Renal tubular NEDD4-2 deficiency causes NCC-mediated salt-dependent hypertension
Identifieur interne : 001923 ( Pmc/Corpus ); précédent : 001922; suivant : 001924Renal tubular NEDD4-2 deficiency causes NCC-mediated salt-dependent hypertension
Auteurs : Caroline Ronzaud ; Dominique Loffing-Cueni ; Pierrette Hausel ; Anne Debonneville ; Sumedha Ram Malsure ; Nicole Fowler-Jaeger ; Natasha A. Boase ; Romain Perrier ; Marc Maillard ; Baoli Yang ; John B. Stokes ; Robert Koesters ; Sharad Kumar ; Edith Hummler ; Johannes Loffing ; Olivier StaubSource :
- The Journal of Clinical Investigation [ 0021-9738 ] ; 2013.
Abstract
The E3 ubiquitin ligase NEDD4-2 (encoded by the
Url:
DOI: 10.1172/JCI61110
PubMed: 23348737
PubMed Central: 3561795
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PMC:3561795Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Renal tubular NEDD4-2 deficiency causes NCC-mediated salt-dependent hypertension</title>
<author><name sortKey="Ronzaud, Caroline" sort="Ronzaud, Caroline" uniqKey="Ronzaud C" first="Caroline" last="Ronzaud">Caroline Ronzaud</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
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<author><name sortKey="Loffing Cueni, Dominique" sort="Loffing Cueni, Dominique" uniqKey="Loffing Cueni D" first="Dominique" last="Loffing-Cueni">Dominique Loffing-Cueni</name>
<affiliation><nlm:aff id="JCI61110">Institute of Anatomy, University of Zurich, Zurich, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Hausel, Pierrette" sort="Hausel, Pierrette" uniqKey="Hausel P" first="Pierrette" last="Hausel">Pierrette Hausel</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Debonneville, Anne" sort="Debonneville, Anne" uniqKey="Debonneville A" first="Anne" last="Debonneville">Anne Debonneville</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Malsure, Sumedha Ram" sort="Malsure, Sumedha Ram" uniqKey="Malsure S" first="Sumedha Ram" last="Malsure">Sumedha Ram Malsure</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Fowler Jaeger, Nicole" sort="Fowler Jaeger, Nicole" uniqKey="Fowler Jaeger N" first="Nicole" last="Fowler-Jaeger">Nicole Fowler-Jaeger</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Boase, Natasha A" sort="Boase, Natasha A" uniqKey="Boase N" first="Natasha A." last="Boase">Natasha A. Boase</name>
<affiliation><nlm:aff id="JCI61110">Department of Hematology, Centre for Cancer Biology, Adelaide, Australia.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Perrier, Romain" sort="Perrier, Romain" uniqKey="Perrier R" first="Romain" last="Perrier">Romain Perrier</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Maillard, Marc" sort="Maillard, Marc" uniqKey="Maillard M" first="Marc" last="Maillard">Marc Maillard</name>
<affiliation><nlm:aff id="JCI61110">Nephrology Department, Centre Hospitalier Universitaire Vaudois (CHUV), Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Yang, Baoli" sort="Yang, Baoli" uniqKey="Yang B" first="Baoli" last="Yang">Baoli Yang</name>
<affiliation><nlm:aff id="JCI61110">Department of Obstetrics and Gynecology, University of Iowa, Iowa City, Iowa, USA.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Stokes, John B" sort="Stokes, John B" uniqKey="Stokes J" first="John B." last="Stokes">John B. Stokes</name>
<affiliation><nlm:aff id="JCI61110">Department of Internal Medicine, University of Iowa, and VA Medical Center, Iowa City, Iowa, USA.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Koesters, Robert" sort="Koesters, Robert" uniqKey="Koesters R" first="Robert" last="Koesters">Robert Koesters</name>
<affiliation><nlm:aff id="JCI61110">INSERM UMRS 702, UPMC, Tenon Hospital, Paris, France.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Kumar, Sharad" sort="Kumar, Sharad" uniqKey="Kumar S" first="Sharad" last="Kumar">Sharad Kumar</name>
<affiliation><nlm:aff id="JCI61110">Department of Hematology, Centre for Cancer Biology, Adelaide, Australia.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Hummler, Edith" sort="Hummler, Edith" uniqKey="Hummler E" first="Edith" last="Hummler">Edith Hummler</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Loffing, Johannes" sort="Loffing, Johannes" uniqKey="Loffing J" first="Johannes" last="Loffing">Johannes Loffing</name>
