Differential requirement for DICER1 activity during the development of mitral and tricuspid valves
Mitral and tricuspid valves are essential for unidirectional blood flow in the heart. They are derived from similar cell sources, and yet congenital dysplasia affecting both valves is clinically rare, suggesting the presence of differential regulatory mechanisms underlying their development. Here, w...
Gespeichert in:
Veröffentlicht in: | Journal of cell science 2022-09, Vol.135 (17) |
---|---|
Hauptverfasser: | , , , , , , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | |
---|---|
container_issue | 17 |
container_start_page | |
container_title | Journal of cell science |
container_volume | 135 |
creator | Yan, Shun Peng, Yin Lu, Jin Shakil, Saima Shi, Yang Crossman, David K Johnson, Walter H Liu, Shanrun Rokosh, Donald G Lincoln, Joy Wang, Qin Jiao, Kai |
description | Mitral and tricuspid valves are essential for unidirectional blood flow in the heart. They are derived from similar cell sources, and yet congenital dysplasia affecting both valves is clinically rare, suggesting the presence of differential regulatory mechanisms underlying their development. Here, we specifically inactivated Dicer1 in the endocardium during cardiogenesis and found that Dicer1 deletion caused congenital mitral valve stenosis and regurgitation, whereas it had no impact on other valves. We showed that hyperplastic mitral valves were caused by abnormal condensation and extracellular matrix (ECM) remodeling. Our single-cell RNA sequencing analysis revealed impaired maturation of mesenchymal cells and abnormal expression of ECM genes in mutant mitral valves. Furthermore, expression of a set of miRNAs that target ECM genes was significantly lower in tricuspid valves compared to mitral valves, consistent with the idea that the miRNAs are differentially required for mitral and tricuspid valve development. We thus reveal miRNA-mediated gene regulation as a novel molecular mechanism that differentially regulates mitral and tricuspid valve development, thereby enhancing our understanding of the non-association of inborn mitral and tricuspid dysplasia observed clinically. |
doi_str_mv | 10.1242/jcs.259783 |
format | Article |
fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9482344</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2700638172</sourcerecordid><originalsourceid>FETCH-LOGICAL-c378t-ef8dcb70ca20bc4baa905040743cb7e45ef29833fa42ea877b14df476fca91d63</originalsourceid><addsrcrecordid>eNpVkctKAzEUhoMotl42PoBkKcJobtNMNoK09QKCILoOmcyJpsylJjMDfXujVdFVODkf3_nhR-iEkgvKBLtc2XjBciULvoOmVEiZKcrlLpoSwmimcs4n6CDGFSFEMiX30YTnSswEy6eoXHjnIEDbe1PjAO-DD9CkEbsu4MX9fPlEsbG9H32_wdUQfPuK-zfAFYxQd-svtHO48X1IAtNWuA_eDnHtKzyaeoR4hPacqSMcf7-H6OVm-Ty_yx4eb-_n1w-Z5bLoM3BFZUtJrGGktKI0RpGcCCIFT98gcnBMFZw7IxiYQsqSisoJOXPWKFrN-CG62nrXQ9lAZVOyFEmvg29M2OjOeP1_0_o3_dqNWomCcSGS4OxbELr3AWKvGx8t1LVpoRuiZpKQGS-oZAk936I2dDEGcL9nKNGfpehUit6WkuDTv8F-0Z8W-Ad7OYrV</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2700638172</pqid></control><display><type>article</type><title>Differential requirement for DICER1 activity during the development of mitral and tricuspid valves</title><source>MEDLINE</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Alma/SFX Local Collection</source><source>Company of Biologists</source><creator>Yan, Shun ; Peng, Yin ; Lu, Jin ; Shakil, Saima ; Shi, Yang ; Crossman, David K ; Johnson, Walter H ; Liu, Shanrun ; Rokosh, Donald G ; Lincoln, Joy ; Wang, Qin ; Jiao, Kai</creator><creatorcontrib>Yan, Shun ; Peng, Yin ; Lu, Jin ; Shakil, Saima ; Shi, Yang ; Crossman, David K ; Johnson, Walter H ; Liu, Shanrun ; Rokosh, Donald G ; Lincoln, Joy ; Wang, Qin ; Jiao, Kai</creatorcontrib><description>Mitral and tricuspid valves are essential for unidirectional blood flow in the heart. They are derived from similar cell sources, and yet congenital dysplasia affecting both valves is clinically rare, suggesting the presence of differential regulatory mechanisms underlying their development. Here, we specifically inactivated Dicer1 in the endocardium during cardiogenesis and found that Dicer1 deletion caused congenital mitral valve stenosis and regurgitation, whereas it had no impact on other valves. We showed that hyperplastic mitral valves were caused by abnormal condensation and extracellular matrix (ECM) remodeling. Our single-cell RNA sequencing analysis revealed impaired maturation of mesenchymal cells and abnormal expression of ECM genes in mutant mitral valves. Furthermore, expression of a set of miRNAs that target ECM genes was significantly lower in tricuspid valves compared to mitral valves, consistent with the idea that the miRNAs are differentially required for mitral and tricuspid valve development. We thus reveal miRNA-mediated gene regulation as a novel molecular mechanism that differentially regulates mitral and tricuspid valve development, thereby enhancing our understanding of the non-association of inborn mitral and tricuspid dysplasia observed clinically.