Keratinocytes Communicate with Sensory Neurons via Synaptic‐like Contacts
Objective Pain, temperature, and itch are conventionally thought to be exclusively transduced by the intraepidermal nerve endings. Although recent studies have shown that epidermal keratinocytes also participate in sensory transduction, the mechanism underlying keratinocyte communication with intrae...
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| Veröffentlicht in: | Annals of neurology 2020-12, Vol.88 (6), p.1205-1219 |
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| container_title | Annals of neurology |
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| creator | Talagas, Matthieu Lebonvallet, Nicolas Leschiera, Raphael Sinquin, Gerard Elies, Philippe Haftek, Marek Pennec, Jean‐Pierre Ressnikoff, Denis La Padula, Veronica Le Garrec, Raphaele L'herondelle, Killian Mignen, Olivier Le Pottier, Laetitia Kerfant, Nathalie Reux, Alexia Marcorelles, Pascale Misery, Laurent |
| description | Objective
Pain, temperature, and itch are conventionally thought to be exclusively transduced by the intraepidermal nerve endings. Although recent studies have shown that epidermal keratinocytes also participate in sensory transduction, the mechanism underlying keratinocyte communication with intraepidermal nerve endings remains poorly understood. We sought to demonstrate the synaptic character of the contacts between keratinocytes and sensory neurons and their involvement in sensory communication between keratinocytes and sensory neurons.
Methods
Contacts were explored by morphological, molecular, and functional approaches in cocultures of epidermal keratinocytes and sensory neurons. To interrogate whether structures observed in vitro were also present in the human epidermis, in situ correlative light electron microscopy was performed on human skin biopsies.
Results
Epidermal keratinocytes dialogue with sensory neurons through en passant synaptic‐like contacts. These contacts have the ultrastructural features and molecular hallmarks of chemical synaptic‐like contacts: narrow intercellular cleft, keratinocyte synaptic vesicles expressing synaptophysin and synaptotagmin 1, and sensory information transmitted from keratinocytes to sensory neurons through SNARE‐mediated (syntaxin1) vesicle release.
Interpretation
By providing selective communication between keratinocytes and sensory neurons, synaptic‐like contacts are the hubs of a 2‐site receptor. The permanent epidermal turnover, implying a specific en passant structure and high plasticity, may have delayed their identification, thereby contributing to the long‐held concept of nerve endings passing freely between keratinocytes. The discovery of keratinocyte–sensory neuron synaptic‐like contacts may call for a reassessment of basic assumptions in cutaneous sensory perception and sheds new light on the pathophysiology of pain and itch as well as the physiology of touch. ANN NEUROL 2020;88:1205–1219 |
| doi_str_mv | 10.1002/ana.25912 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_hal_p</sourceid><recordid>TN_cdi_hal_primary_oai_HAL_hal_03368016v1</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2444602388</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3872-b0fca97038a5abe4bf1b520adb3ca68f8f83dd02793dc6a88fe9e4a7777b78483</originalsourceid><addsrcrecordid>eNp1kc9u1DAQhy0EokvhwAugSFzgkHb8J45zXK2Aoq7KoXC2Jo6juiT2YietcuMR-ox9ErxsKRIS9sGS9fkbz_wIeU3hhAKwU_R4wqqGsidkRStOS8VE85SsgEtRVpSLI_IipWsAaCSF5-SIs6airBYrcn5uI07OB7NMNhWbMI6zdwYnW9y66aq4tD6FuBQXdo7Bp-LGYXG5eNxNztz_vBvcd5sf-QnNlF6SZz0Oyb56OI_Jt48fvm7Oyu2XT583621puKpZ2UJvsKmBK6ywtaLtaVsxwK7lBqXq8-ZdB6xueGckKtXbxgqs82prJRQ_Ju8P3isc9C66EeOiAzp9tt7q_R1wLhVQeUMz--7A7mL4Mds06dElY4cBvQ1z0kwIIYFxtde-_Qe9DnP0uZNMSagrWQv-t7iJIaVo-8cfUND7NHROQ_9OI7NvHoxzO9rukfwz_gycHoBbN9jl_ya9vlgflL8AgkiTaw</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2460756743</pqid></control><display><type>article</type><title>Keratinocytes Communicate with Sensory Neurons via Synaptic‐like Contacts</title><source>MEDLINE</source><source>Wiley Online Library Journals Frontfile Complete</source><creator>Talagas, Matthieu ; Lebonvallet, Nicolas ; Leschiera, Raphael ; Sinquin, Gerard ; Elies, Philippe ; Haftek, Marek ; Pennec, Jean‐Pierre ; Ressnikoff, Denis ; La Padula, Veronica ; Le Garrec, Raphaele ; L'herondelle, Killian ; Mignen, Olivier ; Le Pottier, Laetitia ; Kerfant, Nathalie ; Reux, Alexia ; Marcorelles, Pascale ; Misery, Laurent</creator><creatorcontrib>Talagas, Matthieu ; Lebonvallet, Nicolas ; Leschiera, Raphael ; Sinquin, Gerard ; Elies, Philippe ; Haftek, Marek ; Pennec, Jean‐Pierre ; Ressnikoff, Denis ; La Padula, Veronica ; Le Garrec, Raphaele ; L'herondelle, Killian ; Mignen, Olivier ; Le Pottier, Laetitia ; Kerfant, Nathalie ; Reux, Alexia ; Marcorelles, Pascale ; Misery, Laurent</creatorcontrib><description>Objective
Pain, temperature, and itch are conventionally thought to be exclusively transduced by the intraepidermal nerve endings. Although recent studies have shown that epidermal keratinocytes also participate in sensory transduction, the mechanism underlying keratinocyte communication with intraepidermal nerve endings remains poorly understood. We sought to demonstrate the synaptic character of the contacts between keratinocytes and sensory neurons and their involvement in sensory communication between keratinocytes and sensory neurons.
