Maternal smoke exposure decreases mesenchymal proliferation and modulates Rho‐GTPase‐dependent actin cytoskeletal signaling in fetal lungs
ABSTRACT The present study tested the hypothesis that maternal smoke exposure results in fetal lung growth retardation due to dysregulation in various signaling pathways, including the Wnt (wingless‐related integration site)/β‐catenin pathway. Pregnant female C57BL/6J mice were exposed to cigarette...
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The present study tested the hypothesis that maternal smoke exposure results in fetal lung growth retardation due to dysregulation in various signaling pathways, including the Wnt (wingless‐related integration site)/β‐catenin pathway. Pregnant female C57BL/6J mice were exposed to cigarette smoke (100–150 mg/m3) or room air, and offspring were humanely killed on 12.5, 14.5, 16.5, and 18.5 d post coitum (dpc). We assessed lung stereology with Cavalieri estimation; apoptosis with proliferating cell nuclear antigen, TUNEL, and caspase assays; and gene expression with quantitative PCR (qPCR) and RNA sequencing on lung epithelium and mesenchyme retrieved by laser capture microdissection. Results demonstrated a significant decrease in body weight and lung volume of smoke‐exposed embryos. At 16.5 dpc, the reduction in lung volume was due to loss of lung mesenchymal tissue correlating with a decrease in cell proliferation (n = 10; air: 61.65% vs. smoke: 44.21%, P < 0.05). RNA sequence analysis demonstrated an alteration in the Wnt pathway, and qPCR confirmed an increased expression of secreted frizzled‐related protein 1 (sFRP‐1) [n = 12; relative quantification (RQ) 1 vs. 2.33, P < 0.05] and down‐regulation of Cyclin D1 (n = 7; RQ 1 vs. 0.61, P < 0.05) in mesenchymal tissue. Furthermore, genome expression studies revealed a smoke‐induced up‐regulation of Rho‐GTPase‐dependent actin cytoskeletal signaling that can lead to loss of tissue integrity.—Unachukwu, U., Trischler, J., Goldklang, M., Xiao, R., D'Armiento, J. Maternal smoke exposure decreases mesenchymal proliferation and modulates Rho‐GTPase‐dependent actin cytoskeletal signaling in fetal lungs. FASEB J. 31, 2340–2351 (2017). www.fasebj.org |
| doi_str_mv | 10.1096/fj.201601063R |
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The present study tested the hypothesis that maternal smoke exposure results in fetal lung growth retardation due to dysregulation in various signaling pathways, including the Wnt (wingless‐related integration site)/β‐catenin pathway. Pregnant female C57BL/6J mice were exposed to cigarette smoke (100–150 mg/m3) or room air, and offspring were humanely killed on 12.5, 14.5, 16.5, and 18.5 d post coitum (dpc). We assessed lung stereology with Cavalieri estimation; apoptosis with proliferating cell nuclear antigen, TUNEL, and caspase assays; and gene expression with quantitative PCR (qPCR) and RNA sequencing on lung epithelium and mesenchyme retrieved by laser capture microdissection. Results demonstrated a significant decrease in body weight and lung volume of smoke‐exposed embryos. At 16.5 dpc, the reduction in lung volume was due to loss of lung mesenchymal tissue correlating with a decrease in cell proliferation (n = 10; air: 61.65% vs. smoke: 44.21%, P < 0.05). RNA sequence analysis demonstrated an alteration in the Wnt pathway, and qPCR confirmed an increased expression of secreted frizzled‐related protein 1 (sFRP‐1) [n = 12; relative quantification (RQ) 1 vs. 2.33, P < 0.05] and down‐regulation of Cyclin D1 (n = 7; RQ 1 vs. 0.61, P < 0.05) in mesenchymal tissue. Furthermore, genome expression studies revealed a smoke‐induced up‐regulation of Rho‐GTPase‐dependent actin cytoskeletal signaling that can lead to loss of tissue integrity.