Evidence for SH2 Domain-Containing 5′-Inositol Phosphatase-2 (SHIP2) Contributing to a Lymphatic Dysfunction
Identifieur interne : 001B75 ( Pmc/Checkpoint ); précédent : 001B74; suivant : 001B76Evidence for SH2 Domain-Containing 5′-Inositol Phosphatase-2 (SHIP2) Contributing to a Lymphatic Dysfunction
Auteurs : Germaine D. Agollah [États-Unis] ; Manuel L. Gonzalez-Garay [États-Unis] ; John C. Rasmussen [États-Unis] ; I-Chih Tan [États-Unis] ; Melissa B. Aldrich [États-Unis] ; Chinmay Darne [États-Unis] ; Caroline E. Fife [États-Unis] ; Renie Guilliod [États-Unis] ; Erik A. Maus [États-Unis] ; Philip D. King [États-Unis] ; Eva M. Sevick-Muraca [États-Unis]Source :
- PLoS ONE [ 1932-6203 ] ; 2014.
Abstract
The lymphatic vasculature plays a critical role in a number of disease conditions of increasing prevalence, such as autoimmune disorders, obesity, blood vascular diseases, and cancer metastases. Yet, unlike the blood vasculature, the tools available to interrogate the molecular basis of lymphatic dysfunction/disease have been lacking. More recently, investigators have reported that dysregulation of the PI3K pathway is involved in syndromic human diseases that involve abnormal lymphatic vasculatures, but there have been few compelling results that show the direct association of this molecular pathway with lymphatic dysfunction in humans. Using near-infrared fluorescence lymphatic imaging (NIRFLI) to phenotype and next generation sequencing (NGS) for unbiased genetic discovery in a family with non-syndromic lymphatic disease, we discovered a rare, novel mutation in
Url:
DOI: 10.1371/journal.pone.0112548
PubMed: 25383712
PubMed Central: 4226566
Affiliations:
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<front><div type="abstract" xml:lang="en"><p>The lymphatic vasculature plays a critical role in a number of disease conditions of increasing prevalence, such as autoimmune disorders, obesity, blood vascular diseases, and cancer metastases. Yet, unlike the blood vasculature, the tools available to interrogate the molecular basis of lymphatic dysfunction/disease have been lacking. More recently, investigators have reported that dysregulation of the PI3K pathway is involved in syndromic human diseases that involve abnormal lymphatic vasculatures, but there have been few compelling results that show the direct association of this molecular pathway with lymphatic dysfunction in humans. Using near-infrared fluorescence lymphatic imaging (NIRFLI) to phenotype and next generation sequencing (NGS) for unbiased genetic discovery in a family with non-syndromic lymphatic disease, we discovered a rare, novel mutation in <italic>INPPL1</italic>
that encodes the protein SHIP2, which is a negative regulator of the PI3K pathway, to be associated with lymphatic dysfunction in the family. <italic>In vitro</italic>
interrogation shows that SHIP2 is directly associated with impairment of normal lymphatic endothelial cell (LEC) behavior and that SHIP2 associates with receptors that are associated in lymphedema, implicating its direct involvement in the lymphatic vasculature.</p>
</div>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25383712</article-id>
<article-id pub-id-type="pmc">4226566</article-id>
<article-id pub-id-type="publisher-id">PONE-D-14-34053</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0112548</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Cell Biology</subject>
</subj-group>
<subj-group><subject>Genetics</subject>
<subj-group><subject>Genetics of Disease</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Vascular Medicine</subject>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Research and Analysis Methods</subject>
<subj-group><subject>Imaging Techniques</subject>
<subj-group><subject>Fluorescence Imaging</subject>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Evidence for SH2 Domain-Containing 5′-Inositol Phosphatase-2 (SHIP2) Contributing to a Lymphatic Dysfunction</article-title>
<alt-title alt-title-type="running-head">SHIP2 Contributes to Lymphatic Dysfunction</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Agollah</surname>
<given-names>Germaine D.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gonzalez-Garay</surname>
<given-names>Manuel L.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rasmussen</surname>