Methods
Contacts were explored by morphological, molecular, and functional approaches in cocultures of epidermal keratinocytes and sensory neurons. To interrogate whether structures observed in vitro were also present in the human epidermis, in situ correlative light electron microscopy was performed on human skin biopsies.
Results
Epidermal keratinocytes dialogue with sensory neurons through en passant synaptic‐like contacts. These contacts have the ultrastructural features and molecular hallmarks of chemical synaptic‐like contacts: narrow intercellular cleft, keratinocyte synaptic vesicles expressing synaptophysin and synaptotagmin 1, and sensory information transmitted from keratinocytes to sensory neurons through SNARE‐mediated (syntaxin1) vesicle release.
Interpretation
By providing selective communication between keratinocytes and sensory neurons, synaptic‐like contacts are the hubs of a 2‐site receptor. The permanent epidermal turnover, implying a specific en passant structure and high plasticity, may have delayed their identification, thereby contributing to the long‐held concept of nerve endings passing freely between keratinocytes. The discovery of keratinocyte–sensory neuron synaptic‐like contacts may call for a reassessment of basic assumptions in cutaneous sensory perception and sheds new light on the pathophysiology of pain and itch as well as the physiology of touch. ANN NEUROL 2020;88:1205–1219</description><identifier>ISSN: 0364-5134</identifier><identifier>EISSN: 1531-8249</identifier><identifier>DOI: 10.1002/ana.25912</identifier><identifier>PMID: 32951274</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Adult ; Aged ; Animals ; Coculture Techniques ; Communication ; Electron microscopy ; Epidermis ; Epidermis - innervation ; Female ; Human performance ; Humans ; Keratinocytes ; Keratinocytes - metabolism ; Keratinocytes - ultrastructure ; Life Sciences ; Male ; Microscopy, Electron ; Middle Aged ; Nerve endings ; Neurons ; Pain ; Qa-SNARE Proteins - metabolism ; Rats ; Sensory neurons ; Sensory perception ; Sensory Receptor Cells - ultrastructure ; Sensory transduction ; SNAP receptors ; Synapses - ultrastructure ; Synaptic vesicles ; Synaptic Vesicles - metabolism ; Synaptophysin ; Synaptophysin - metabolism ; Synaptotagmin ; Synaptotagmin I - metabolism</subject><ispartof>Annals of neurology, 2020-12, Vol.88 (6), p.1205-1219</ispartof><rights>2020 American Neurological Association</rights><rights>2020 American Neurological Association.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3872-b0fca97038a5abe4bf1b520adb3ca68f8f83dd02793dc6a88fe9e4a7777b78483</citedby><cites>FETCH-LOGICAL-c3872-b0fca97038a5abe4bf1b520adb3ca68f8f83dd02793dc6a88fe9e4a7777b78483</cites><orcidid>0000-0001-6769-3364 ; 0000-0001-8088-7059 ; 0000-0003-0427-8993 ; 0000-0002-0269-9076 ; 0000-0001-7913-6119</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fana.25912$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fana.25912$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32951274$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03368016$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Talagas, Matthieu</creatorcontrib><creatorcontrib>Lebonvallet, Nicolas</creatorcontrib><creatorcontrib>Leschiera, Raphael</creatorcontrib><creatorcontrib>Sinquin, Gerard</creatorcontrib><creatorcontrib>Elies, Philippe</creatorcontrib><creatorcontrib>Haftek, Marek</creatorcontrib><creatorcontrib>Pennec, Jean‐Pierre</creatorcontrib><creatorcontrib>Ressnikoff, Denis</creatorcontrib><creatorcontrib>La Padula, Veronica</creatorcontrib><creatorcontrib>Le Garrec, Raphaele</creatorcontrib><creatorcontrib>L'herondelle, Killian</creatorcontrib><creatorcontrib>Mignen, Olivier</creatorcontrib><creatorcontrib>Le Pottier, Laetitia</creatorcontrib><creatorcontrib>Kerfant, Nathalie</creatorcontrib><creatorcontrib>Reux, Alexia</creatorcontrib><creatorcontrib>Marcorelles, Pascale</creatorcontrib><creatorcontrib>Misery, Laurent</creatorcontrib><title>Keratinocytes Communicate with Sensory Neurons via Synaptic‐like Contacts</title><title>Annals of neurology</title><addtitle>Ann Neurol</addtitle><description>Objective
