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<title xml:lang="en">Lymphatic abnormalities are associated with
<italic>RASA1</italic>
gene mutations in mouse and man</title>
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<affiliation>
<nlm:aff id="aff1">Department of Diagnostic and Interventional Imaging,
<institution>University of Texas Health Science Center at Houston</institution>
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<addr-line>TX</addr-line>
77030;</nlm:aff>
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<author>
<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>
<affiliation>
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<institution>University of Texas Health Science Center at Houston</institution>
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<addr-line>TX</addr-line>
77030;</nlm:aff>
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<affiliation>
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<institution>University of Texas Health Science Center at Houston</institution>
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<addr-line>TX</addr-line>
77030;</nlm:aff>
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77030</nlm:aff>
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<name sortKey="Kwon, Sunkuk" sort="Kwon, Sunkuk" uniqKey="Kwon S" first="Sunkuk" last="Kwon">Sunkuk Kwon</name>
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<addr-line>TX</addr-line>
77030;</nlm:aff>
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<affiliation>
<nlm:aff id="aff5">Department of Microbiology and Immunology,
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48109</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="King, Philip D" sort="King, Philip D" uniqKey="King P" first="Philip D." last="King">Philip D. King</name>
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<nlm:aff id="aff5">Department of Microbiology and Immunology,
<institution>University of Michigan Medical School</institution>
, Ann Arbor,
<addr-line>MI</addr-line>
48109</nlm:aff>
</affiliation>
</author>
<author>
<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>
<affiliation>
<nlm:aff id="aff3">Center for Molecular Imaging, The Brown Foundation Institute of Molecular Medicine,
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<addr-line>TX</addr-line>
77030;</nlm:aff>
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<title xml:lang="en" level="a" type="main">Lymphatic abnormalities are associated with
<italic>RASA1</italic>
gene mutations in mouse and man</title>
<author>
<name sortKey="Burrows, Patricia E" sort="Burrows, Patricia E" uniqKey="Burrows P" first="Patricia E." last="Burrows">Patricia E. Burrows</name>
<affiliation>
<nlm:aff id="aff1">Department of Diagnostic and Interventional Imaging,
<institution>University of Texas Health Science Center at Houston</institution>
, Houston,
<addr-line>TX</addr-line>
77030;</nlm:aff>
</affiliation>
</author>
<author>
<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>
<affiliation>
<nlm:aff id="aff2">Division of Genomics and Bioinformatics,
<institution>University of Texas Health Science Center at Houston</institution>
, Houston,
<addr-line>TX</addr-line>
77030;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff3">Center for Molecular Imaging, The Brown Foundation Institute of Molecular Medicine,
<institution>University of Texas Health Science Center at Houston</institution>
, Houston,
<addr-line>TX</addr-line>
77030;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Rasmussen, John C" sort="Rasmussen, John C" uniqKey="Rasmussen J" first="John C." last="Rasmussen">John C. Rasmussen</name>
<affiliation>
<nlm:aff id="aff3">Center for Molecular Imaging, The Brown Foundation Institute of Molecular Medicine,
<institution>University of Texas Health Science Center at Houston</institution>
, Houston,
<addr-line>TX</addr-line>
77030;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Aldrich, Melissa B" sort="Aldrich, Melissa B" uniqKey="Aldrich M" first="Melissa B." last="Aldrich">Melissa B. Aldrich</name>
<affiliation>
<nlm:aff id="aff3">Center for Molecular Imaging, The Brown Foundation Institute of Molecular Medicine,
<institution>University of Texas Health Science Center at Houston</institution>
, Houston,
<addr-line>TX</addr-line>
77030;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Guilliod, Renie" sort="Guilliod, Renie" uniqKey="Guilliod R" first="Renie" last="Guilliod">Renie Guilliod</name>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff4">
<institution>Center for Lymphedema Management</institution>
, Memorial Hermann Hospital, Houston,
<addr-line>TX</addr-line>
77030</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Maus, Erik A" sort="Maus, Erik A" uniqKey="Maus E" first="Erik A." last="Maus">Erik A. Maus</name>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff4">
<institution>Center for Lymphedema Management</institution>
, Memorial Hermann Hospital, Houston,
<addr-line>TX</addr-line>
77030</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Fife, Caroline E" sort="Fife, Caroline E" uniqKey="Fife C" first="Caroline E." last="Fife">Caroline E. Fife</name>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff4">
<institution>Center for Lymphedema Management</institution>
, Memorial Hermann Hospital, Houston,
<addr-line>TX</addr-line>