</description><identifier>ISSN: 0021-9533</identifier><identifier>EISSN: 1477-9137</identifier><identifier>DOI: 10.1242/jcs.259783</identifier><identifier>PMID: 35946425</identifier><language>eng</language><publisher>England: The Company of Biologists Ltd</publisher><subject>Cell Biology and Disease ; Extracellular Matrix - metabolism ; MicroRNAs - genetics ; MicroRNAs - metabolism ; Mitral Valve ; Short Report ; Tricuspid Valve - abnormalities</subject><ispartof>Journal of cell science, 2022-09, Vol.135 (17)</ispartof><rights>2022. Published by The Company of Biologists Ltd.</rights><rights>2022. Published by The Company of Biologists Ltd 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c378t-ef8dcb70ca20bc4baa905040743cb7e45ef29833fa42ea877b14df476fca91d63</citedby><cites>FETCH-LOGICAL-c378t-ef8dcb70ca20bc4baa905040743cb7e45ef29833fa42ea877b14df476fca91d63</cites><orcidid>0000-0002-5415-9020</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,3665,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35946425$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yan, Shun</creatorcontrib><creatorcontrib>Peng, Yin</creatorcontrib><creatorcontrib>Lu, Jin</creatorcontrib><creatorcontrib>Shakil, Saima</creatorcontrib><creatorcontrib>Shi, Yang</creatorcontrib><creatorcontrib>Crossman, David K</creatorcontrib><creatorcontrib>Johnson, Walter H</creatorcontrib><creatorcontrib>Liu, Shanrun</creatorcontrib><creatorcontrib>Rokosh, Donald G</creatorcontrib><creatorcontrib>Lincoln, Joy</creatorcontrib><creatorcontrib>Wang, Qin</creatorcontrib><creatorcontrib>Jiao, Kai</creatorcontrib><title>Differential requirement for DICER1 activity during the development of mitral and tricuspid valves</title><title>Journal of cell science</title><addtitle>J Cell Sci</addtitle><description>Mitral and tricuspid valves are essential for unidirectional blood flow in the heart. They are derived from similar cell sources, and yet congenital dysplasia affecting both valves is clinically rare, suggesting the presence of differential regulatory mechanisms underlying their development. Here, we specifically inactivated Dicer1 in the endocardium during cardiogenesis and found that Dicer1 deletion caused congenital mitral valve stenosis and regurgitation, whereas it had no impact on other valves. We showed that hyperplastic mitral valves were caused by abnormal condensation and extracellular matrix (ECM) remodeling. Our single-cell RNA sequencing analysis revealed impaired maturation of mesenchymal cells and abnormal expression of ECM genes in mutant mitral valves. Furthermore, expression of a set of miRNAs that target ECM genes was significantly lower in tricuspid valves compared to mitral valves, consistent with the idea that the miRNAs are differentially required for mitral and tricuspid valve development. We thus reveal miRNA-mediated gene regulation as a novel molecular mechanism that differentially regulates mitral and tricuspid valve development, thereby enhancing our understanding of the non-association of inborn mitral and tricuspid dysplasia observed clinically.</description><subject>Cell Biology and Disease</subject><subject>Extracellular Matrix - metabolism</subject><subject>MicroRNAs - genetics</subject><subject>MicroRNAs - metabolism</subject><subject>Mitral Valve</subject><subject>Short Report</subject><subject>Tricuspid Valve - abnormalities</subject><issn>0021-9533</issn><issn>1477-9137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkctKAzEUhoMotl42PoBkKcJobtNMNoK09QKCILoOmcyJpsylJjMDfXujVdFVODkf3_nhR-iEkgvKBLtc2XjBciULvoOmVEiZKcrlLpoSwmimcs4n6CDGFSFEMiX30YTnSswEy6eoXHjnIEDbe1PjAO-DD9CkEbsu4MX9fPlEsbG9H32_wdUQfPuK-zfAFYxQd-svtHO48X1IAtNWuA_eDnHtKzyaeoR4hPacqSMcf7-H6OVm-Ty_yx4eb-_n1w-Z5bLoM3BFZUtJrGGktKI0RpGcCCIFT98gcnBMFZw7IxiYQsqSisoJOXPWKFrN-CG62nrXQ9lAZVOyFEmvg29M2OjOeP1_0_o3_dqNWomCcSGS4OxbELr3AWKvGx8t1LVpoRuiZpKQGS-oZAk936I2dDEGcL9nKNGfpehUit6WkuDTv8F-0Z8W-Ad7OYrV</recordid><startdate>20220901</startdate><enddate>20220901</enddate><creator>Yan, Shun</creator><creator>Peng, Yin</creator><creator>Lu, Jin</creator><creator>Shakil, Saima</creator><creator>Shi, Yang</creator><creator>Crossman, David K</creator><creator>Johnson, Walter H</creator><creator>Liu, Shanrun</creator><creator>Rokosh, Donald G</creator><creator>Lincoln, Joy</creator><creator>Wang, Qin</creator><creator>Jiao, Kai</creator><general>The Company of Biologists 