Pain, temperature, and itch are conventionally thought to be exclusively transduced by the intraepidermal nerve endings. Although recent studies have shown that epidermal keratinocytes also participate in sensory transduction, the mechanism underlying keratinocyte communication with intraepidermal nerve endings remains poorly understood. We sought to demonstrate the synaptic character of the contacts between keratinocytes and sensory neurons and their involvement in sensory communication between keratinocytes and sensory neurons.
Methods
Contacts were explored by morphological, molecular, and functional approaches in cocultures of epidermal keratinocytes and sensory neurons. To interrogate whether structures observed in vitro were also present in the human epidermis, in situ correlative light electron microscopy was performed on human skin biopsies.
Results
Epidermal keratinocytes dialogue with sensory neurons through en passant synaptic‐like contacts. These contacts have the ultrastructural features and molecular hallmarks of chemical synaptic‐like contacts: narrow intercellular cleft, keratinocyte synaptic vesicles expressing synaptophysin and synaptotagmin 1, and sensory information transmitted from keratinocytes to sensory neurons through SNARE‐mediated (syntaxin1) vesicle release.
Interpretation
By providing selective communication between keratinocytes and sensory neurons, synaptic‐like contacts are the hubs of a 2‐site receptor. The permanent epidermal turnover, implying a specific en passant structure and high plasticity, may have delayed their identification, thereby contributing to the long‐held concept of nerve endings passing freely between keratinocytes. The discovery of keratinocyte–sensory neuron synaptic‐like contacts may call for a reassessment of basic assumptions in cutaneous sensory perception and sheds new light on the pathophysiology of pain and itch as well as the physiology of touch. ANN NEUROL 2020;88:1205–1219</description><subject>Adult</subject><subject>Aged</subject><subject>Animals</subject><subject>Coculture Techniques</subject><subject>Communication</subject><subject>Electron microscopy</subject><subject>Epidermis</subject><subject>Epidermis - innervation</subject><subject>Female</subject><subject>Human performance</subject><subject>Humans</subject><subject>Keratinocytes</subject><subject>Keratinocytes - metabolism</subject><subject>Keratinocytes - ultrastructure</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Microscopy, Electron</subject><subject>Middle Aged</subject><subject>Nerve endings</subject><subject>Neurons</subject><subject>Pain</subject><subject>Qa-SNARE Proteins - metabolism</subject><subject>Rats</subject><subject>Sensory neurons</subject><subject>Sensory perception</subject><subject>Sensory Receptor Cells - ultrastructure</subject><subject>Sensory transduction</subject><subject>SNAP receptors</subject><subject>Synapses - ultrastructure</subject><subject>Synaptic vesicles</subject><subject>Synaptic Vesicles - metabolism</subject><subject>Synaptophysin</subject><subject>Synaptophysin - metabolism</subject><subject>Synaptotagmin</subject><subject>Synaptotagmin I - metabolism</subject><issn>0364-5134</issn><issn>1531-8249</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kc9u1DAQhy0EokvhwAugSFzgkHb8J45zXK2Aoq7KoXC2Jo6juiT2YietcuMR-ox9ErxsKRIS9sGS9fkbz_wIeU3hhAKwU_R4wqqGsidkRStOS8VE85SsgEtRVpSLI_IipWsAaCSF5-SIs6airBYrcn5uI07OB7NMNhWbMI6zdwYnW9y66aq4tD6FuBQXdo7Bp-LGYXG5eNxNztz_vBvcd5sf-QnNlF6SZz0Oyb56OI_Jt48fvm7Oyu2XT583621puKpZ2UJvsKmBK6ywtaLtaVsxwK7lBqXq8-ZdB6xueGckKtXbxgqs82prJRQ_Ju8P3isc9C66EeOiAzp9tt7q_R1wLhVQeUMz--7A7mL4Mds06dElY4cBvQ1z0kwIIYFxtde-_Qe9DnP0uZNMSagrWQv-t7iJIaVo-8cfUND7NHROQ_9OI7NvHoxzO9rukfwz_gycHoBbN9jl_ya9vlgflL8AgkiTaw</recordid><startdate>202012</startdate><enddate>202012</enddate><creator>Talagas, Matthieu</creator><creator>Lebonvallet, Nicolas</creator><creator>Leschiera, Raphael</creator><creator>Sinquin, Gerard</creator><creator>Elies, Philippe</creator><creator>Haftek, Marek</creator><creator>Pennec, Jean‐Pierre</creator><creator>Ressnikoff, Denis</creator><creator>La