77030</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Kwon, Sunkuk" sort="Kwon, Sunkuk" uniqKey="Kwon S" first="Sunkuk" last="Kwon">Sunkuk Kwon</name>
<affiliation>
<nlm:aff id="aff3">Center for Molecular Imaging, The Brown Foundation Institute of Molecular Medicine,
<institution>University of Texas Health Science Center at Houston</institution>
, Houston,
<addr-line>TX</addr-line>
77030;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Lapinski, Philip E" sort="Lapinski, Philip E" uniqKey="Lapinski P" first="Philip E." last="Lapinski">Philip E. Lapinski</name>
<affiliation>
<nlm:aff id="aff5">Department of Microbiology and Immunology,
<institution>University of Michigan Medical School</institution>
, Ann Arbor,
<addr-line>MI</addr-line>
48109</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="King, Philip D" sort="King, Philip D" uniqKey="King P" first="Philip D." last="King">Philip D. King</name>
<affiliation>
<nlm:aff id="aff5">Department of Microbiology and Immunology,
<institution>University of Michigan Medical School</institution>
, Ann Arbor,
<addr-line>MI</addr-line>
48109</nlm:aff>
</affiliation>
</author>
<author>
<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>
<affiliation>
<nlm:aff id="aff3">Center for Molecular Imaging, The Brown Foundation Institute of Molecular Medicine,
<institution>University of Texas Health Science Center at Houston</institution>
, Houston,
<addr-line>TX</addr-line>
77030;</nlm:aff>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="ISSN">0027-8424</idno>
<idno type="eISSN">1091-6490</idno>
<imprint>
<date when="2013">2013</date>
</imprint>
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<front>
<div type="abstract" xml:lang="en">
<p>Mutations in gene
<italic>RASA1</italic>
have been historically associated with capillary malformation–arteriovenous malformation, but sporadic reports of lymphatic involvement have yet to be investigated in detail. To investigate the impact of
<italic>RASA1</italic>
mutations in the lymphatic system, we performed investigational near-infrared fluorescence lymphatic imaging and confirmatory radiographic lymphangiography in a Parkes–Weber syndrome (PKWS) patient with suspected
<italic>RASA1</italic>
mutations and correlated the lymphatic abnormalities against that imaged in an inducible Rasa1 knockout mouse. Whole-exome sequencing (WES) analysis and validation by Sanger sequencing of DNA from the patient and unaffected biological parents enabled us to identify an early-frameshift deletion in
<italic>RASA1</italic>
that was shared with the father, who possessed a capillary stain but otherwise no overt disease phenotype. Abnormal lymphatic vasculature was imaged in both affected and unaffected legs of the PKWS subject that transported injected indocyanine green dye to the inguinal lymph node and drained atypically into the abdomen and into dermal lymphocele-like vesicles on the groin. Dermal lymphatic hyperplasia and dilated vessels were observed in Rasa1-deficient mice, with subsequent development of chylous ascites. WES analyses did not identify potential gene modifiers that could explain the variability of penetrance between father and son. Nonetheless, we conclude that the
<italic>RASA1</italic>
mutation is responsible for the aberrant lymphatic architecture and functional abnormalities, as visualized in the PKWS subject and in the animal model. Our unique method to combine investigatory near-infrared fluorescence lymphatic imaging and WES for accurate phenoptyping and unbiased genotyping allows the study of molecular mechanisms of lymphatic involvement of hemovascular disorders.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article">
<pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
<journal-id journal-id-type="pmc">pnas</journal-id>
<journal-id journal-id-type="publisher-id">PNAS</journal-id>
<journal-title-group>
<journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title>
</journal-title-group>
<issn pub-type="ppub">0027-8424</issn>
<issn pub-type="epub">1091-6490</issn>
<publisher>
<publisher-name>National Academy of Sciences</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">23650393</article-id>
<article-id pub-id-type="pmc">3666675</article-id>
<article-id pub-id-type="publisher-id">201222722</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1222722110</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Biological Sciences</subject>
<subj-group>
<subject>Genetics</subject>
</subj-group>
</subj-group>
<subj-group subj-group-type="heading">
<subject>Physical Sciences</subject>
<subj-group>
<subject>Engineering</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Lymphatic abnormalities are associated with
<italic>RASA1</italic>
gene mutations in mouse and man</article-title>
<alt-title alt-title-type="short">Phenotyping RASA1 with NIRF lymphatic imaging</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Burrows</surname>
<given-names>Patricia E.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn2">
<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="aff2">
<sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Rasmussen</surname>
<given-names>John C.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">
<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="aff3">
<sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Guilliod</surname>
<given-names>Renie</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>d</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>d</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>d</sup>