—Unachukwu, U., Trischler, J., Goldklang, M., Xiao, R., D'Armiento, J. Maternal smoke exposure decreases mesenchymal proliferation and modulates Rho‐GTPase‐dependent actin cytoskeletal signaling in fetal lungs. FASEB J. 31, 2340–2351 (2017). www.fasebj.org</description><identifier>ISSN: 0892-6638</identifier><identifier>EISSN: 1530-6860</identifier><identifier>DOI: 10.1096/fj.201601063R</identifier><identifier>PMID: 28209772</identifier><language>eng</language><publisher>United States: Federation of American Societies for Experimental Biology (FASEB)</publisher><subject>Actin ; Actins - physiology ; Animals ; Apoptosis ; Body weight ; Caspase ; Cell proliferation ; Cell Proliferation - drug effects ; Cigarette smoke ; Cyclin D1 ; Cytoskeleton ; Embryos ; Epithelium ; Exposure ; Female ; Fetus - drug effects ; Fetuses ; Frizzled protein ; Frizzled-related protein ; Frizzled-related protein 1 ; Gene expression ; Gene Expression Regulation, Developmental - drug effects ; Gene sequencing ; Gene therapy ; Genomes ; Growth rate ; GTPase-Activating Proteins - genetics ; GTPase-Activating Proteins - metabolism ; Guanine nucleotide-binding protein ; Guanosine triphosphatases ; in utero ; Lung - drug effects ; Lung - embryology ; Lung - metabolism ; Lungs ; Mesenchymal Stromal Cells - drug effects ; Mesenchymal Stromal Cells - physiology ; Mesenchyme ; Mice ; Nucleotide sequence ; Offspring ; Pregnancy ; proliferation ; Ribonucleic acid ; RNA ; Signal transduction ; Signal Transduction - drug effects ; Signal Transduction - physiology ; Signaling ; Smoke ; Smoke - adverse effects ; Stereology ; Tobacco Products ; Wnt Proteins - genetics ; Wnt Proteins - metabolism ; Wnt/β‐catenin</subject><ispartof>The FASEB journal, 2017-06, Vol.31 (6), p.2340-2351</ispartof><rights>FASEB</rights><rights>FASEB.</rights><rights>Copyright Federation of American Societies for Experimental Biology (FASEB) Jun 2017</rights><rights>FASEB 2017 FASEB</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c500R-703267e1a50ac06decb602c2aa9d3eb1004bca3f676cb150e9d3259a27d424a83</citedby><cites>FETCH-LOGICAL-c500R-703267e1a50ac06decb602c2aa9d3eb1004bca3f676cb150e9d3259a27d424a83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1096%2Ffj.201601063R$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1096%2Ffj.201601063R$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1416,27922,27923,45572,45573</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28209772$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Unachukwu, Uchenna</creatorcontrib><creatorcontrib>Trischler, Jordis</creatorcontrib><creatorcontrib>Goldklang, Monica</creatorcontrib><creatorcontrib>Xiao, Rui</creatorcontrib><creatorcontrib>D'Armiento, Jeanine</creatorcontrib><title>Maternal smoke exposure decreases mesenchymal proliferation and modulates Rho‐GTPase‐dependent actin cytoskeletal signaling in fetal lungs</title><title>The FASEB journal</title><addtitle>FASEB J</addtitle><description>ABSTRACT
