Spontaneous transient hyperpolarizations in the rabbit small intestine
Key points Recently, it was shown that fibroblast‐like cells (FLCs) possess the apparatus to mediate purinergic motor neurotransmission in the gastrointestinal tract. However, the electrophysiological properties of FLCs in situ have not been determined. We recorded two patterns of slow waves from lo...
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| Veröffentlicht in: | The Journal of physiology 2014-11, Vol.592 (21), p.4733-4745 |
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| creator | Kito, Yoshihiko Kurahashi, Masaaki Mitsui, Retsu Ward, Sean M. Sanders, Kenton M. |
| description | Key points
Recently, it was shown that fibroblast‐like cells (FLCs) possess the apparatus to mediate purinergic motor neurotransmission in the gastrointestinal tract. However, the electrophysiological properties of FLCs in situ have not been determined.
We recorded two patterns of slow waves from longitudinal smooth muscle cells and circular smooth muscle cells, large amplitude slow waves from interstitial cells of Cajal, and spontaneous transient hyperpolarizations (STHs) from FLCs in the rabbit small intestine using intracellular recording combined with dye injection to identify the cellular morphology of impaled cells.
Drugs that inhibit the signalling pathway involved in purinergic neurotransmission inhibited STHs in FLCs. Small amplitude STHs were recorded in smooth muscle cells but not in interstitial cells of Cajal, suggesting that STHs from FLCs were conducted passively to smooth muscle cells.
We conclude that FLCs display the molecular apparatus necessary to mediate purinergic neurotransmission and may tonically dampen smooth muscle excitability in the rabbit small intestine by an ongoing discharge of STHs.
Four types of electrical activity were recorded and related to cell structure by intracellular recording and dye injection into impaled cells in muscles of rabbit small intestine. The specific cell types from which recordings were made were longitudinal smooth muscle cells (LSMCs), circular smooth muscle cells (CSMCs), interstitial cells of Cajal distributed in the myenteric region (ICC‐MY) and fibroblast‐like cells (FLCs). Slow waves (slow wavesSMC) were recorded from LSMCs and CSMCs. Slow waves (slow wavesICC) were of greatest amplitude (>50 mV) and highest maximum rate of rise (>10 V s−1) in ICC‐MY. The dominant activity in FLCs was spontaneous transient hyperpolarizations (STHs), with maximum amplitudes above 30 mV. STHs were often superimposed upon small amplitude slow waves (slow wavesFLC). STHs displayed a cyclical pattern of discharge irrespective of background slow wave activity. STHs were inhibited by MRS2500 (3 μm), a P2Y1 antagonist, and abolished by apamin (0.3 μm), a blocker of small conductance Ca2+‐activated K+ channels. Small amplitude STHs ( |
| doi_str_mv | 10.1113/jphysiol.2014.276337 |
| format | Article |
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Recently, it was shown that fibroblast‐like cells (FLCs) possess the apparatus to mediate purinergic motor neurotransmission in the gastrointestinal tract. However, the electrophysiological properties of FLCs in situ have not been determined.
We recorded two patterns of slow waves from longitudinal smooth muscle cells and circular smooth muscle cells, large amplitude slow waves from interstitial cells of Cajal, and spontaneous transient hyperpolarizations (STHs) from FLCs in the rabbit small intestine using intracellular recording combined with dye injection to identify the cellular morphology of impaled cells.
Drugs that inhibit the signalling pathway involved in purinergic neurotransmission inhibited STHs in FLCs. Small amplitude STHs were recorded in smooth muscle cells but not in interstitial cells of Cajal, suggesting that STHs from FLCs were conducted passively to smooth muscle cells.
We conclude that FLCs display the molecular apparatus necessary to mediate purinergic neurotransmission and may tonically dampen smooth muscle excitability in the rabbit small intestine by an ongoing discharge of STHs.