<given-names>John C.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Tan</surname>
<given-names>I-Chih</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Aldrich</surname>
<given-names>Melissa B.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Darne</surname>
<given-names>Chinmay</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fife</surname>
<given-names>Caroline E.</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Guilliod</surname>
<given-names>Renie</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Maus</surname>
<given-names>Erik A.</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>King</surname>
<given-names>Philip D.</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sevick-Muraca</surname>
<given-names>Eva M.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Center for Molecular Imaging, The Brown Foundation Institute of Molecular Medicine, The University of Texas Health Science Center, Houston, Texas, United States of America</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>The University of Texas Graduate School of Biomedical Sciences at Houston, The University of Texas MD Anderson Cancer Center, Houston, Texas, United States of America</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Division of Genomics and Bioinformatics, Center for Molecular Imaging, The Brown Foundation Institute of Molecular Medicine, Houston, Texas, United States of America</addr-line>
</aff>
<aff id="aff4"><label>4</label>
<addr-line>Memorial Hermann Hospital Center for Lymphedema Management, Houston, Texas, United States of America</addr-line>
</aff>
<aff id="aff5"><label>5</label>
<addr-line>Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, Michigan, United States of America</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Fritz</surname>
<given-names>Jörg Hermann</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>McGill University, Canada</addr-line>
</aff>
<author-notes><corresp id="cor1">* E-mail: <email>Eva.Sevick@uth.tmc.edu</email>
</corresp>
<fn fn-type="conflict"><p><bold>Competing Interests: </bold>
JCR, ICT, MBA, CEF and EMS-M are inventors of near-infrared fluorescence lymphatic imaging and could receive financial benefit associated with the commercialization of the imaging technology. EMS-M is a stockholder of NIRF Imaging, Inc. which is commercializing the technology of near-infrared fluorescence imaging. JCR has received consulting fees from NIRF Imaging, Inc. This does not alter the authors' adherence to PLOS ONE policies on sharing data and materials. There are patents that are directly or indirectly associated with the technology described herein. These patent interests do not alter the authors' adherence to PLOS ONE policies on sharing data and materials. There are no other disclosures to make.</p>
</fn>
<fn fn-type="con"><p>Conceived and designed the experiments: GDA PDK EMS-M. Performed the experiments: GDA. Analyzed the data: GDA JCR MLG-G. Contributed reagents/materials/analysis tools: JCR MLG-G. Wrote the paper: GDA PDK EMS-M. Conducted clinical lymphatic imaging: JCR ICT MBA CD GDA. Conducted clinical investigations: CEF RG EAM. Analyzed the clinical imaging data: JCR. Analyzed genetics and bioinformatics data: MLG-G. Performed Sanger validation: GDA.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2014</year>
</pub-date>
<pub-date pub-type="epub"><day>10</day>
<month>11</month>
<year>2014</year>
</pub-date>
<volume>9</volume>
<issue>11</issue>
<elocation-id>e112548</elocation-id>
<history><date date-type="received"><day>29</day>
<month>7</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>7</day>
<month>10</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-year>2014</copyright-year>
<copyright-holder>Agollah et al</copyright-holder>