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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5415-9020</orcidid></search><sort><creationdate>20220901</creationdate><title>Differential requirement for DICER1 activity during the development of mitral and tricuspid valves</title><author>Yan, Shun ; Peng, Yin ; Lu, Jin ; Shakil, Saima ; Shi, Yang ; Crossman, David K ; Johnson, Walter H ; Liu, Shanrun ; Rokosh, Donald G ; Lincoln, Joy ; Wang, Qin ; Jiao, Kai</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c378t-ef8dcb70ca20bc4baa905040743cb7e45ef29833fa42ea877b14df476fca91d63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Cell Biology and Disease</topic><topic>Extracellular Matrix - metabolism</topic><topic>MicroRNAs - genetics</topic><topic>MicroRNAs - metabolism</topic><topic>Mitral Valve</topic><topic>Short Report</topic><topic>Tricuspid Valve - abnormalities</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yan, Shun</creatorcontrib><creatorcontrib>Peng, Yin</creatorcontrib><creatorcontrib>Lu, Jin</creatorcontrib><creatorcontrib>Shakil, Saima</creatorcontrib><creatorcontrib>Shi, Yang</creatorcontrib><creatorcontrib>Crossman, David K</creatorcontrib><creatorcontrib>Johnson, Walter H</creatorcontrib><creatorcontrib>Liu, Shanrun</creatorcontrib><creatorcontrib>Rokosh, Donald G</creatorcontrib><creatorcontrib>Lincoln, Joy</creatorcontrib><creatorcontrib>Wang, Qin</creatorcontrib><creatorcontrib>Jiao, Kai</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of cell science</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yan, Shun</au><au>Peng, Yin</au><au>Lu, Jin</au><au>Shakil, Saima</au><au>Shi, Yang</au><au>Crossman, David K</au><au>Johnson, Walter H</au><au>Liu, Shanrun</au><au>Rokosh, Donald G</au><au>Lincoln, Joy</au><au>Wang, Qin</au><au>Jiao, Kai</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential requirement for DICER1 activity during the development of mitral and tricuspid valves</atitle><jtitle>Journal of cell science</jtitle><addtitle>J Cell Sci</addtitle><date>2022-09-01</date><risdate>2022</risdate><volume>135</volume><issue>17</issue><issn>0021-9533</issn><eissn>1477-9137</eissn><abstract>Mitral and tricuspid valves are essential for unidirectional blood flow in the heart. They are derived from similar cell sources, and yet congenital dysplasia affecting both valves is clinically rare, suggesting the presence of differential regulatory mechanisms underlying their development. Here, we specifically inactivated Dicer1 in the endocardium during cardiogenesis and found that Dicer1 deletion caused congenital mitral valve stenosis and regurgitation, whereas it had no impact on other valves. We showed that hyperplastic mitral valves were caused by abnormal condensation and extracellular matrix (ECM) remodeling. Our single-cell RNA sequencing analysis revealed impaired maturation of mesenchymal cells and abnormal expression of ECM genes in mutant mitral valves. Furthermore, expression of a set of miRNAs that target ECM genes was significantly lower in tricuspid valves compared to mitral valves, consistent with the idea that the miRNAs are differentially required for mitral and tricuspid valve development. We thus reveal miRNA-mediated gene regulation as a novel molecular mechanism that differentially regulates mitral and tricuspid valve development, thereby enhancing our understanding of the non-association of inborn mitral and tricuspid dysplasia observed clinically.</abstract><cop>England</cop><pub>The Company of Biologists Ltd</pub><pmid>35946425</pmid><doi>10.1242/jcs.259783</doi><orcidid>https://orcid.org/0000-0002-5415-9020</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0021-9533 |
ispartof | Journal of cell science, 2022-09, Vol.135 (17) |
issn | 0021-9533 1477-9137 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9482344 |
source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection; Company of Biologists |
subjects | Cell Biology and Disease Extracellular Matrix - metabolism MicroRNAs - genetics MicroRNAs - metabolism Mitral Valve Short Report Tricuspid Valve - abnormalities |
title | Differential requirement for DICER1 activity during the development of mitral and tricuspid valves |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-03T16%3A13%3A01IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Differential%20requirement%20for%20DICER1%20activity%20during%20the%20development%20of%20mitral%20and%20tricuspid%20valves&rft.jtitle=Journal%20of%20cell%20science&rft.au=Yan,%20Shun&rft.date=2022-09-01&rft.volume=135&rft.issue=17&rft.issn=0021-9533&rft.eissn=1477-9137&rft_id=info:doi/10.1242/jcs.259783&rft_dat=%3Cproquest_pubme%3E2700638172%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2700638172&rft_id=info:pmid/35946425&rfr_iscdi=true |