</xref>
<xref ref-type="author-notes" rid="fn3">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kwon</surname>
<given-names>Sunkuk</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lapinski</surname>
<given-names>Philip E.</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>e</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>e</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sevick-Muraca</surname>
<given-names>Eva M.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>4</sup>
</xref>
</contrib>
<aff id="aff1">
<sup>a</sup>
Department of Diagnostic and Interventional Imaging,
<institution>University of Texas Health Science Center at Houston</institution>
, Houston,
<addr-line>TX</addr-line>
77030;</aff>
<aff id="aff2">
<sup>b</sup>
Division of Genomics and Bioinformatics,
<institution>University of Texas Health Science Center at Houston</institution>
, Houston,
<addr-line>TX</addr-line>
77030;</aff>
<aff id="aff3">
<sup>c</sup>
Center for Molecular Imaging, The Brown Foundation Institute of Molecular Medicine,
<institution>University of Texas Health Science Center at Houston</institution>
, Houston,
<addr-line>TX</addr-line>
77030;</aff>
<aff id="aff4">
<sup>d</sup>
<institution>Center for Lymphedema Management</institution>
, Memorial Hermann Hospital, Houston,
<addr-line>TX</addr-line>
77030; and</aff>
<aff id="aff5">
<sup>e</sup>
Department of Microbiology and Immunology,
<institution>University of Michigan Medical School</institution>
, Ann Arbor,
<addr-line>MI</addr-line>
48109</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<sup>4</sup>
To whom correspondence should be addressed. E-mail:
<email>Eva.Sevick@uth.tmc.edu</email>
.</corresp>
<fn fn-type="edited-by">
<p>Edited by Rakesh K. Jain, Harvard Medical School and Massachusetts General Hospital, Boston, MA, and approved April 8, 2013 (received for review December 28, 2012)</p>
</fn>
<fn fn-type="con">
<p>Author contributions: P.E.B., M.L.G.-G., J.C.R., and E.M.S.-M. designed research; P.E.B., M.L.G.-G., J.C.R., M.B.A., R.G., E.A.M., C.E.F., S.K., and P.E.L. performed research; P.E.L. and P.D.K. contributed new reagents/analytic tools; M.L.G.-G., J.C.R., M.B.A., and S.K. analyzed data; and P.E.B., M.L.G.-G., J.C.R., P.D.K., and E.M.S.-M. wrote the paper.</p>
</fn>
<fn fn-type="equal" id="fn1">
<p>
<sup>1</sup>
P.E.B., M.L.G.-G., and J.C.R. contributed equally to this work.</p>
</fn>
<fn fn-type="present-address" id="fn2">
<p>
<sup>2</sup>
Present address: Division of Vascular Interventional Radiology, Medical College of Wisconsin, Children’s Hospital of Wisconsin, Milwaukee, WI 53226.</p>
</fn>
<fn fn-type="present-address" id="fn3">
<p>
<sup>3</sup>
Present address: St. Luke's Wound Clinic, The Woodlands, Texas, 77381.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<day>21</day>
<month>5</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="epub">
<day>6</day>
<month>5</month>
<year>2013</year>
</pub-date>
<volume>110</volume>
<issue>21</issue>
<fpage>8621</fpage>
<lpage>8626</lpage>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201222722.pdf"></self-uri>
<abstract>
<p>Mutations in gene
<italic>RASA1</italic>
have been historically associated with capillary malformation–arteriovenous malformation, but sporadic reports of lymphatic involvement have yet to be investigated in detail. To investigate the impact of
<italic>RASA1</italic>
mutations in the lymphatic system, we performed investigational near-infrared fluorescence lymphatic imaging and confirmatory radiographic lymphangiography in a Parkes–Weber syndrome (PKWS) patient with suspected
<italic>RASA1</italic>
mutations and correlated the lymphatic abnormalities against that imaged in an inducible Rasa1 knockout mouse. Whole-exome sequencing (WES) analysis and validation by Sanger sequencing of DNA from the patient and unaffected biological parents enabled us to identify an early-frameshift deletion in
<italic>RASA1</italic>
that was shared with the father, who possessed a capillary stain but otherwise no overt disease phenotype. Abnormal lymphatic vasculature was imaged in both affected and unaffected legs of the PKWS subject that transported injected indocyanine green dye to the inguinal lymph node and drained atypically into the abdomen and into dermal lymphocele-like vesicles on the groin. Dermal lymphatic hyperplasia and dilated vessels were observed in Rasa1-deficient mice, with subsequent development of chylous ascites. WES analyses did not identify potential gene modifiers that could explain the variability of penetrance between father and son. Nonetheless, we conclude that the
<italic>RASA1</italic>
mutation is responsible for the aberrant lymphatic architecture and functional abnormalities, as visualized in the PKWS subject and in the animal model. Our unique method to combine investigatory near-infrared fluorescence lymphatic imaging and WES for accurate phenoptyping and unbiased genotyping allows the study of molecular mechanisms of lymphatic involvement of hemovascular disorders.</p>
</abstract>
<kwd-group>
<kwd>CM-AVM</kwd>
<kwd>lymphatics</kwd>
<kwd>near-infrared fluorescence imaging</kwd>
<kwd>indocyanine green imaging</kwd>
</kwd-group>
<counts>
<page-count count="6"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>

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