The present study tested the hypothesis that maternal smoke exposure results in fetal lung growth retardation due to dysregulation in various signaling pathways, including the Wnt (wingless‐related integration site)/β‐catenin pathway. Pregnant female C57BL/6J mice were exposed to cigarette smoke (100–150 mg/m3) or room air, and offspring were humanely killed on 12.5, 14.5, 16.5, and 18.5 d post coitum (dpc). We assessed lung stereology with Cavalieri estimation; apoptosis with proliferating cell nuclear antigen, TUNEL, and caspase assays; and gene expression with quantitative PCR (qPCR) and RNA sequencing on lung epithelium and mesenchyme retrieved by laser capture microdissection. Results demonstrated a significant decrease in body weight and lung volume of smoke‐exposed embryos. At 16.5 dpc, the reduction in lung volume was due to loss of lung mesenchymal tissue correlating with a decrease in cell proliferation (n = 10; air: 61.65% vs. smoke: 44.21%, P < 0.05). RNA sequence analysis demonstrated an alteration in the Wnt pathway, and qPCR confirmed an increased expression of secreted frizzled‐related protein 1 (sFRP‐1) [n = 12; relative quantification (RQ) 1 vs. 2.33, P < 0.05] and down‐regulation of Cyclin D1 (n = 7; RQ 1 vs. 0.61, P < 0.05) in mesenchymal tissue. Furthermore, genome expression studies revealed a smoke‐induced up‐regulation of Rho‐GTPase‐dependent actin cytoskeletal signaling that can lead to loss of tissue integrity.—Unachukwu, U., Trischler, J., Goldklang, M., Xiao, R., D'Armiento, J. Maternal smoke exposure decreases mesenchymal proliferation and modulates Rho‐GTPase‐dependent actin cytoskeletal signaling in fetal lungs. FASEB J. 31, 2340–2351 (2017). www.fasebj.org</description><subject>Actin</subject><subject>Actins - physiology</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Body weight</subject><subject>Caspase</subject><subject>Cell proliferation</subject><subject>Cell Proliferation - drug effects</subject><subject>Cigarette smoke</subject><subject>Cyclin D1</subject><subject>Cytoskeleton</subject><subject>Embryos</subject><subject>Epithelium</subject><subject>Exposure</subject><subject>Female</subject><subject>Fetus - drug effects</subject><subject>Fetuses</subject><subject>Frizzled protein</subject><subject>Frizzled-related protein</subject><subject>Frizzled-related protein 1</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Developmental - drug effects</subject><subject>Gene sequencing</subject><subject>Gene therapy</subject><subject>Genomes</subject><subject>Growth rate</subject><subject>GTPase-Activating Proteins - genetics</subject><subject>GTPase-Activating Proteins - metabolism</subject><subject>Guanine nucleotide-binding protein</subject><subject>Guanosine triphosphatases</subject><subject>in utero</subject><subject>Lung - drug effects</subject><subject>Lung - embryology</subject><subject>Lung - metabolism</subject><subject>Lungs</subject><subject>Mesenchymal Stromal Cells - drug effects</subject><subject>Mesenchymal Stromal Cells - physiology</subject><subject>Mesenchyme</subject><subject>Mice</subject><subject>Nucleotide sequence</subject><subject>Offspring</subject><subject>Pregnancy</subject><subject>proliferation</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Signal transduction</subject><subject>Signal Transduction - drug effects</subject><subject>Signal Transduction - physiology</subject><subject>Signaling</subject><subject>Smoke</subject><subject>Smoke - adverse effects</subject><subject>Stereology</subject><subject>Tobacco Products</subject><subject>Wnt Proteins - genetics</subject><subject>Wnt Proteins - metabolism</subject><subject>Wnt/β‐catenin</subject><issn>0892-6638</issn><issn>1530-6860</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNksFu1DAQQCMEokvhyBVZ4sIlZWwnTiwkpFKxBVQEWsrZ8jqT3WwdO9gJsDe-APGNfAletpTCAXGyNfP8ZmxPlt2ncERBisft5ogBFUBB8MWNbEZLDrmoBdzMZlBLlgvB64PsTowbgERRcTs7YDUDWVVsln19rUcMTlsSe3-BBD8PPk4BSYMmoI4YSY8RnVlv-wQNwduuxaDHzjuiXUN630w2OSJZrP33L99Oz9-mU2nT4ICuQTcSbcbOEbMdfbxAi-OuWLdKNTu3IinT_gzZya3i3exWq23Ee5frYfZ-_vz85EV-9ub05cnxWW5KgEVeAWeiQqpL0AZE6nUpgBmmtWw4LilAsTSat6ISZklLwBRmpdSsagpW6JofZk_33mFa9tiY1GbQVg2h63XYKq879WfGdWu18h-VoDI9e5kEjy4FwX-YMI6q76JBa7VDP0WVMCpoXdD_QGshpeAF8IQ-_Avd-Gn3OzthzSWThaCJyveUCT7GgO1V3xTUbihUu1G_hyLxD65f9or-NQUJeLIHPnUWt_-2qfm7Z2z-6pr-B-J7ySE</recordid><startdate>201706</startdate><enddate>201706</enddate><creator>Unachukwu, Uchenna</creator><creator>Trischler, Jordis</creator><creator>Goldklang, Monica</creator><creator>Xiao, Rui</creator><creator>D'Armiento, Jeanine</creator><general>Federation