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Coordinated cadherin functions sculpt respiratory motor circuit connectivity
Breathing, and the motor circuits that control it, is essential for life. At the core of respiratory circuits are Dbx1-derived interneurons, which generate the rhythm and pattern of breathing, and phrenic motor neurons (MNs), which provide the final motor output that drives diaphragm muscle contract...
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creator | Vagnozzi, Alicia N Moore, Matthew T Lin, Minshan Brozost, Elyse M Kc, Ritesh Agarwal, Aambar Schwarz, Lindsay A Duan, Xin Zampieri, Niccolò Landmesser, Lynn T Philippidou, Polyxeni |
description | Breathing, and the motor circuits that control it, is essential for life. At the core of respiratory circuits are Dbx1-derived interneurons, which generate the rhythm and pattern of breathing, and phrenic motor neurons (MNs), which provide the final motor output that drives diaphragm muscle contractions during inspiration. Despite their critical function, the principles that dictate how respiratory circuits assemble are unknown. Here, we show that coordinated activity of a type I cadherin (N-cadherin) and type II cadherins (Cadherin-6, -9, and -10) is required in both MNs and Dbx1-derived neurons to generate robust respiratory motor output. Both MN- and Dbx1-specific cadherin inactivation in mice during a critical developmental window results in perinatal lethality due to respiratory failure and a striking reduction in phrenic MN bursting activity. This combinatorial cadherin code is required to establish phrenic MN cell body and dendritic topography; surprisingly, however, cell body position appears to be dispensable for the targeting of phrenic MNs by descending respiratory inputs. Our findings demonstrate that type I and II cadherins function cooperatively throughout the respiratory circuit to generate a robust breathing output and reveal novel strategies that drive the assembly of motor circuits. |
doi_str_mv | 10.7554/ELIFE.82116 |
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At the core of respiratory circuits are Dbx1-derived interneurons, which generate the rhythm and pattern of breathing, and phrenic motor neurons (MNs), which provide the final motor output that drives diaphragm muscle contractions during inspiration. Despite their critical function, the principles that dictate how respiratory circuits assemble are unknown. Here, we show that coordinated activity of a type I cadherin (N-cadherin) and type II cadherins (Cadherin-6, -9, and -10) is required in both MNs and Dbx1-derived neurons to generate robust respiratory motor output. Both MN- and Dbx1-specific cadherin inactivation in mice during a critical developmental window results in perinatal lethality due to respiratory failure and a striking reduction in phrenic MN bursting activity. This combinatorial cadherin code is required to establish phrenic MN cell body and dendritic topography; surprisingly, however, cell body position appears to be dispensable for the targeting of phrenic MNs by descending respiratory inputs. Our findings demonstrate that type I and II cadherins function cooperatively throughout the respiratory circuit to generate a robust breathing output and reveal novel strategies that drive the assembly of motor circuits.