intestine</subject><subject>Smooth muscle myocytes</subject><subject>Stem Cell Factor - analysis</subject><subject>Stomach</subject><subject>Stomach - drug effects</subject><subject>Stomach - innervation</subject><subject>Stomach - physiology</subject><subject>Synaptic Transmission - drug effects</subject><subject>Vasoactive Intestinal Peptide - pharmacology</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1996</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc2LUzEUxYMoY2d0L4L4mIW4ac3nSwJupPhRGJ2Fug55793YlNekk-SJ89-b2lpGF7oK4fzO5Z57EHpC8IJgyV7tgs0LzRaULAjFWN1DM4I1mbdc4_tohjGVc8Upf4jOc95gjLVQ-AydKSVbKtgMXa9CgZSLL96OzRLGMTfRNUu7qd-PMHhboFmFte98iem2-QRTiiXZkLc-Zx9D40NT1tB8LnFr-_Uj9MDZMcPj43uBvr57-2X5YX51_X61fHM174XSZe6cdlRCC7YH3gLrHOZUqr7rBttpLnsm9UBbzAYxUA0UpHQtDFZ0TpPOOXaBXh_m7qZuC0MPoS41ml3yW5tuTbTe_KkEvzbf4nfDFJG82l8c7SneTJCLqXH6mt4GiFM2UnEhGGH_BYlQjHGlKnj5F7iJUwr1BoZiwghlQlcIH6A-xZwTuNPCBJt9oWZfqNHMUGJ-FVotz-4GPRmODVb95VHfO3-rdyYYN41jgR-los__jVbi6YHY5Nr2CeFYCMp-An8bv_4</recordid><startdate>19961015</startdate><enddate>19961015</enddate><creator>Burns, Alan J.</creator><creator>Alan E. J. Lomax</creator><creator>Torihashi, Shigeko</creator><creator>Sanders, Kenton M.</creator><creator>Ward, Sean M.</creator><general>National Academy of Sciences of the United States of America</general><general>National Acad Sciences</general><general>National Academy of Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>19961015</creationdate><title>Interstitial Cells of Cajal Mediate Inhibitory Neurotransmission in the Stomach</title><author>Burns, Alan J. ; Alan E. J. Lomax ; Torihashi, Shigeko ; Sanders, Kenton M. ; Ward, Sean M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c589t-ff9f27e6eace46e3bf04278cbbdab947c379d2603d5d29e2e77f6eda5bf91bff3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1996</creationdate><topic>Anatomy & physiology</topic><topic>Animals</topic><topic>Atropine - pharmacology</topic><topic>Connective Tissue - physiology</topic><topic>Connective Tissue - ultrastructure</topic><topic>Connective Tissue Cells</topic><topic>Dihydrolipoamide Dehydrogenase - analysis</topic><topic>Female</topic><topic>Gastric Fundus</topic><topic>Gastrointestinal tract</topic><topic>Heterozygote</topic><topic>In Vitro Techniques</topic><topic>Interstitial cells</topic><topic>Isometric Contraction</topic><topic>Male</topic><topic>Membrane potential</topic><topic>Membrane Potentials - drug effects</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Mutant Strains</topic><topic>Muscle, Smooth - drug effects</topic><topic>Muscle, Smooth - innervation</topic><topic>Muscle, Smooth - physiology</topic><topic>Muscles</topic><topic>Nerves</topic><topic>Neurons</topic><topic>Neurons - cytology</topic><topic>Neurons - physiology</topic><topic>Neurons - ultrastructure</topic><topic>Neurotransmission</topic><topic>NG-Nitroarginine Methyl Ester - pharmacology</topic><topic>Nitroprusside - pharmacology</topic><topic>Phentolamine - pharmacology</topic><topic>Propranolol - pharmacology</topic><topic>Pyloric Antrum</topic><topic>Small intestine</topic><topic>Smooth muscle myocytes</topic><topic>Stem Cell Factor - analysis</topic><topic>Stomach</topic><topic>Stomach - drug effects</topic><topic>Stomach - innervation</topic><topic>Stomach - physiology</topic><topic>Synaptic Transmission - drug effects</topic><topic>Vasoactive Intestinal Peptide - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Burns, Alan J.</creatorcontrib><creatorcontrib>Alan E. 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Lomax</creatorcontrib><creatorcontrib>Torihashi, Shigeko</creatorcontrib><creatorcontrib>Sanders, Kenton M.