Essential Regulation of CNS Angiogenesis by the Orphan G Protein-Coupled Receptor GPR124
The orphan G protein-coupled receptor (GPCR) GPR124/tumor endothelial marker 5 is highly expressed in central nervous system (CNS) endothelium. Here, we show that complete null or endothelial-specific GPR124 deletion resulted in embryonic lethality from CNS-specific angiogenesis arrest in forebrain...
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| Veröffentlicht in: | Science (American Association for the Advancement of Science) 2010-11, Vol.330 (6006), p.985-989 |
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| creator | Kuhnert, Frank Mancuso, Michael R Shamloo, Amir Wang, Hsiao-Ting Choksi, Vir Florek, Mareike Su, Hua Fruttiger, Marcus Young, William L Heilshorn, Sarah C Kuo, Calvin J |
| description | The orphan G protein-coupled receptor (GPCR) GPR124/tumor endothelial marker 5 is highly expressed in central nervous system (CNS) endothelium. Here, we show that complete null or endothelial-specific GPR124 deletion resulted in embryonic lethality from CNS-specific angiogenesis arrest in forebrain and neural tube. Conversely, GPR124 overexpression throughout all adult vascular beds produced CNS-specific hyperproliferative vascular malformations. In vivo, GPR124 functioned cell-autonomously in endothelium to regulate sprouting, migration, and developmental expression of the blood-brain barrier marker Glut1, whereas in vitro, GPR124 mediated Cdc42-dependent directional migration to forebrain-derived, vascular endothelial growth factor-independent cues. Our results demonstrate CNS-specific angiogenesis regulation by an endothelial receptor and illuminate functions of the poorly understood adhesion GPCR subfamily. Further, the functional tropism of GPR124 marks this receptor as a therapeutic target for CNS-related vascular pathologies. |
| doi_str_mv | 10.1126/science.1196554 |
| format | Article |
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Here, we show that complete null or endothelial-specific GPR124 deletion resulted in embryonic lethality from CNS-specific angiogenesis arrest in forebrain and neural tube. Conversely, GPR124 overexpression throughout all adult vascular beds produced CNS-specific hyperproliferative vascular malformations. In vivo, GPR124 functioned cell-autonomously in endothelium to regulate sprouting, migration, and developmental expression of the blood-brain barrier marker Glut1, whereas in vitro, GPR124 mediated Cdc42-dependent directional migration to forebrain-derived, vascular endothelial growth factor-independent cues. Our results demonstrate CNS-specific angiogenesis regulation by an endothelial receptor and illuminate functions of the poorly understood adhesion GPCR subfamily. Further, the functional tropism of GPR124 marks this receptor as a therapeutic target for CNS-related vascular pathologies.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.1196554</identifier><identifier>PMID: 21071672</identifier><identifier>CODEN: SCIEAS</identifier><language>eng</language><publisher>Washington, DC: American Association for the Advancement of Science</publisher><subject>Adhesion ; Anatomy ; Angiogenesis ; Animals ; Biological and medical sciences ; Blood Vessels - abnormalities ; Blood-Brain Barrier - metabolism ; Brain ; Brain research ; Cell Movement ; Central nervous system ; Control ; Embryonic Development ; Embryos ; Endothelial cells ; Endothelial Cells - physiology ; Endothelium ; Endothelium, Vascular - embryology ; Endothelium, Vascular - metabolism ; Forebrain ; Fundamental and applied biological sciences. Psychology ; Gene Deletion ; General aspects ; Glucose Transporter Type 1 - metabolism ; Markers ; Mesencephalon - blood supply ; Mesencephalon - embryology ; Mesencephalon - metabolism ; Mice ; Mice, Knockout ; Mice, Transgenic ; Migration ; Neovascularization, Physiologic ; Nervous system ; Neural Tube - blood supply ; Neural Tube - embryology ; Neural Tube - metabolism ; Prosencephalon - blood supply ; Prosencephalon - embryology ; Prosencephalon - metabolism ; Proteins ; Receptors ; Receptors, G-Protein-Coupled - genetics ; Receptors, G-Protein-Coupled - metabolism ; Rhombencephalon - blood supply ; Rhombencephalon - embryology ; Rhombencephalon - metabolism ; Sprouts ; Telencephalon ; Telencephalon - blood supply ; Telencephalon - embryology ; Telencephalon - metabolism ; Tropism ; Vascular malformations ; Veins & arteries ; Vertebrates: cardiovascular system</subject><ispartof>Science (American Association for the Advancement of Science), 2010-11, Vol.330 (6006), p.985-989</ispartof><rights>Copyright © 2010 American Association for the Advancement of Science</rights><rights>2015 INIST-CNRS</rights><rights>Copyright © 2010, American Association for the Advancement of Science</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c659t-961ac1a3b102d176bde51744495b581c6ce03a93ee235949da8ae9d40792fd13</citedby><cites>FETCH-LOGICAL-c659t-961ac1a3b102d176bde51744495b581c6ce03a93ee235949da8ae9d40792fd13</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/40931878$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/40931878$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,781,785,804,886,2885,2886,27928,27929,58021,58254</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=23452181$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21071672$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kuhnert, Frank</creatorcontrib><creatorcontrib>Mancuso, Michael R</creatorcontrib><creatorcontrib>Shamloo, Amir</creatorcontrib><creatorcontrib>Wang, Hsiao-Ting</creatorcontrib><creatorcontrib>Choksi, Vir</creatorcontrib><creatorcontrib>Florek, Mareike</creatorcontrib><creatorcontrib>Su, Hua</creatorcontrib><creatorcontrib>Fruttiger, Marcus</creatorcontrib><creatorcontrib>Young, William L</creatorcontrib><creatorcontrib>Heilshorn, Sarah C</creatorcontrib><creatorcontrib>Kuo, Calvin J</creatorcontrib><title>Essential Regulation of CNS Angiogenesis by the Orphan G Protein-Coupled Receptor GPR124</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>The orphan G protein-coupled receptor (GPCR) GPR124/tumor endothelial marker 5 is highly expressed in central nervous system (CNS) endothelium. Here, we show that complete null or endothelial-specific GPR124 deletion resulted in embryonic lethality from CNS-specific angiogenesis arrest in forebrain and neural tube. Conversely, GPR124 overexpression throughout all adult vascular beds produced CNS-specific hyperproliferative vascular malformations. In vivo, GPR124 functioned cell-autonomously in endothelium to regulate sprouting, migration, and developmental expression of the blood-brain barrier marker Glut1, whereas in vitro, GPR124 mediated Cdc42-dependent directional migration to forebrain-derived, vascular endothelial growth factor-independent cues. Our results demonstrate CNS-specific angiogenesis regulation by an endothelial receptor and illuminate functions of the poorly understood adhesion GPCR subfamily. Further, the functional tropism of GPR124 marks this receptor as a therapeutic target for CNS-related vascular pathologies.</description><subject>Adhesion</subject><subject>Anatomy</subject><subject>Angiogenesis</subject><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Blood Vessels - abnormalities</subject><subject>Blood-Brain Barrier - metabolism</subject><subject>Brain</subject><subject>Brain research</subject><subject>Cell Movement</subject><subject>Central nervous system</subject><subject>Control</subject><subject>Embryonic Development</subject><subject>Embryos</subject><subject>Endothelial cells</subject><subject>Endothelial Cells - physiology</subject><subject>Endothelium</subject><subject>Endothelium, Vascular - embryology</subject><subject>Endothelium, Vascular - metabolism</subject><subject>Forebrain</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Deletion</subject><subject>General aspects</subject><subject>Glucose Transporter Type 1 - metabolism</subject><subject>Markers</subject><subject>Mesencephalon - blood supply</subject><subject>Mesencephalon - embryology</subject><subject>Mesencephalon - metabolism</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Mice, Transgenic</subject><subject>Migration</subject><subject>Neovascularization, Physiologic</subject><subject>Nervous system</subject><subject>Neural Tube - blood