</description><identifier>ISSN: 2050-084X</identifier><identifier>EISSN: 2050-084X</identifier><identifier>DOI: 10.7554/ELIFE.82116</identifier><identifier>PMID: 36583530</identifier><language>eng</language><publisher>England: eLife Science Publications, Ltd</publisher><subject>Analysis ; Animals ; Cadherins ; Cell body ; Circuits ; Connectivity ; Dbx1 protein ; Developmental Biology ; Diaphragm ; Firing pattern ; Homeodomain Proteins - metabolism ; Identification and classification ; Interneurons ; Interneurons - physiology ; Lethality ; Mice ; Morphology ; Motor neurons ; Motor Neurons - physiology ; Motor task performance ; Muscle contraction ; N-Cadherin ; Neural networks ; Neurogenesis ; Neuroscience ; phrenic motor neurons ; Phrenic Nerve ; Properties ; Respiration ; respiratory circuits ; Respiratory failure ; Respiratory Rate ; rVRG ; Spinal cord ; Topography ; Ventilation</subject><ispartof>eLife, 2022-12, Vol.11</ispartof><rights>2022, Vagnozzi et al.</rights><rights>COPYRIGHT 2022 eLife Science Publications, Ltd.</rights><rights>2022, Vagnozzi et al. This work is published under https://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2022, Vagnozzi et al 2022 Vagnozzi et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c576t-7b962467f85b30f1816df912a98372bbf535fa214ea341edfb80bc966ec8e53b3</citedby><cites>FETCH-LOGICAL-c576t-7b962467f85b30f1816df912a98372bbf535fa214ea341edfb80bc966ec8e53b3</cites><orcidid>0000-0002-0733-3591 ; 0000-0002-2228-9453 ; 0000-0002-6152-8728</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2780677724/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2780677724?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36583530$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Vagnozzi, Alicia N</creatorcontrib><creatorcontrib>Moore, Matthew T</creatorcontrib><creatorcontrib>Lin, Minshan</creatorcontrib><creatorcontrib>Brozost, Elyse M</creatorcontrib><creatorcontrib>Kc, Ritesh</creatorcontrib><creatorcontrib>Agarwal, Aambar</creatorcontrib><creatorcontrib>Schwarz, Lindsay A</creatorcontrib><creatorcontrib>Duan, Xin</creatorcontrib><creatorcontrib>Zampieri, Niccolò</creatorcontrib><creatorcontrib>Landmesser, Lynn T</creatorcontrib><creatorcontrib>Philippidou, Polyxeni</creatorcontrib><title>Coordinated cadherin functions sculpt respiratory motor circuit connectivity</title><title>eLife</title><addtitle>Elife</addtitle><description>Breathing, and the motor circuits that control it, is essential for life. At the core of respiratory circuits are Dbx1-derived interneurons, which generate the rhythm and pattern of breathing, and phrenic motor neurons (MNs), which provide the final motor output that drives diaphragm muscle contractions during inspiration. Despite their critical function, the principles that dictate how respiratory circuits assemble are unknown. Here, we show that coordinated activity of a type I cadherin (N-cadherin) and type II cadherins (Cadherin-6, -9, and -10) is required in both MNs and Dbx1-derived neurons to generate robust respiratory motor output. Both MN- and Dbx1-specific cadherin inactivation in mice during a critical developmental window results in perinatal lethality due to respiratory failure and a striking reduction in phrenic MN bursting activity. This combinatorial cadherin code is required to establish phrenic MN cell body and dendritic topography; surprisingly, however, cell body position appears to be dispensable for the targeting of phrenic MNs by descending respiratory inputs. Our findings demonstrate that type I and II cadherins function cooperatively throughout the respiratory circuit to generate a robust breathing output and reveal novel strategies that drive the assembly of motor circuits.