Padula, Veronica</creator><creator>Le Garrec, Raphaele</creator><creator>L'herondelle, Killian</creator><creator>Mignen, Olivier</creator><creator>Le Pottier, Laetitia</creator><creator>Kerfant, Nathalie</creator><creator>Reux, Alexia</creator><creator>Marcorelles, Pascale</creator><creator>Misery, Laurent</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><general>Wiley</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>7U7</scope><scope>C1K</scope><scope>K9.</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0001-6769-3364</orcidid><orcidid>https://orcid.org/0000-0001-8088-7059</orcidid><orcidid>https://orcid.org/0000-0003-0427-8993</orcidid><orcidid>https://orcid.org/0000-0002-0269-9076</orcidid><orcidid>https://orcid.org/0000-0001-7913-6119</orcidid></search><sort><creationdate>202012</creationdate><title>Keratinocytes Communicate with Sensory Neurons via Synaptic‐like Contacts</title><author>Talagas, Matthieu ; Lebonvallet, Nicolas ; Leschiera, Raphael ; Sinquin, Gerard ; Elies, Philippe ; Haftek, Marek ; Pennec, Jean‐Pierre ; Ressnikoff, Denis ; La Padula, Veronica ; Le Garrec, Raphaele ; L'herondelle, Killian ; Mignen, Olivier ; Le Pottier, Laetitia ; Kerfant, Nathalie ; Reux, Alexia ; Marcorelles, Pascale ; Misery, Laurent</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3872-b0fca97038a5abe4bf1b520adb3ca68f8f83dd02793dc6a88fe9e4a7777b78483</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adult</topic><topic>Aged</topic><topic>Animals</topic><topic>Coculture Techniques</topic><topic>Communication</topic><topic>Electron microscopy</topic><topic>Epidermis</topic><topic>Epidermis - innervation</topic><topic>Female</topic><topic>Human performance</topic><topic>Humans</topic><topic>Keratinocytes</topic><topic>Keratinocytes - metabolism</topic><topic>Keratinocytes - ultrastructure</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Microscopy, Electron</topic><topic>Middle Aged</topic><topic>Nerve endings</topic><topic>Neurons</topic><topic>Pain</topic><topic>Qa-SNARE Proteins - metabolism</topic><topic>Rats</topic><topic>Sensory neurons</topic><topic>Sensory perception</topic><topic>Sensory Receptor Cells - ultrastructure</topic><topic>Sensory transduction</topic><topic>SNAP receptors</topic><topic>Synapses - ultrastructure</topic><topic>Synaptic vesicles</topic><topic>Synaptic Vesicles - metabolism</topic><topic>Synaptophysin</topic><topic>Synaptophysin - metabolism</topic><topic>Synaptotagmin</topic><topic>Synaptotagmin I - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Talagas, Matthieu</creatorcontrib><creatorcontrib>Lebonvallet, Nicolas</creatorcontrib><creatorcontrib>Leschiera, Raphael</creatorcontrib><creatorcontrib>Sinquin, Gerard</creatorcontrib><creatorcontrib>Elies, Philippe</creatorcontrib><creatorcontrib>Haftek, Marek</creatorcontrib><creatorcontrib>Pennec, Jean‐Pierre</creatorcontrib><creatorcontrib>Ressnikoff, Denis</creatorcontrib><creatorcontrib>La Padula, Veronica</creatorcontrib><creatorcontrib>Le Garrec, Raphaele</creatorcontrib><creatorcontrib>L'herondelle, Killian</creatorcontrib><creatorcontrib>Mignen, Olivier</creatorcontrib><creatorcontrib>Le Pottier, Laetitia</creatorcontrib><creatorcontrib>Kerfant, Nathalie</creatorcontrib><creatorcontrib>Reux, Alexia</creatorcontrib><creatorcontrib>Marcorelles, Pascale</creatorcontrib><creatorcontrib>Misery, Laurent</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>Toxicology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Annals of neurology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Talagas, Matthieu</au><au>Lebonvallet, Nicolas</au><au>Leschiera, Raphael</au><au>Sinquin, Gerard</au><au>Elies, Philippe</au><au>Haftek, Marek</au><au>Pennec, Jean‐Pierre</au><au>Ressnikoff, Denis</au><au>La