miR-10 Regulates the Angiogenic Behavior of Zebrafish and Human Endothelial Cells by Promoting VEGF Signaling
Identifieur interne : 003C88 ( Main/Exploration ); précédent : 003C87; suivant : 003C89miR-10 Regulates the Angiogenic Behavior of Zebrafish and Human Endothelial Cells by Promoting VEGF Signaling
Auteurs : David Hassel [États-Unis, Allemagne] ; Paul Cheng [États-Unis] ; Mark P. White [États-Unis] ; Kathryn N. Ivey [États-Unis] ; Jens Kroll [Allemagne] ; Hellmut G. Augustin [Allemagne] ; Hugo A. Katus [Allemagne] ; Didier Y. R. Stainier [États-Unis, Allemagne] ; Deepak Srivastava [États-Unis]Source :
- Circulation research [ 0009-7330 ] ; 2012.
Abstract
Formation and remodeling of the vasculature during development and disease involves a highly conserved and precisely regulated network of attractants and repellants. Various signaling pathways control the behavior of endothelial cells, but their post-transcriptional dose-titration by miRNAs is poorly understood.
To identify miRNAs that regulate angiogenesis.
We show that the highly conserved microRNA family encoding miR-10 regulates the behavior of endothelial cells during angiogenesis by positively titrating pro-angiogenic signaling. Knockdown of miR-10 led to premature truncation of intersegmental vessel growth (ISV) in the trunk of zebrafish larvae, while overexpression of miR-10 promoted angiogenic behavior in zebrafish and cultured human umbilical venous endothelial cells (HUVECs). We found that miR-10 functions, in part, by directly regulating the level of fms-related tyrosine kinase 1 (FLT1), a cell-surface protein that sequesters VEGF, and its soluble splice variant sFLT1. The increase in FLT1/sFLT1 protein levels upon miR-10 knockdown in zebrafish and in HUVECs inhibited the angiogenic behavior of endothelial cells largely by antagonizing VEGF receptor-2 signaling.
Our study provides insights into how FLT1 and VEGF receptor-2 signaling is titrated in a miRNA-mediated manner and establishes miR-10 as a potential new target for the selective modulation of angiogenesis.
Url:
DOI: 10.1161/CIRCRESAHA.112.279711
PubMed: 22955733
PubMed Central: 3525481
Affiliations:
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Stainier</name><affiliation wicri:level="1"><nlm:aff id="A4">Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, CA 94158</wicri:regionArea><wicri:noRegion>CA 94158</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A8">Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, 61231 Bad Nauheim, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, 61231 Bad Nauheim</wicri:regionArea><wicri:noRegion>61231 Bad Nauheim</wicri:noRegion><wicri:noRegion>61231 Bad Nauheim</wicri:noRegion><wicri:noRegion>61231 Bad Nauheim</wicri:noRegion></affiliation></author><author><name sortKey="Srivastava, Deepak" 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Signaling</title><author><name sortKey="Hassel, David" sort="Hassel, David" uniqKey="Hassel D" first="David" last="Hassel">David Hassel</name><affiliation wicri:level="1"><nlm:aff id="A1">Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158</wicri:regionArea><wicri:noRegion>CA 94158</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:aff id="A7">Department of Medicine III, Cardiology, University of Heidelberg, 69120 Heidelberg, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Medicine III, Cardiology, University of Heidelberg, 69120 Heidelberg</wicri:regionArea><placeName><region type="land" nuts="1">Bade-Wurtemberg</region><region type="district" nuts="2">District de Karlsruhe</region><settlement type="city">Heidelberg</settlement></placeName></affiliation></author><author><name sortKey="Cheng, Paul" sort="Cheng, Paul" uniqKey="Cheng P" first="Paul" last="Cheng">Paul Cheng</name><affiliation wicri:level="1"><nlm:aff id="A1">Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158</wicri:regionArea><wicri:noRegion>CA 94158</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Roddenberry Center for Stem Cell Biology and Medicine at Gladstone, San Francisco, CA, 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Roddenberry Center for Stem Cell Biology and Medicine at Gladstone, San Francisco, CA, 94158</wicri:regionArea><wicri:noRegion>94158</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A3">Department