</description><subject>Analysis</subject><subject>Animals</subject><subject>Cadherins</subject><subject>Cell body</subject><subject>Circuits</subject><subject>Connectivity</subject><subject>Dbx1 protein</subject><subject>Developmental Biology</subject><subject>Diaphragm</subject><subject>Firing pattern</subject><subject>Homeodomain Proteins - metabolism</subject><subject>Identification and classification</subject><subject>Interneurons</subject><subject>Interneurons - physiology</subject><subject>Lethality</subject><subject>Mice</subject><subject>Morphology</subject><subject>Motor neurons</subject><subject>Motor Neurons - physiology</subject><subject>Motor task performance</subject><subject>Muscle contraction</subject><subject>N-Cadherin</subject><subject>Neural networks</subject><subject>Neurogenesis</subject><subject>Neuroscience</subject><subject>phrenic motor neurons</subject><subject>Phrenic Nerve</subject><subject>Properties</subject><subject>Respiration</subject><subject>respiratory circuits</subject><subject>Respiratory failure</subject><subject>Respiratory Rate</subject><subject>rVRG</subject><subject>Spinal cord</subject><subject>Topography</subject><subject>Ventilation</subject><issn>2050-084X</issn><issn>2050-084X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptkk1rGzEQhpfS0oQ0p97LQi8txa60Wn1dCsE4iWGh0A_oTWi1I0dmLbmSNtT_vkqcpnGpdBgxeuYVemeq6jVGc05p-3HZrS6Xc9FgzJ5Vpw2iaIZE--P5k_NJdZ7SBpXFWyGwfFmdEEYFoQSdVt0ihDg4rzMMtdHDDUTnazt5k13wqU5mGne5jpB2Luoc4r7ehhJq46KZXK5N8B4KfOvy_lX1wuoxwflDPKu-Xy6_La5n3eer1eKimxnKWZ7xXrKmZdwK2hNkscBssBI3WgrCm763lFCrG9yCJi2GwfYC9UYyBkYAJT05q1YH3SHojdpFt9Vxr4J26j4R4lrpmJ0ZQdlBAwgpe2x1q7kWbQ9MGoskabU1rGh9Omjtpn4LgwGfox6PRI9vvLtR63CrpMRINLIIvHsQiOHnBCmrrUsGxlF7CFNSDadSUikoLejbf9BNmKIvVhVKIMY5b9q_1FqXDzhvQ3nX3ImqC04YEax0tVDz_1BlD7B1pSlgXckfFbw_KihMhl95raeU1Orrl2P2w4E1MaQUwT76gZG6mzsFnbOg7ueu0G-eWvjI_pky8huaFdM2</recordid><startdate>20221230</startdate><enddate>20221230</enddate><creator>Vagnozzi, Alicia N</creator><creator>Moore, Matthew T</creator><creator>Lin, Minshan</creator><creator>Brozost, Elyse M</creator><creator>Kc, Ritesh</creator><creator>Agarwal, Aambar</creator><creator>Schwarz, Lindsay A</creator><creator>Duan, Xin</creator><creator>Zampieri, Niccolò</creator><creator>Landmesser, Lynn T</creator><creator>Philippidou, Polyxeni</creator><general>eLife Science Publications, Ltd</general><general>eLife Sciences Publications Ltd</general><general>eLife Sciences Publications, 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>ISR</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-0733-3591</orcidid><orcidid>https://orcid.org/0000-0002-2228-9453</orcidid><orcidid>https://orcid.org/0000-0002-6152-8728</orcidid></search><sort><creationdate>20221230</creationdate><title>Coordinated cadherin functions sculpt respiratory motor circuit connectivity</title><author>Vagnozzi, Alicia N ; Moore, Matthew T ; Lin, Minshan ; Brozost, Elyse M ; Kc, Ritesh ; Agarwal, Aambar ; Schwarz, Lindsay A ; Duan, Xin ; Zampieri, Niccolò ; Landmesser, Lynn T ; Philippidou, Polyxeni</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c576t-7b962467f85b30f1816df912a98372bbf535fa214ea341edfb80bc966ec8e53b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Cadherins</topic><topic>Cell body</topic><topic>Circuits</topic><topic>Connectivity</topic><topic>Dbx1 protein</topic><topic>Developmental Biology</topic><topic>Diaphragm</topic><topic>Firing pattern</topic><topic>Homeodomain Proteins - metabolism</topic><topic>Identification and classification</topic><topic>Interneurons</topic><topic>Interneurons - physiology</topic><topic>Lethality</topic><topic>Mice</topic><topic>Morphology</topic><topic>Motor neurons</topic><topic>Motor Neurons - physiology</topic><topic>Motor task performance</topic><topic>Muscle contraction</topic><topic>N-Cadherin</topic><topic>Neural networks</topic><topic>Neurogenesis</topic><topic>Neuroscience</topic><topic>phrenic motor neurons</topic><topic>Phrenic Nerve</topic><topic>Properties</topic><topic>Respiration</topic><topic>respiratory circuits</topic><topic>Respiratory failure</topic><topic>Respiratory Rate</topic><topic>rVRG</topic><topic>Spinal cord</topic><topic>Topography</topic><topic>Ventilation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Vagnozzi, Alicia