of American Societies for Experimental Biology (FASEB)</general><general>Federation of American Societies for Experimental Biology</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>7QO</scope><scope>7QP</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U7</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>201706</creationdate><title>Maternal smoke exposure decreases mesenchymal proliferation and modulates Rho‐GTPase‐dependent actin cytoskeletal signaling in fetal lungs</title><author>Unachukwu, Uchenna ; Trischler, Jordis ; Goldklang, Monica ; Xiao, Rui ; D'Armiento, Jeanine</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c500R-703267e1a50ac06decb602c2aa9d3eb1004bca3f676cb150e9d3259a27d424a83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Actin</topic><topic>Actins - physiology</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>Body weight</topic><topic>Caspase</topic><topic>Cell proliferation</topic><topic>Cell Proliferation - drug effects</topic><topic>Cigarette smoke</topic><topic>Cyclin D1</topic><topic>Cytoskeleton</topic><topic>Embryos</topic><topic>Epithelium</topic><topic>Exposure</topic><topic>Female</topic><topic>Fetus - drug effects</topic><topic>Fetuses</topic><topic>Frizzled protein</topic><topic>Frizzled-related protein</topic><topic>Frizzled-related protein 1</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Developmental - drug effects</topic><topic>Gene sequencing</topic><topic>Gene therapy</topic><topic>Genomes</topic><topic>Growth rate</topic><topic>GTPase-Activating Proteins - genetics</topic><topic>GTPase-Activating Proteins - metabolism</topic><topic>Guanine nucleotide-binding protein</topic><topic>Guanosine triphosphatases</topic><topic>in utero</topic><topic>Lung - drug effects</topic><topic>Lung - embryology</topic><topic>Lung - metabolism</topic><topic>Lungs</topic><topic>Mesenchymal Stromal Cells - drug effects</topic><topic>Mesenchymal Stromal Cells - physiology</topic><topic>Mesenchyme</topic><topic>Mice</topic><topic>Nucleotide sequence</topic><topic>Offspring</topic><topic>Pregnancy</topic><topic>proliferation</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Signal transduction</topic><topic>Signal Transduction - drug effects</topic><topic>Signal Transduction - physiology</topic><topic>Signaling</topic><topic>Smoke</topic><topic>Smoke - adverse effects</topic><topic>Stereology</topic><topic>Tobacco Products</topic><topic>Wnt Proteins - genetics</topic><topic>Wnt Proteins - metabolism</topic><topic>Wnt/β‐catenin</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Unachukwu, Uchenna</creatorcontrib><creatorcontrib>Trischler, Jordis</creatorcontrib><creatorcontrib>Goldklang, Monica</creatorcontrib><creatorcontrib>Xiao, Rui</creatorcontrib><creatorcontrib>D'Armiento, Jeanine</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>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Toxicology 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>The FASEB journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Unachukwu, Uchenna</au><au>Trischler, Jordis</au><au>Goldklang, Monica</au><au>Xiao, Rui</au><au>D'Armiento, Jeanine</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Maternal smoke exposure decreases mesenchymal proliferation and modulates Rho‐GTPase‐dependent actin cytoskeletal signaling in fetal lungs</atitle><jtitle>The FASEB journal</jtitle><addtitle>FASEB J</addtitle><date>2017-06</date><risdate>2017</risdate><volume>31</volume><issue>6</issue><spage>2340</spage><epage>2351</epage><pages>2340-2351</pages><issn>0892-6638</issn><eissn>1530-6860</eissn><abstract>ABSTRACT