Padula, Veronica</au><au>Le Garrec, Raphaele</au><au>L'herondelle, Killian</au><au>Mignen, Olivier</au><au>Le Pottier, Laetitia</au><au>Kerfant, Nathalie</au><au>Reux, Alexia</au><au>Marcorelles, Pascale</au><au>Misery, Laurent</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Keratinocytes Communicate with Sensory Neurons via Synaptic‐like Contacts</atitle><jtitle>Annals of neurology</jtitle><addtitle>Ann Neurol</addtitle><date>2020-12</date><risdate>2020</risdate><volume>88</volume><issue>6</issue><spage>1205</spage><epage>1219</epage><pages>1205-1219</pages><issn>0364-5134</issn><eissn>1531-8249</eissn><abstract>Objective
Pain, temperature, and itch are conventionally thought to be exclusively transduced by the intraepidermal nerve endings. Although recent studies have shown that epidermal keratinocytes also participate in sensory transduction, the mechanism underlying keratinocyte communication with intraepidermal nerve endings remains poorly understood. We sought to demonstrate the synaptic character of the contacts between keratinocytes and sensory neurons and their involvement in sensory communication between keratinocytes and sensory neurons.
Methods
Contacts were explored by morphological, molecular, and functional approaches in cocultures of epidermal keratinocytes and sensory neurons. To interrogate whether structures observed in vitro were also present in the human epidermis, in situ correlative light electron microscopy was performed on human skin biopsies.
Results
Epidermal keratinocytes dialogue with sensory neurons through en passant synaptic‐like contacts. These contacts have the ultrastructural features and molecular hallmarks of chemical synaptic‐like contacts: narrow intercellular cleft, keratinocyte synaptic vesicles expressing synaptophysin and synaptotagmin 1, and sensory information transmitted from keratinocytes to sensory neurons through SNARE‐mediated (syntaxin1) vesicle release.
Interpretation
By providing selective communication between keratinocytes and sensory neurons, synaptic‐like contacts are the hubs of a 2‐site receptor. The permanent epidermal turnover, implying a specific en passant structure and high plasticity, may have delayed their identification, thereby contributing to the long‐held concept of nerve endings passing freely between keratinocytes. The discovery of keratinocyte–sensory neuron synaptic‐like contacts may call for a reassessment of basic assumptions in cutaneous sensory perception and sheds new light on the pathophysiology of pain and itch as well as the physiology of touch. ANN NEUROL 2020;88:1205–1219</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>32951274</pmid><doi>10.1002/ana.25912</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-6769-3364</orcidid><orcidid>https://orcid.org/0000-0001-8088-7059</orcidid><orcidid>https://orcid.org/0000-0003-0427-8993</orcidid><orcidid>https://orcid.org/0000-0002-0269-9076</orcidid><orcidid>https://orcid.org/0000-0001-7913-6119</orcidid></addata></record> |
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| ispartof | Annals of neurology, 2020-12, Vol.88 (6), p.1205-1219 |
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| source | MEDLINE; Wiley Online Library Journals Frontfile Complete |
| subjects | Adult Aged Animals Coculture Techniques Communication Electron microscopy Epidermis Epidermis - innervation Female Human performance Humans Keratinocytes Keratinocytes - metabolism Keratinocytes - ultrastructure Life Sciences Male Microscopy, Electron Middle Aged Nerve endings Neurons Pain Qa-SNARE Proteins - metabolism Rats Sensory neurons Sensory perception Sensory Receptor Cells - ultrastructure Sensory transduction SNAP receptors Synapses - ultrastructure Synaptic vesicles Synaptic Vesicles - metabolism Synaptophysin Synaptophysin - metabolism Synaptotagmin Synaptotagmin I - metabolism |
| title | Keratinocytes Communicate with Sensory Neurons via Synaptic‐like Contacts |
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