<affiliation><nlm:aff id="JCI61110">Institute of Anatomy, University of Zurich, Zurich, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Staub, Olivier" sort="Staub, Olivier" uniqKey="Staub O" first="Olivier" last="Staub">Olivier Staub</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Renal tubular NEDD4-2 deficiency causes NCC-mediated salt-dependent hypertension</title>
<author><name sortKey="Ronzaud, Caroline" sort="Ronzaud, Caroline" uniqKey="Ronzaud C" first="Caroline" last="Ronzaud">Caroline Ronzaud</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Loffing Cueni, Dominique" sort="Loffing Cueni, Dominique" uniqKey="Loffing Cueni D" first="Dominique" last="Loffing-Cueni">Dominique Loffing-Cueni</name>
<affiliation><nlm:aff id="JCI61110">Institute of Anatomy, University of Zurich, Zurich, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Hausel, Pierrette" sort="Hausel, Pierrette" uniqKey="Hausel P" first="Pierrette" last="Hausel">Pierrette Hausel</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Debonneville, Anne" sort="Debonneville, Anne" uniqKey="Debonneville A" first="Anne" last="Debonneville">Anne Debonneville</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Malsure, Sumedha Ram" sort="Malsure, Sumedha Ram" uniqKey="Malsure S" first="Sumedha Ram" last="Malsure">Sumedha Ram Malsure</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Fowler Jaeger, Nicole" sort="Fowler Jaeger, Nicole" uniqKey="Fowler Jaeger N" first="Nicole" last="Fowler-Jaeger">Nicole Fowler-Jaeger</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Boase, Natasha A" sort="Boase, Natasha A" uniqKey="Boase N" first="Natasha A." last="Boase">Natasha A. Boase</name>
<affiliation><nlm:aff id="JCI61110">Department of Hematology, Centre for Cancer Biology, Adelaide, Australia.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Perrier, Romain" sort="Perrier, Romain" uniqKey="Perrier R" first="Romain" last="Perrier">Romain Perrier</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Maillard, Marc" sort="Maillard, Marc" uniqKey="Maillard M" first="Marc" last="Maillard">Marc Maillard</name>
<affiliation><nlm:aff id="JCI61110">Nephrology Department, Centre Hospitalier Universitaire Vaudois (CHUV), Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Yang, Baoli" sort="Yang, Baoli" uniqKey="Yang B" first="Baoli" last="Yang">Baoli Yang</name>
<affiliation><nlm:aff id="JCI61110">Department of Obstetrics and Gynecology, University of Iowa, Iowa City, Iowa, USA.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Stokes, John B" sort="Stokes, John B" uniqKey="Stokes J" first="John B." last="Stokes">John B. Stokes</name>
<affiliation><nlm:aff id="JCI61110">Department of Internal Medicine, University of Iowa, and VA Medical Center, Iowa City, Iowa, USA.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Koesters, Robert" sort="Koesters, Robert" uniqKey="Koesters R" first="Robert" last="Koesters">Robert Koesters</name>
<affiliation><nlm:aff id="JCI61110">INSERM UMRS 702, UPMC, Tenon Hospital, Paris, France.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Kumar, Sharad" sort="Kumar, Sharad" uniqKey="Kumar S" first="Sharad" last="Kumar">Sharad Kumar</name>
<affiliation><nlm:aff id="JCI61110">Department of Hematology, Centre for Cancer Biology, Adelaide, Australia.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Hummler, Edith" sort="Hummler, Edith" uniqKey="Hummler E" first="Edith" last="Hummler">Edith Hummler</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Loffing, Johannes" sort="Loffing, Johannes" uniqKey="Loffing J" first="Johannes" last="Loffing">Johannes Loffing</name>
<affiliation><nlm:aff id="JCI61110">Institute of Anatomy, University of Zurich, Zurich, Switzerland.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Staub, Olivier" sort="Staub, Olivier" uniqKey="Staub O" first="Olivier" last="Staub">Olivier Staub</name>