N</creatorcontrib><creatorcontrib>Moore, Matthew T</creatorcontrib><creatorcontrib>Lin, Minshan</creatorcontrib><creatorcontrib>Brozost, Elyse M</creatorcontrib><creatorcontrib>Kc, Ritesh</creatorcontrib><creatorcontrib>Agarwal, Aambar</creatorcontrib><creatorcontrib>Schwarz, Lindsay A</creatorcontrib><creatorcontrib>Duan, Xin</creatorcontrib><creatorcontrib>Zampieri, Niccolò</creatorcontrib><creatorcontrib>Landmesser, Lynn T</creatorcontrib><creatorcontrib>Philippidou, Polyxeni</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Science (Gale in Context)</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection (Proquest)</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>ProQuest Science Journals</collection><collection>ProQuest Biological Science Journals</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>eLife</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Vagnozzi, Alicia N</au><au>Moore, Matthew T</au><au>Lin, Minshan</au><au>Brozost, Elyse M</au><au>Kc, Ritesh</au><au>Agarwal, Aambar</au><au>Schwarz, Lindsay A</au><au>Duan, Xin</au><au>Zampieri, Niccolò</au><au>Landmesser, Lynn T</au><au>Philippidou, Polyxeni</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Coordinated cadherin functions sculpt respiratory motor circuit connectivity</atitle><jtitle>eLife</jtitle><addtitle>Elife</addtitle><date>2022-12-30</date><risdate>2022</risdate><volume>11</volume><issn>2050-084X</issn><eissn>2050-084X</eissn><abstract>Breathing, and the motor circuits that control it, is essential for life. At the core of respiratory circuits are Dbx1-derived interneurons, which generate the rhythm and pattern of breathing, and phrenic motor neurons (MNs), which provide the final motor output that drives diaphragm muscle contractions during inspiration. Despite their critical function, the principles that dictate how respiratory circuits assemble are unknown. Here, we show that coordinated activity of a type I cadherin (N-cadherin) and type II cadherins (Cadherin-6, -9, and -10) is required in both MNs and Dbx1-derived neurons to generate robust respiratory motor output. Both MN- and Dbx1-specific cadherin inactivation in mice during a critical developmental window results in perinatal lethality due to respiratory failure and a striking reduction in phrenic MN bursting activity. This combinatorial cadherin code is required to establish phrenic MN cell body and dendritic topography; surprisingly, however, cell body position appears to be dispensable for the targeting of phrenic MNs by descending respiratory inputs. Our findings demonstrate that type I and II cadherins function cooperatively throughout the respiratory circuit to generate a robust breathing output and reveal novel strategies that drive the assembly of motor circuits.</abstract><cop>England</cop><pub>eLife Science Publications, Ltd</pub><pmid>36583530</pmid><doi>10.7554/ELIFE.82116</doi><orcidid>https://orcid.org/0000-0002-0733-3591</orcidid><orcidid>https://orcid.org/0000-0002-2228-9453</orcidid><orcidid>https://orcid.org/0000-0002-6152-8728</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Analysis Animals Cadherins Cell body Circuits Connectivity Dbx1 protein Developmental Biology Diaphragm Firing pattern Homeodomain Proteins - metabolism Identification and classification Interneurons Interneurons - physiology Lethality Mice Morphology Motor neurons Motor Neurons - physiology Motor task performance Muscle contraction N-Cadherin Neural networks Neurogenesis Neuroscience phrenic motor neurons Phrenic Nerve Properties Respiration respiratory circuits Respiratory failure Respiratory Rate rVRG Spinal cord Topography Ventilation |
title | Coordinated cadherin functions sculpt respiratory motor circuit connectivity |
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