of Pediatrics, University of California, San Francisco, San Francisco, CA 94143, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pediatrics, University of California, San Francisco, San Francisco, CA 94143</wicri:regionArea><wicri:noRegion>CA 94143</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A4">Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, CA 94158</wicri:regionArea><wicri:noRegion>CA 94158</wicri:noRegion></affiliation></author><author><name sortKey="White, Mark P" sort="White, Mark P" uniqKey="White M" first="Mark P." last="White">Mark P. White</name><affiliation wicri:level="1"><nlm:aff id="A1">Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158</wicri:regionArea><wicri:noRegion>CA 94158</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Roddenberry Center for Stem Cell Biology and Medicine at Gladstone, San Francisco, CA, 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Roddenberry Center for Stem Cell Biology and Medicine at Gladstone, San Francisco, CA, 94158</wicri:regionArea><wicri:noRegion>94158</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A3">Department of Pediatrics, University of California, San Francisco, San Francisco, CA 94143, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pediatrics, University of California, San Francisco, San Francisco, CA 94143</wicri:regionArea><wicri:noRegion>CA 94143</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A4">Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, CA 94158</wicri:regionArea><wicri:noRegion>CA 94158</wicri:noRegion></affiliation></author><author><name sortKey="Ivey, Kathryn N" sort="Ivey, Kathryn N" uniqKey="Ivey K" first="Kathryn N." last="Ivey">Kathryn N. Ivey</name><affiliation wicri:level="1"><nlm:aff id="A1">Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158</wicri:regionArea><wicri:noRegion>CA 94158</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Roddenberry Center for Stem Cell Biology and Medicine at Gladstone, San Francisco, CA, 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Roddenberry Center for Stem Cell Biology and Medicine at Gladstone, San Francisco, CA, 94158</wicri:regionArea><wicri:noRegion>94158</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A3">Department of Pediatrics, University of California, San Francisco, San Francisco, CA 94143, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pediatrics, University of California, San Francisco, San Francisco, CA 94143</wicri:regionArea><wicri:noRegion>CA 94143</wicri:noRegion></affiliation></author><author><name sortKey="Kroll, Jens" sort="Kroll, Jens" uniqKey="Kroll J" first="Jens" last="Kroll">Jens Kroll</name><affiliation wicri:level="3"><nlm:aff id="A5">Department of Vascular Biology and Tumor Angiogenesis, Center for Biomedicine and Medical Technology Mannheim, Mannheim, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Vascular Biology and Tumor Angiogenesis, Center for Biomedicine and Medical Technology Mannheim, Mannheim</wicri:regionArea><placeName><region type="land" nuts="1">Bade-Wurtemberg</region><region type="district" nuts="2">District de Karlsruhe</region><settlement type="city">Mannheim</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="A6">Division of Vascular Oncology and Metastasis, German Cancer Research Center (DKFZ-ZMBH Alliance), Heidelberg, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Division of Vascular Oncology and Metastasis, German Cancer Research Center (DKFZ-ZMBH Alliance), Heidelberg</wicri:regionArea><placeName><region type="land" nuts="1">Bade-Wurtemberg</region><region type="district" nuts="2">District de Karlsruhe</region><settlement type="city">Heidelberg</settlement></placeName></affiliation></author><author><name sortKey="Augustin, Hellmut G" sort="Augustin, Hellmut G" uniqKey="Augustin H" first="Hellmut G." last="Augustin">Hellmut G. Augustin</name><affiliation wicri:level="3"><nlm:aff id="A5">Department of Vascular Biology and Tumor Angiogenesis, Center for Biomedicine and Medical Technology Mannheim, Mannheim, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Vascular Biology and Tumor Angiogenesis, Center for Biomedicine and Medical Technology Mannheim, Mannheim</wicri:regionArea><placeName><region