Vimentin intermediate filament assembly regulates fibroblast invasion in fibrogenic lung injury
Identifieur interne : 000518 ( Ncbi/Merge ); précédent : 000517; suivant : 000519Vimentin intermediate filament assembly regulates fibroblast invasion in fibrogenic lung injury
Auteurs : Ranu Surolia ; Fu Jun Li ; Zheng Wang ; Huashi Li ; Kevin Dsouza ; Vinoy Thomas ; Sergey Mirov [États-Unis] ; Dolores Pérez-Sala [Espagne] ; Mohammad Athar [États-Unis] ; Victor J. Thannickal ; Veena B. AntonySource :
- JCI Insight [ 2379-3708 ] ; ????.
Abstract
Idiopathic pulmonary fibrosis (IPF) is a progressive disease, with a median survival of 3–5 years following diagnosis. Lung remodeling by invasive fibroblasts is a hallmark of IPF. In this study, we demonstrate that inhibition of vimentin intermediate filaments (VimIFs) decreases the invasiveness of IPF fibroblasts and confers protection against fibrosis in a murine model of experimental lung injury. Increased expression and organization of VimIFs contribute to the invasive property of IPF fibroblasts in connection with deficient cellular autophagy. Blocking VimIF assembly by pharmacologic and genetic means also increases autophagic clearance of collagen type I. Furthermore, inhibition of expression of collagen type I by siRNA decreased invasiveness of fibroblasts. In a bleomycin injury model, enhancing autophagy in fibroblasts by an inhibitor of VimIF assembly, withaferin A (WFA), protected from fibrotic lung injury. Additionally, in 3D lung organoids, or pulmospheres, from patients with IPF, WFA reduced the invasiveness of lung fibroblasts in the majority of subjects tested. These studies provide insights into the functional role of vimentin, which regulates autophagy and restricts the invasiveness of lung fibroblasts.
Url:
DOI: 10.1172/jci.insight.123253
PubMed: 30944258
PubMed Central: 6483650
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PMC:6483650Le document en format XML
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<front><div type="abstract" xml:lang="en"><p>Idiopathic pulmonary fibrosis (IPF) is a progressive disease, with a median survival of 3–5 years following diagnosis. Lung remodeling by invasive fibroblasts is a hallmark of IPF. In this study, we demonstrate that inhibition of vimentin intermediate filaments (VimIFs) decreases the invasiveness of IPF fibroblasts and confers protection against fibrosis in a murine model of experimental lung injury. Increased expression and organization of VimIFs contribute to the invasive property of IPF fibroblasts in connection with deficient cellular autophagy. Blocking VimIF assembly by pharmacologic and genetic means also increases autophagic clearance of collagen type I. Furthermore, inhibition of expression of collagen type I by siRNA decreased invasiveness of fibroblasts. In a bleomycin injury model, enhancing autophagy in fibroblasts by an inhibitor of VimIF assembly, withaferin A (WFA), protected from fibrotic lung injury. Additionally, in 3D lung organoids, or pulmospheres, from patients with IPF, WFA reduced the invasiveness of lung fibroblasts in the majority of subjects tested. These studies provide insights into the functional role of vimentin, which regulates autophagy and restricts the invasiveness of lung fibroblasts.</p>
</div>
</front>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">JCI Insight</journal-id>
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<article-id pub-id-type="doi">10.1172/jci.insight.123253</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
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<title-group><article-title>Vimentin intermediate filament assembly regulates fibroblast invasion in fibrogenic lung injury</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Surolia</surname>
<given-names>Ranu</given-names>
</name>
<email>ranusurolia@uabmc.edu</email>
<xref ref-type="aff" rid="A1">1</xref>
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<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Fu Jun</given-names>
</name>
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</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Zheng</given-names>
</name>
<email>Zhengwang@uabmc.edu</email>
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</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Huashi</given-names>
</name>
<email>huashili@uabmc.edu</email>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dsouza</surname>
<given-names>Kevin</given-names>
</name>
<email>kdsouza@uabmc.edu</email>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Thomas</surname>
<given-names>Vinoy</given-names>
</name>
<email>vthomas@uab.edu</email>
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<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0002-4186-8450</contrib-id>
<name><surname>Mirov</surname>
<given-names>Sergey</given-names>
</name>
<email>mirov@uab.edu</email>
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</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0003-0600-665X</contrib-id>
<name><surname>Pérez-Sala</surname>
<given-names>Dolores</given-names>
</name>
<email>dperezsala@cib.csic.es</email>
<xref ref-type="aff" rid="A4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Athar</surname>
<given-names>Mohammad</given-names>
</name>
<email>mathar@uab.edu</email>
<xref ref-type="aff" rid="A5">5</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0003-4266-8677</contrib-id>