Four types of electrical activity were recorded and related to cell structure by intracellular recording and dye injection into impaled cells in muscles of rabbit small intestine. The specific cell types from which recordings were made were longitudinal smooth muscle cells (LSMCs), circular smooth muscle cells (CSMCs), interstitial cells of Cajal distributed in the myenteric region (ICC‐MY) and fibroblast‐like cells (FLCs). Slow waves (slow wavesSMC) were recorded from LSMCs and CSMCs. Slow waves (slow wavesICC) were of greatest amplitude (>50 mV) and highest maximum rate of rise (>10 V s−1) in ICC‐MY. The dominant activity in FLCs was spontaneous transient hyperpolarizations (STHs), with maximum amplitudes above 30 mV. STHs were often superimposed upon small amplitude slow waves (slow wavesFLC). STHs displayed a cyclical pattern of discharge irrespective of background slow wave activity. STHs were inhibited by MRS2500 (3 μm), a P2Y1 antagonist, and abolished by apamin (0.3 μm), a blocker of small conductance Ca2+‐activated K+ channels. Small amplitude STHs (<15 mV) were detected in smooth muscle layers, whereas STHs were not resolved in cells identified as ICC‐MY. Electrical field stimulation evoked purinergic inhibitory junction potentials (IJPs) in CSMCs. Purinergic IJPs were not recorded from ICC‐MY. These results suggest that FLCs may regulate smooth muscle excitability in the rabbit small intestine via generation of rhythmic apamin‐sensitive STHs. Stimulation of P2Y1 receptors modulates the amplitudes of STHs. Our results also suggest that purinergic inhibitory motor neurons regulate the motility of the rabbit small intestine by causing IJPs in FLCs that conduct to CSMCs.</description><identifier>ISSN: 0022-3751</identifier><identifier>EISSN: 1469-7793</identifier><identifier>DOI: 10.1113/jphysiol.2014.276337</identifier><identifier>PMID: 25217377</identifier><identifier>CODEN: JPHYA7</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Alimentary ; Animals ; Interstitial Cells of Cajal - physiology ; Male ; Membrane Potentials - physiology ; Myocytes, Smooth Muscle - physiology ; Purines - metabolism ; Rabbits ; Synaptic Transmission - physiology</subject><ispartof>The Journal of physiology, 2014-11, Vol.592 (21), p.4733-4745</ispartof><rights>2014 The Authors. The Journal of Physiology © 2014 The Physiological Society</rights><rights>2014 The Authors. The Journal of Physiology © 2014 The Physiological Society.</rights><rights>Journal compilation © 2014 The Physiological Society</rights><rights>2014 The Authors. The Journal of Physiology © 2014 The Physiological Society 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5524-b2fe49dd4fe4138f62342738315ba3cb8f546c388876d8289f1ec4444400b6bc3</citedby><cites>FETCH-LOGICAL-c5524-b2fe49dd4fe4138f62342738315ba3cb8f546c388876d8289f1ec4444400b6bc3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4253473/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4253473/$$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/25217377$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kito, Yoshihiko</creatorcontrib><creatorcontrib>Kurahashi, Masaaki</creatorcontrib><creatorcontrib>Mitsui, Retsu</creatorcontrib><creatorcontrib>Ward, Sean M.</creatorcontrib><creatorcontrib>Sanders, Kenton M.</creatorcontrib><title>Spontaneous transient hyperpolarizations in the rabbit small intestine</title><title>The Journal of physiology</title><addtitle>J Physiol</addtitle><description>Key points
Recently, it was shown that fibroblast‐like cells (FLCs) possess the apparatus to mediate purinergic motor neurotransmission in the gastrointestinal tract. However, the electrophysiological properties of FLCs in situ have not been determined.
We recorded two patterns of slow waves from longitudinal smooth muscle cells and circular smooth muscle cells, large amplitude slow waves from interstitial cells of Cajal, and spontaneous transient hyperpolarizations (STHs) from FLCs in the rabbit small intestine using intracellular recording combined with dye injection to identify the cellular morphology of impaled cells.
Drugs that inhibit the signalling pathway involved in purinergic neurotransmission inhibited STHs in FLCs. Small amplitude STHs were recorded in smooth muscle cells but not in interstitial cells of Cajal, suggesting that STHs from FLCs were conducted passively to smooth muscle cells.
We conclude that FLCs display the molecular apparatus necessary to mediate purinergic neurotransmission and may tonically dampen smooth muscle excitability in the rabbit small intestine by an ongoing discharge of STHs.