type="land" nuts="1">Bade-Wurtemberg</region><region type="district" nuts="2">District de Karlsruhe</region><settlement type="city">Mannheim</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="A6">Division of Vascular Oncology and Metastasis, German Cancer Research Center (DKFZ-ZMBH Alliance), Heidelberg, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Division of Vascular Oncology and Metastasis, German Cancer Research Center (DKFZ-ZMBH Alliance), Heidelberg</wicri:regionArea><placeName><region type="land" nuts="1">Bade-Wurtemberg</region><region type="district" nuts="2">District de Karlsruhe</region><settlement type="city">Heidelberg</settlement></placeName></affiliation></author><author><name sortKey="Katus, Hugo A" sort="Katus, Hugo A" uniqKey="Katus H" first="Hugo A." last="Katus">Hugo A. Katus</name><affiliation wicri:level="3"><nlm:aff id="A7">Department of Medicine III, Cardiology, University of Heidelberg, 69120 Heidelberg, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Medicine III, Cardiology, University of Heidelberg, 69120 Heidelberg</wicri:regionArea><placeName><region type="land" nuts="1">Bade-Wurtemberg</region><region type="district" nuts="2">District de Karlsruhe</region><settlement type="city">Heidelberg</settlement></placeName></affiliation></author><author><name sortKey="Stainier, Didier Y R" sort="Stainier, Didier Y R" uniqKey="Stainier D" first="Didier Y. R." last="Stainier">Didier Y. R. Stainier</name><affiliation wicri:level="1"><nlm:aff id="A4">Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, CA 94158</wicri:regionArea><wicri:noRegion>CA 94158</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A8">Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, 61231 Bad Nauheim, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, 61231 Bad Nauheim</wicri:regionArea><wicri:noRegion>61231 Bad Nauheim</wicri:noRegion><wicri:noRegion>61231 Bad Nauheim</wicri:noRegion><wicri:noRegion>61231 Bad Nauheim</wicri:noRegion></affiliation></author><author><name sortKey="Srivastava, Deepak" sort="Srivastava, Deepak" uniqKey="Srivastava D" first="Deepak" last="Srivastava">Deepak Srivastava</name><affiliation wicri:level="1"><nlm:aff id="A1">Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Gladstone Institute of Cardiovascular Disease, San Francisco, CA 94158</wicri:regionArea><wicri:noRegion>CA 94158</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Roddenberry Center for Stem Cell Biology and Medicine at Gladstone, San Francisco, CA, 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Roddenberry Center for Stem Cell Biology and Medicine at Gladstone, San Francisco, CA, 94158</wicri:regionArea><wicri:noRegion>94158</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A3">Department of Pediatrics, University of California, San Francisco, San Francisco, CA 94143, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pediatrics, University of California, San Francisco, San Francisco, CA 94143</wicri:regionArea><wicri:noRegion>CA 94143</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A4">Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, CA 94158</wicri:regionArea><wicri:noRegion>CA 94158</wicri:noRegion></affiliation></author></analytic><series><title level="j">Circulation research</title><idno type="ISSN">0009-7330</idno><idno type="eISSN">1524-4571</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec id="S1"><title>Rationale</title><p id="P1">Formation and remodeling of the vasculature during development and disease involves a highly conserved and precisely regulated network of attractants and repellants. Various signaling pathways control the behavior of endothelial cells, but their post-transcriptional dose-titration by miRNAs is poorly understood.</p></sec><sec id="S2"><title>Objective</title><p id="P2">To identify miRNAs that regulate angiogenesis.