</creatorcontrib><creatorcontrib>Ward, Sean M.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Burns, Alan J.</au><au>Alan E. J. Lomax</au><au>Torihashi, Shigeko</au><au>Sanders, Kenton M.</au><au>Ward, Sean M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Interstitial Cells of Cajal Mediate Inhibitory Neurotransmission in the Stomach</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>1996-10-15</date><risdate>1996</risdate><volume>93</volume><issue>21</issue><spage>12008</spage><epage>12013</epage><pages>12008-12013</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>The structural relationships between interstitial cells of Cajal (ICC), varicose nerve fibers, and smooth muscle cells in the gastrointestinal tract have led to the suggestion that ICC may be involved in or mediate enteric neurotransmission. We characterized the distribution of ICC in the murine stomach and found two distinct classes on the basis of morphology and immunoreactivity to antibodies against c-Kit receptors. ICC with multiple processes formed a network in the myenteric plexus region from corpus to pylorus. Spindle-shaped ICC were found within the circular and longitudinal muscle layers (IC-IM) throughout the stomach. The density of these cells was greatest in the proximal stomach. IC-IM ran along nerve fibers and were closely associated with nerve terminals and adjacent smooth muscle cells. IC-IM failed to develop in mice with mutations in c-kit. Therefore, we used W/W$^{V}$ mutants to test whether IC-IM mediate neural inputs in muscles of the gastric fundus. The distribution of inhibitory nerves in the stomachs of c-kit mutants was normal, but NO-dependent inhibitory neuroregulation was greatly reduced. Smooth muscle tissues of W/W$^{V}$ mutants relaxed in response to exogenous sodium nitroprusside, but the membrane potential effects of sodium nitroprusside were attenuated. These data suggest that IC-IM play a critical serial role in NO-dependent neurotransmission: the cellular mechanism(s) responsible for transducing NO into electrical responses may be expressed in IC-IM. Loss of these cells causes loss of electrical responsiveness and greatly reduces responses to nitrergic nerve stimulation.</abstract><cop>United States</cop><pub>National Academy of Sciences of the United States of America</pub><pmid>8876253</pmid><doi>10.1073/pnas.93.21.12008</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Anatomy & physiology Animals Atropine - pharmacology Connective Tissue - physiology Connective Tissue - ultrastructure Connective Tissue Cells Dihydrolipoamide Dehydrogenase - analysis Female Gastric Fundus Gastrointestinal tract Heterozygote In Vitro Techniques Interstitial cells Isometric Contraction Male Membrane potential Membrane Potentials - drug effects Mice Mice, Inbred C57BL Mice, Mutant Strains Muscle, Smooth - drug effects Muscle, Smooth - innervation Muscle, Smooth - physiology Muscles Nerves Neurons Neurons - cytology Neurons - physiology Neurons - ultrastructure Neurotransmission NG-Nitroarginine Methyl Ester - pharmacology Nitroprusside - pharmacology Phentolamine - pharmacology Propranolol - pharmacology Pyloric Antrum Small intestine Smooth muscle myocytes Stem Cell Factor - analysis Stomach Stomach - drug effects Stomach - innervation Stomach - physiology Synaptic Transmission - drug effects Vasoactive Intestinal Peptide - pharmacology |
| title | Interstitial Cells of Cajal Mediate Inhibitory Neurotransmission in the Stomach |
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