<affiliation><nlm:aff id="JCI61110">Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">The Journal of Clinical Investigation</title>
<idno type="ISSN">0021-9738</idno>
<idno type="eISSN">1558-8238</idno>
<imprint><date when="2013">2013</date>
</imprint>
</series>
</biblStruct>
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<front><div type="abstract" xml:lang="en"><p>The E3 ubiquitin ligase NEDD4-2 (encoded by the <italic>Nedd4L</italic>
gene) regulates the amiloride-sensitive epithelial Na<sup>+</sup>
channel (ENaC/SCNN1) to mediate Na<sup>+</sup>
homeostasis. Mutations in the human β/γENaC subunits that block NEDD4-2 binding or constitutive ablation of exons 6–8 of <italic>Nedd4L</italic>
in mice both result in salt-sensitive hypertension and elevated ENaC activity (Liddle syndrome). To determine the role of renal tubular NEDD4-2 in adult mice, we generated tetracycline-inducible, nephron-specific <italic>Nedd4L</italic>
KO mice. Under standard and high-Na<sup>+</sup>
diets, conditional KO mice displayed decreased plasma aldosterone but normal Na<sup>+</sup>
/K<sup>+</sup>
balance. Under a high-Na<sup>+</sup>
diet, KO mice exhibited hypercalciuria and increased blood pressure, which were reversed by thiazide treatment. Protein expression of βENaC, γENaC, the renal outer medullary K<sup>+</sup>
channel (ROMK), and total and phosphorylated thiazide-sensitive Na<sup>+</sup>
Cl<sup>–</sup>
cotransporter (NCC) levels were increased in KO kidneys. Unexpectedly, <italic>Scnn1a</italic>
mRNA, which encodes the αENaC subunit, was reduced and proteolytic cleavage of αENaC decreased. Taken together, these results demonstrate that loss of NEDD4-2 in adult renal tubules causes a new form of mild, salt-sensitive hypertension without hyperkalemia that is characterized by upregulation of NCC, elevation of β/γENaC, but not αENaC, and a normal Na<sup>+</sup>
/K<sup>+</sup>
balance maintained by downregulation of ENaC activity and upregulation of ROMK.
</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">J Clin Invest</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Clin. Invest</journal-id>
<journal-id journal-id-type="publisher-id">J CLIN INVEST</journal-id>
<journal-title-group><journal-title>The Journal of Clinical Investigation</journal-title>
</journal-title-group>
<issn pub-type="ppub">0021-9738</issn>
<issn pub-type="epub">1558-8238</issn>
<publisher><publisher-name>American Society for Clinical Investigation</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">23348737</article-id>
<article-id pub-id-type="pmc">3561795</article-id>
<article-id pub-id-type="publisher-id">61110</article-id>
<article-id pub-id-type="doi">10.1172/JCI61110</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Renal tubular NEDD4-2 deficiency causes NCC-mediated salt-dependent hypertension</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Ronzaud</surname>
<given-names>Caroline</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Loffing-Cueni</surname>
<given-names>Dominique</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hausel</surname>
<given-names>Pierrette</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Debonneville</surname>
<given-names>Anne</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Malsure</surname>
<given-names>Sumedha Ram</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fowler-Jaeger</surname>
<given-names>Nicole</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Boase</surname>
<given-names>Natasha A.</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Perrier</surname>
<given-names>Romain</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Maillard</surname>
<given-names>Marc</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yang</surname>
<given-names>Baoli</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Stokes</surname>
<given-names>John B.</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Koesters</surname>
<given-names>Robert</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kumar</surname>
<given-names>Sharad</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hummler</surname>