Four types of electrical activity were recorded and related to cell structure by intracellular recording and dye injection into impaled cells in muscles of rabbit small intestine. The specific cell types from which recordings were made were longitudinal smooth muscle cells (LSMCs), circular smooth muscle cells (CSMCs), interstitial cells of Cajal distributed in the myenteric region (ICC‐MY) and fibroblast‐like cells (FLCs). Slow waves (slow wavesSMC) were recorded from LSMCs and CSMCs. Slow waves (slow wavesICC) were of greatest amplitude (>50 mV) and highest maximum rate of rise (>10 V s−1) in ICC‐MY. The dominant activity in FLCs was spontaneous transient hyperpolarizations (STHs), with maximum amplitudes above 30 mV. STHs were often superimposed upon small amplitude slow waves (slow wavesFLC). STHs displayed a cyclical pattern of discharge irrespective of background slow wave activity. STHs were inhibited by MRS2500 (3 μm), a P2Y1 antagonist, and abolished by apamin (0.3 μm), a blocker of small conductance Ca2+‐activated K+ channels. Small amplitude STHs (<15 mV) were detected in smooth muscle layers, whereas STHs were not resolved in cells identified as ICC‐MY. Electrical field stimulation evoked purinergic inhibitory junction potentials (IJPs) in CSMCs. Purinergic IJPs were not recorded from ICC‐MY. These results suggest that FLCs may regulate smooth muscle excitability in the rabbit small intestine via generation of rhythmic apamin‐sensitive STHs. Stimulation of P2Y1 receptors modulates the amplitudes of STHs. Our results also suggest that purinergic inhibitory motor neurons regulate the motility of the rabbit small intestine by causing IJPs in FLCs that conduct to CSMCs.</description><subject>Alimentary</subject><subject>Animals</subject><subject>Interstitial Cells of Cajal - physiology</subject><subject>Male</subject><subject>Membrane Potentials - physiology</subject><subject>Myocytes, Smooth Muscle - physiology</subject><subject>Purines - metabolism</subject><subject>Rabbits</subject><subject>Synaptic Transmission - physiology</subject><issn>0022-3751</issn><issn>1469-7793</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU9rGzEQxUVpaRy33yCEhV5yWVfSSCvtJVBMnD8YWmh6Ftq1NpaRpY20TnA-fWQ2CWlP1WVA85vHm3kInRA8I4TA902_3icb3IxiwmZUVADiA5oQVtWlEDV8RBOMKS1BcHKEjlPaYEwA1_VndEQ5JQKEmKDF7z74QXsTdqkYovbJGj8U631vYh-cjvZJDzb4VFhfDGtTRN00dijSVjuX_waTBuvNF_Sp0y6Zry91iv4sLm7nV-Xy5-X1_MeybDmnrGxoZ1i9WrFcCMiuosCoAAmENxraRnacVS1IKUW1klTWHTEtOzyMm6ppYYrOR91-12zNqs1eo3aqj3ar414FbdXfHW_X6i48KEY5MAFZ4OxFIIb7XTavtja1xrnxBIpUNF-Ncy4y-u0fdBN20ef1MkVkzaQAmik2Um0MKUXTvZkhWB2CUq9BqUNQagwqj52-X-Rt6DWZDNQj8Gid2f-XqLq9-VUBZ_AMCiukbQ</recordid><startdate>20141101</startdate><enddate>20141101</enddate><creator>Kito, Yoshihiko</creator><creator>Kurahashi, Masaaki</creator><creator>Mitsui, Retsu</creator><creator>Ward, Sean M.</creator><creator>Sanders, Kenton M.</creator><general>Wiley Subscription Services, Inc</general><general>BlackWell Publishing Ltd</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>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></search><sort><creationdate>20141101</creationdate><title>Spontaneous transient hyperpolarizations in the rabbit small intestine</title><author>Kito, Yoshihiko ; Kurahashi, Masaaki ; Mitsui, Retsu ; Ward, Sean M. ; Sanders, Kenton M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5524-b2fe49dd4fe4138f62342738315ba3cb8f546c388876d8289f1ec4444400b6bc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Alimentary</topic><topic>Animals</topic><topic>Interstitial Cells of Cajal - physiology</topic><topic>Male</topic><topic>Membrane Potentials - physiology</topic><topic>Myocytes, Smooth Muscle - physiology</topic><topic>Purines - metabolism</topic><topic>Rabbits</topic><topic>Synaptic Transmission - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kito, Yoshihiko</creatorcontrib><creatorcontrib>Kurahashi, Masaaki</creatorcontrib><creatorcontrib>Mitsui, Retsu</creatorcontrib><creatorcontrib>Ward, Sean M.