<name><surname>Thannickal</surname>
<given-names>Victor J.</given-names>
</name>
<email>vjthan@uab.edu</email>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Antony</surname>
<given-names>Veena B.</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
</contrib-group>
<aff id="A1"><label>1</label>
Division of Pulmonary, Allergy, and Critical Care Medicine, Department of Medicine,</aff>
<aff id="A2"><label>2</label>
Department of Materials Science and Engineering, and</aff>
<aff id="A3"><label>3</label>
Department of Physics, University of Alabama at Birmingham (UAB), Birmingham, Alabama, USA.</aff>
<aff id="A4"><label>4</label>
Department of Structural and Chemical and Biology, Centro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain.</aff>
<aff id="A5"><label>5</label>
Department of Dermatology, UAB, Birmingham, Alabama, USA.</aff>
<author-notes><corresp>Address correspondence to: Veena B. Antony, 1530 3rd Avenue South, THT-541, Birmingham, Alabama 35294, USA. Phone: 205.975.3255; Email: <email>vantony@uabmc.edu</email>
.</corresp>
<fn fn-type="COI-statement"><p><bold>Conflict of interest:</bold>
The authors have declared no conflict of interest.</p>
</fn>
</author-notes>
<pub-date date-type="pub" publication-format="electronic" iso-8601-date="2019-04-04T09:00:00-0400"><day>4</day>
<month>4</month>
<year>2019</year>
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<volume>4</volume>
<issue>7</issue>
<elocation-id>e123253</elocation-id>
<history><date date-type="received"><day>16</day>
<month>7</month>
<year>2018</year>
</date>
<date date-type="accepted"><day>26</day>
<month>2</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© 2019 American Society for Clinical Investigation</copyright-statement>
<copyright-year>2019</copyright-year>
<copyright-holder>American Society for Clinical Investigation</copyright-holder>
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<self-uri xlink:href="https://insight.jci.org/articles/view/123253">This article is available online at https://insight.jci.org/articles/view/123253</self-uri>
<abstract><p>Idiopathic pulmonary fibrosis (IPF) is a progressive disease, with a median survival of 3–5 years following diagnosis. Lung remodeling by invasive fibroblasts is a hallmark of IPF. In this study, we demonstrate that inhibition of vimentin intermediate filaments (VimIFs) decreases the invasiveness of IPF fibroblasts and confers protection against fibrosis in a murine model of experimental lung injury. Increased expression and organization of VimIFs contribute to the invasive property of IPF fibroblasts in connection with deficient cellular autophagy. Blocking VimIF assembly by pharmacologic and genetic means also increases autophagic clearance of collagen type I. Furthermore, inhibition of expression of collagen type I by siRNA decreased invasiveness of fibroblasts. In a bleomycin injury model, enhancing autophagy in fibroblasts by an inhibitor of VimIF assembly, withaferin A (WFA), protected from fibrotic lung injury. Additionally, in 3D lung organoids, or pulmospheres, from patients with IPF, WFA reduced the invasiveness of lung fibroblasts in the majority of subjects tested. These studies provide insights into the functional role of vimentin, which regulates autophagy and restricts the invasiveness of lung fibroblasts.</p>
</abstract>
<abstract abstract-type="toc"><p>Vimentin regulates fibroblast invasion, extracellular matrix formation, and autophagy in idiopathic pulmonary fibrosis, and inhibiting vimentin-intermediate filament assembly may be an attractive therapeutic approach.</p>
</abstract>
<kwd-group kwd-group-type="specialties"><kwd>Pulmonology</kwd>
</kwd-group>
<kwd-group kwd-group-type="keywords"><kwd>Autophagy</kwd>
<kwd>Drug therapy</kwd>
<kwd>Fibrosis</kwd>
</kwd-group>
<funding-group><award-group><funding-source>NIH grant</funding-source>
<award-id>P01 HL114470</award-id>
</award-group>
</funding-group>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Espagne</li>
<li>États-Unis</li>
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<name sortKey="Li, Fu Jun" sort="Li, Fu Jun" uniqKey="Li F" first="Fu Jun" last="Li">Fu Jun Li</name>
<name sortKey="Li, Huashi" sort="Li, Huashi" uniqKey="Li H" first="Huashi" last="Li">Huashi Li</name>
<name sortKey="Surolia, Ranu" sort="Surolia, Ranu" uniqKey="Surolia R" first="Ranu" last="Surolia">Ranu Surolia</name>
<name sortKey="Thannickal, Victor J" sort="Thannickal, Victor J" uniqKey="Thannickal V" first="Victor J." last="Thannickal">Victor J. Thannickal</name>
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<name sortKey="Wang, Zheng" sort="Wang, Zheng" uniqKey="Wang Z" first="Zheng" last="Wang">Zheng Wang</name>
</noCountry>
<country name="États-Unis"><region name="Alabama"><name sortKey="Mirov, Sergey" sort="Mirov, Sergey" uniqKey="Mirov S" first="Sergey" last="Mirov">Sergey Mirov</name>
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<name sortKey="Athar, Mohammad" sort="Athar, Mohammad" uniqKey="Athar M" first="Mohammad" last="Athar">Mohammad Athar</name>
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<country name="Espagne"><region name="Communauté de Madrid"><name sortKey="Perez Sala, Dolores" sort="Perez Sala, Dolores" uniqKey="Perez Sala D" first="Dolores" last="Pérez-Sala">Dolores Pérez-Sala</name>
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