<license><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<abstract><p>The lymphatic vasculature plays a critical role in a number of disease conditions of increasing prevalence, such as autoimmune disorders, obesity, blood vascular diseases, and cancer metastases. Yet, unlike the blood vasculature, the tools available to interrogate the molecular basis of lymphatic dysfunction/disease have been lacking. More recently, investigators have reported that dysregulation of the PI3K pathway is involved in syndromic human diseases that involve abnormal lymphatic vasculatures, but there have been few compelling results that show the direct association of this molecular pathway with lymphatic dysfunction in humans. Using near-infrared fluorescence lymphatic imaging (NIRFLI) to phenotype and next generation sequencing (NGS) for unbiased genetic discovery in a family with non-syndromic lymphatic disease, we discovered a rare, novel mutation in <italic>INPPL1</italic>
that encodes the protein SHIP2, which is a negative regulator of the PI3K pathway, to be associated with lymphatic dysfunction in the family. <italic>In vitro</italic>
interrogation shows that SHIP2 is directly associated with impairment of normal lymphatic endothelial cell (LEC) behavior and that SHIP2 associates with receptors that are associated in lymphedema, implicating its direct involvement in the lymphatic vasculature.</p>
</abstract>
<funding-group><funding-statement>This work was supported in parts by the National Institutes of Health (NIH) grants R01 HL092923, R01 CA128919, U54 CA136404 and The Texas Star Award (EMS-M) and R01 HL096498 (PDK). GDA acknowledges support from The Schissler Foundation Fellowship for Translational Studies of Common Human Diseases. Flow cytometry measurements were supported in part through a Cancer Prevention and Research Institute of Texas (CPRIT) instrumentation grant (RP110776). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><page-count count="18"></page-count>
</counts>
<custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name>
<meta-value>The authors confirm that all data underlying the findings are fully available without restriction. Ethical restrictions prevent public deposition of data. An anonymized data set will be made available through the GWAS database upon requests. Requests may be made to Dr. Eva M. Sevick-Muraca (<email>Eva.Sevick@uth.tmc.edu</email>
).</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes><title>Data Availability</title>
<p>The authors confirm that all data underlying the findings are fully available without restriction. Ethical restrictions prevent public deposition of data. An anonymized data set will be made available through the GWAS database upon requests. Requests may be made to Dr. Eva M. Sevick-Muraca (<email>Eva.Sevick@uth.tmc.edu</email>
).</p>
</notes>
</front>
</pmc>
<affiliations><list><country><li>États-Unis</li>
</country>
<region><li>Michigan</li>
<li>Texas</li>
</region>
</list>
<tree><country name="États-Unis"><region name="Texas"><name sortKey="Agollah, Germaine D" sort="Agollah, Germaine D" uniqKey="Agollah G" first="Germaine D." last="Agollah">Germaine D. Agollah</name>
</region>
<name sortKey="Agollah, Germaine D" sort="Agollah, Germaine D" uniqKey="Agollah G" first="Germaine D." last="Agollah">Germaine D. Agollah</name>
<name sortKey="Aldrich, Melissa B" sort="Aldrich, Melissa B" uniqKey="Aldrich M" first="Melissa B." last="Aldrich">Melissa B. Aldrich</name>
<name sortKey="Darne, Chinmay" sort="Darne, Chinmay" uniqKey="Darne C" first="Chinmay" last="Darne">Chinmay Darne</name>
<name sortKey="Fife, Caroline E" sort="Fife, Caroline E" uniqKey="Fife C" first="Caroline E." last="Fife">Caroline E. Fife</name>
<name sortKey="Gonzalez Garay, Manuel L" sort="Gonzalez Garay, Manuel L" uniqKey="Gonzalez Garay M" first="Manuel L." last="Gonzalez-Garay">Manuel L. Gonzalez-Garay</name>
<name sortKey="Guilliod, Renie" sort="Guilliod, Renie" uniqKey="Guilliod R" first="Renie" last="Guilliod">Renie Guilliod</name>
<name sortKey="King, Philip D" sort="King, Philip D" uniqKey="King P" first="Philip D." last="King">Philip D. King</name>
<name sortKey="Maus, Erik A" sort="Maus, Erik A" uniqKey="Maus E" first="Erik A." last="Maus">Erik A. Maus</name>
<name sortKey="Rasmussen, John C" sort="Rasmussen, John C" uniqKey="Rasmussen J" first="John C." last="Rasmussen">John C. Rasmussen</name>
<name sortKey="Sevick Muraca, Eva M" sort="Sevick Muraca, Eva M" uniqKey="Sevick Muraca E" first="Eva M." last="Sevick-Muraca">Eva M. Sevick-Muraca</name>
<name sortKey="Tan, I Chih" sort="Tan, I Chih" uniqKey="Tan I" first="I-Chih" last="Tan">I-Chih Tan</name>
</country>
</tree>
</affiliations>
</record>
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