<given-names>Edith</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Loffing</surname>
<given-names>Johannes</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Staub</surname>
<given-names>Olivier</given-names>
</name>
<xref ref-type="aff" rid="JCI61110">1</xref>
</contrib>
</contrib-group>
<aff id="JCI61110"><label>1</label>
Department of Pharmacology and Toxicology, University of Lausanne, Lausanne, Switzerland.<label>2</label>
Institute of Anatomy, University of Zurich, Zurich, Switzerland.<label>3</label>
Department of Hematology, Centre for Cancer Biology, Adelaide, Australia.<label>4</label>
Nephrology Department, Centre Hospitalier Universitaire Vaudois (CHUV), Lausanne, Switzerland.<label>5</label>
Department of Obstetrics and Gynecology, University of Iowa, Iowa City, Iowa, USA.<label>6</label>
Department of Internal Medicine, University of Iowa, and VA Medical Center, Iowa City, Iowa, USA.<label>7</label>
INSERM UMRS 702, UPMC, Tenon Hospital, Paris, France.</aff>
<author-notes><corresp>Address correspondence to: Oliver Staub, Department of Pharmacology and Toxicology, University of Lausanne, Rue du Bugnon 27, 1005 Lausanne, Switzerland. Phone: 41.21.692.5407; Fax: 41.21.692.5355; E-mail:
<email>olivier.staub@unil.ch</email>
. Or to: Johannes Loffing, Institute of Anatomy, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland. Phone: 41.44.635.5320; Fax: 41.44.635.5702; E-mail:
<email>johannes.loffing@anatom.uzh.ch</email>
.
</corresp>
<fn><p><bold>Authorship note:</bold>
Johannes Loffing and Olivier Staub contributed equally to this work. John B. Stokes is deceased.
</p>
</fn>
</author-notes>
<pub-date pub-type="epub"><day>25</day>
<month>1</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="ppub"><day>1</day>
<month>2</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>25</day>
<month>1</month>
<year>2013</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
. </pmc-comment>
<volume>123</volume>
<issue>2</issue>
<fpage>657</fpage>
<lpage>665</lpage>
<history><date date-type="received"><day>13</day>
<month>8</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>16</day>
<month>11</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2013, American Society for Clinical Investigation</copyright-statement>
<copyright-year>2013</copyright-year>
</permissions>
<abstract><p>The E3 ubiquitin ligase NEDD4-2 (encoded by the <italic>Nedd4L</italic>
gene) regulates the amiloride-sensitive epithelial Na<sup>+</sup>
channel (ENaC/SCNN1) to mediate Na<sup>+</sup>
homeostasis. Mutations in the human β/γENaC subunits that block NEDD4-2 binding or constitutive ablation of exons 6–8 of <italic>Nedd4L</italic>
in mice both result in salt-sensitive hypertension and elevated ENaC activity (Liddle syndrome). To determine the role of renal tubular NEDD4-2 in adult mice, we generated tetracycline-inducible, nephron-specific <italic>Nedd4L</italic>
KO mice. Under standard and high-Na<sup>+</sup>
diets, conditional KO mice displayed decreased plasma aldosterone but normal Na<sup>+</sup>
/K<sup>+</sup>
balance. Under a high-Na<sup>+</sup>
diet, KO mice exhibited hypercalciuria and increased blood pressure, which were reversed by thiazide treatment. Protein expression of βENaC, γENaC, the renal outer medullary K<sup>+</sup>
channel (ROMK), and total and phosphorylated thiazide-sensitive Na<sup>+</sup>
Cl<sup>–</sup>
cotransporter (NCC) levels were increased in KO kidneys. Unexpectedly, <italic>Scnn1a</italic>
mRNA, which encodes the αENaC subunit, was reduced and proteolytic cleavage of αENaC decreased. Taken together, these results demonstrate that loss of NEDD4-2 in adult renal tubules causes a new form of mild, salt-sensitive hypertension without hyperkalemia that is characterized by upregulation of NCC, elevation of β/γENaC, but not αENaC, and a normal Na<sup>+</sup>
/K<sup>+</sup>
balance maintained by downregulation of ENaC activity and upregulation of ROMK.
</p>
</abstract>
</article-meta>
</front>
</pmc>
</record>
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