The present study tested the hypothesis that maternal smoke exposure results in fetal lung growth retardation due to dysregulation in various signaling pathways, including the Wnt (wingless‐related integration site)/β‐catenin pathway. Pregnant female C57BL/6J mice were exposed to cigarette smoke (100–150 mg/m3) or room air, and offspring were humanely killed on 12.5, 14.5, 16.5, and 18.5 d post coitum (dpc). We assessed lung stereology with Cavalieri estimation; apoptosis with proliferating cell nuclear antigen, TUNEL, and caspase assays; and gene expression with quantitative PCR (qPCR) and RNA sequencing on lung epithelium and mesenchyme retrieved by laser capture microdissection. Results demonstrated a significant decrease in body weight and lung volume of smoke‐exposed embryos. At 16.5 dpc, the reduction in lung volume was due to loss of lung mesenchymal tissue correlating with a decrease in cell proliferation (n = 10; air: 61.65% vs. smoke: 44.21%, P < 0.05). RNA sequence analysis demonstrated an alteration in the Wnt pathway, and qPCR confirmed an increased expression of secreted frizzled‐related protein 1 (sFRP‐1) [n = 12; relative quantification (RQ) 1 vs. 2.33, P < 0.05] and down‐regulation of Cyclin D1 (n = 7; RQ 1 vs. 0.61, P < 0.05) in mesenchymal tissue. Furthermore, genome expression studies revealed a smoke‐induced up‐regulation of Rho‐GTPase‐dependent actin cytoskeletal signaling that can lead to loss of tissue integrity.—Unachukwu, U., Trischler, J., Goldklang, M., Xiao, R., D'Armiento, J. Maternal smoke exposure decreases mesenchymal proliferation and modulates Rho‐GTPase‐dependent actin cytoskeletal signaling in fetal lungs. FASEB J. 31, 2340–2351 (2017). www.fasebj.org</abstract><cop>United States</cop><pub>Federation of American Societies for Experimental Biology (FASEB)</pub><pmid>28209772</pmid><doi>10.1096/fj.201601063R</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Actin Actins - physiology Animals Apoptosis Body weight Caspase Cell proliferation Cell Proliferation - drug effects Cigarette smoke Cyclin D1 Cytoskeleton Embryos Epithelium Exposure Female Fetus - drug effects Fetuses Frizzled protein Frizzled-related protein Frizzled-related protein 1 Gene expression Gene Expression Regulation, Developmental - drug effects Gene sequencing Gene therapy Genomes Growth rate GTPase-Activating Proteins - genetics GTPase-Activating Proteins - metabolism Guanine nucleotide-binding protein Guanosine triphosphatases in utero Lung - drug effects Lung - embryology Lung - metabolism Lungs Mesenchymal Stromal Cells - drug effects Mesenchymal Stromal Cells - physiology Mesenchyme Mice Nucleotide sequence Offspring Pregnancy proliferation Ribonucleic acid RNA Signal transduction Signal Transduction - drug effects Signal Transduction - physiology Signaling Smoke Smoke - adverse effects Stereology Tobacco Products Wnt Proteins - genetics Wnt Proteins - metabolism Wnt/β‐catenin |
| title | Maternal smoke exposure decreases mesenchymal proliferation and modulates Rho‐GTPase‐dependent actin cytoskeletal signaling in fetal lungs |
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