</creatorcontrib><creatorcontrib>Sanders, Kenton 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>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>Kito, Yoshihiko</au><au>Kurahashi, Masaaki</au><au>Mitsui, Retsu</au><au>Ward, Sean M.</au><au>Sanders, Kenton M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Spontaneous transient hyperpolarizations in the rabbit small intestine</atitle><jtitle>The Journal of physiology</jtitle><addtitle>J Physiol</addtitle><date>2014-11-01</date><risdate>2014</risdate><volume>592</volume><issue>21</issue><spage>4733</spage><epage>4745</epage><pages>4733-4745</pages><issn>0022-3751</issn><eissn>1469-7793</eissn><coden>JPHYA7</coden><abstract>Key points
Recently, it was shown that fibroblast‐like cells (FLCs) possess the apparatus to mediate purinergic motor neurotransmission in the gastrointestinal tract. However, the electrophysiological properties of FLCs in situ have not been determined.
We recorded two patterns of slow waves from longitudinal smooth muscle cells and circular smooth muscle cells, large amplitude slow waves from interstitial cells of Cajal, and spontaneous transient hyperpolarizations (STHs) from FLCs in the rabbit small intestine using intracellular recording combined with dye injection to identify the cellular morphology of impaled cells.
Drugs that inhibit the signalling pathway involved in purinergic neurotransmission inhibited STHs in FLCs. Small amplitude STHs were recorded in smooth muscle cells but not in interstitial cells of Cajal, suggesting that STHs from FLCs were conducted passively to smooth muscle cells.
We conclude that FLCs display the molecular apparatus necessary to mediate purinergic neurotransmission and may tonically dampen smooth muscle excitability in the rabbit small intestine by an ongoing discharge of STHs.
Four types of electrical activity were recorded and related to cell structure by intracellular recording and dye injection into impaled cells in muscles of rabbit small intestine. The specific cell types from which recordings were made were longitudinal smooth muscle cells (LSMCs), circular smooth muscle cells (CSMCs), interstitial cells of Cajal distributed in the myenteric region (ICC‐MY) and fibroblast‐like cells (FLCs). Slow waves (slow wavesSMC) were recorded from LSMCs and CSMCs. Slow waves (slow wavesICC) were of greatest amplitude (>50 mV) and highest maximum rate of rise (>10 V s−1) in ICC‐MY. The dominant activity in FLCs was spontaneous transient hyperpolarizations (STHs), with maximum amplitudes above 30 mV. STHs were often superimposed upon small amplitude slow waves (slow wavesFLC). STHs displayed a cyclical pattern of discharge irrespective of background slow wave activity. STHs were inhibited by MRS2500 (3 μm), a P2Y1 antagonist, and abolished by apamin (0.3 μm), a blocker of small conductance Ca2+‐activated K+ channels. Small amplitude STHs (<15 mV) were detected in smooth muscle layers, whereas STHs were not resolved in cells identified as ICC‐MY. Electrical field stimulation evoked purinergic inhibitory junction potentials (IJPs) in CSMCs. Purinergic IJPs were not recorded from ICC‐MY. These results suggest that FLCs may regulate smooth muscle excitability in the rabbit small intestine via generation of rhythmic apamin‐sensitive STHs. Stimulation of P2Y1 receptors modulates the amplitudes of STHs. Our results also suggest that purinergic inhibitory motor neurons regulate the motility of the rabbit small intestine by causing IJPs in FLCs that conduct to CSMCs.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>25217377</pmid><doi>10.1113/jphysiol.2014.276337</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Alimentary Animals Interstitial Cells of Cajal - physiology Male Membrane Potentials - physiology Myocytes, Smooth Muscle - physiology Purines - metabolism Rabbits Synaptic Transmission - physiology |
| title | Spontaneous transient hyperpolarizations in the rabbit small intestine |
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