</p></sec><sec id="S3"><title>Methods and Results</title><p id="P3">We show that the highly conserved microRNA family encoding miR-10 regulates the behavior of endothelial cells during angiogenesis by positively titrating pro-angiogenic signaling. Knockdown of miR-10 led to premature truncation of intersegmental vessel growth (ISV) in the trunk of zebrafish larvae, while overexpression of miR-10 promoted angiogenic behavior in zebrafish and cultured human umbilical venous endothelial cells (HUVECs). We found that miR-10 functions, in part, by directly regulating the level of fms-related tyrosine kinase 1 (FLT1), a cell-surface protein that sequesters VEGF, and its soluble splice variant sFLT1. The increase in FLT1/sFLT1 protein levels upon miR-10 knockdown in zebrafish and in HUVECs inhibited the angiogenic behavior of endothelial cells largely by antagonizing VEGF receptor-2 signaling.</p></sec><sec id="S4"><title>Conclusion</title><p id="P4">Our study provides insights into how FLT1 and VEGF receptor-2 signaling is titrated in a miRNA-mediated manner and establishes miR-10 as a potential new target for the selective modulation of angiogenesis.</p></sec></div></front></TEI><affiliations><list><country><li>Allemagne</li><li>États-Unis</li></country><region><li>Bade-Wurtemberg</li><li>District de Karlsruhe</li></region><settlement><li>Heidelberg</li><li>Mannheim</li></settlement></list><tree><country name="États-Unis"><noRegion><name sortKey="Hassel, David" sort="Hassel, David" uniqKey="Hassel D" first="David" last="Hassel">David Hassel</name></noRegion><name sortKey="Cheng, Paul" sort="Cheng, Paul" uniqKey="Cheng P" first="Paul" last="Cheng">Paul Cheng</name><name sortKey="Cheng, Paul" sort="Cheng, Paul" uniqKey="Cheng P" first="Paul" last="Cheng">Paul Cheng</name><name sortKey="Cheng, Paul" sort="Cheng, Paul" uniqKey="Cheng P" first="Paul" last="Cheng">Paul Cheng</name><name sortKey="Cheng, Paul" sort="Cheng, Paul" uniqKey="Cheng P" first="Paul" last="Cheng">Paul Cheng</name><name sortKey="Ivey, Kathryn N" sort="Ivey, Kathryn N" uniqKey="Ivey K" first="Kathryn N." last="Ivey">Kathryn N. Ivey</name><name sortKey="Ivey, Kathryn N" sort="Ivey, Kathryn N" uniqKey="Ivey K" first="Kathryn N." last="Ivey">Kathryn N. Ivey</name><name sortKey="Ivey, Kathryn N" sort="Ivey, Kathryn N" uniqKey="Ivey K" first="Kathryn N." last="Ivey">Kathryn N. Ivey</name><name sortKey="Srivastava, Deepak" sort="Srivastava, Deepak" uniqKey="Srivastava D" first="Deepak" last="Srivastava">Deepak Srivastava</name><name sortKey="Srivastava, Deepak" sort="Srivastava, Deepak" uniqKey="Srivastava D" first="Deepak" last="Srivastava">Deepak Srivastava</name><name sortKey="Srivastava, Deepak" sort="Srivastava, Deepak" uniqKey="Srivastava D" first="Deepak" last="Srivastava">Deepak Srivastava</name><name sortKey="Srivastava, Deepak" sort="Srivastava, Deepak" uniqKey="Srivastava D" first="Deepak" last="Srivastava">Deepak Srivastava</name><name sortKey="Stainier, Didier Y R" sort="Stainier, Didier Y R" uniqKey="Stainier D" first="Didier Y. R." last="Stainier">Didier Y. R. Stainier</name><name sortKey="White, Mark P" sort="White, Mark P" uniqKey="White M" first="Mark P." last="White">Mark P. White</name><name sortKey="White, Mark P" sort="White, Mark P" uniqKey="White M" first="Mark P." last="White">Mark P. White</name><name sortKey="White, Mark P" sort="White, Mark P" uniqKey="White M" first="Mark P." last="White">Mark P. White</name><name sortKey="White, Mark P" sort="White, Mark P" uniqKey="White M" first="Mark P." last="White">Mark P. White</name></country><country name="Allemagne"><region name="Bade-Wurtemberg"><name sortKey="Hassel, David" sort="Hassel, David" uniqKey="Hassel D" first="David" last="Hassel">David Hassel</name></region><name sortKey="Augustin, Hellmut G" sort="Augustin, Hellmut G" uniqKey="Augustin H" first="Hellmut G." last="Augustin">Hellmut G. Augustin</name><name sortKey="Augustin, Hellmut G" sort="Augustin, Hellmut G" uniqKey="Augustin H" first="Hellmut G." last="Augustin">Hellmut G. Augustin</name><name sortKey="Katus, Hugo A" sort="Katus, Hugo A" uniqKey="Katus H" first="Hugo A." last="Katus">Hugo A. Katus</name><name sortKey="Kroll, Jens" sort="Kroll, Jens" uniqKey="Kroll J" first="Jens" last="Kroll">Jens Kroll</name><name sortKey="Kroll, Jens" sort="Kroll, Jens" uniqKey="Kroll J" first="Jens" last="Kroll">Jens Kroll</name><name sortKey="Stainier, Didier Y R" sort="Stainier, Didier Y R" uniqKey="Stainier D" first="Didier Y. R." last="Stainier">Didier Y. R. Stainier</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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