supply</subject><subject>Neural Tube - embryology</subject><subject>Neural Tube - metabolism</subject><subject>Prosencephalon - blood supply</subject><subject>Prosencephalon - embryology</subject><subject>Prosencephalon - metabolism</subject><subject>Proteins</subject><subject>Receptors</subject><subject>Receptors, G-Protein-Coupled - genetics</subject><subject>Receptors, G-Protein-Coupled - metabolism</subject><subject>Rhombencephalon - blood supply</subject><subject>Rhombencephalon - embryology</subject><subject>Rhombencephalon - metabolism</subject><subject>Sprouts</subject><subject>Telencephalon</subject><subject>Telencephalon - blood supply</subject><subject>Telencephalon - embryology</subject><subject>Telencephalon - metabolism</subject><subject>Tropism</subject><subject>Vascular malformations</subject><subject>Veins & arteries</subject><subject>Vertebrates: cardiovascular system</subject><issn>0036-8075</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFks1v1DAQxSMEokvhzAmIhBBcQj3-SuaCVK3KglTRqi0SN8vrOLteZe3UTpD63-Nql-XjACdr9H7z5HkzRfEcyHsAKk-ScdYbmwuUQvAHxQwIigopYQ-LGSFMVg2pxVHxJKUNIVlD9rg4okBqkDWdFd_OUrJ-dLovr-xq6vXogi9DV86_XJenfuXCynqbXCqXd-W4tuVFHNbal4vyMobROl_NwzT0ts3txg5jiOXi8goof1o86nSf7LP9e1zcfDy7mX-qzi8Wn-en55WRAscKJWgDmi2B0BZquWytgJpzjmIpGjDSWMI0MmspE8ix1Y222HJSI-1aYMfFh53tMC23tjV5lqh7NUS31fFOBe3Un4p3a7UK3xUjiLzGbPB2bxDD7WTTqLYuGdv32tswJdVw5LJmhP-fZCgx_5ll8t0_yRw9cMpAyIy-_gvdhCn6nJgCSiFHgQ3J1MmOMjGkFG13GBCIuj8EtT8EtT-E3PHy91wO_M_NZ-DNHtDJ6L6L2huXfnGMCwrNfcAvdtwm5eUedE6QQVM3WX-10zsdlF7F7PH1mhJgBJBgIxj7Ad54zY0</recordid><startdate>20101112</startdate><enddate>20101112</enddate><creator>Kuhnert, Frank</creator><creator>Mancuso, Michael R</creator><creator>Shamloo, Amir</creator><creator>Wang, Hsiao-Ting</creator><creator>Choksi, Vir</creator><creator>Florek, Mareike</creator><creator>Su, Hua</creator><creator>Fruttiger, Marcus</creator><creator>Young, William L</creator><creator>Heilshorn, Sarah C</creator><creator>Kuo, Calvin J</creator><general>American Association for the Advancement of Science</general><general>The American Association for the Advancement of Science</general><scope>FBQ</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QF</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QQ</scope><scope>7QR</scope><scope>7SC</scope><scope>7SE</scope><scope>7SN</scope><scope>7SP</scope><scope>7SR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7TK</scope><scope>7TM</scope><scope>7U5</scope><scope>7U9</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>H94</scope><scope>JG9</scope><scope>JQ2</scope><scope>K9.</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>20101112</creationdate><title>Essential Regulation of CNS Angiogenesis by the Orphan G Protein-Coupled Receptor GPR124</title><author>Kuhnert, Frank ; Mancuso, Michael R ; Shamloo, Amir ; Wang, Hsiao-Ting ; Choksi, Vir ; Florek, Mareike ; Su, Hua ; Fruttiger, Marcus ; Young, William L ; Heilshorn, Sarah C ; Kuo, Calvin J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c659t-961ac1a3b102d176bde51744495b581c6ce03a93ee235949da8ae9d40792fd13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Adhesion</topic><topic>Anatomy</topic><topic>Angiogenesis</topic><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Blood Vessels - abnormalities</topic><topic>Blood-Brain Barrier - metabolism</topic><topic>Brain</topic><topic>Brain research</topic><topic>Cell Movement</topic><topic>Central nervous system</topic><topic>Control</topic><topic>Embryonic Development</topic><topic>Embryos</topic><topic>Endothelial cells</topic><topic>Endothelial Cells - physiology</topic><topic>Endothelium</topic><topic>Endothelium, Vascular - embryology</topic><topic>Endothelium, Vascular - metabolism</topic><topic>Forebrain</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Deletion</topic><topic>General aspects</topic><topic>Glucose Transporter Type 1 - metabolism</topic><topic>Markers</topic><topic>Mesencephalon - blood supply</topic><topic>Mesencephalon - embryology</topic><topic>Mesencephalon - metabolism</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Mice, Transgenic</topic><topic>Migration</topic><topic>Neovascularization, Physiologic</topic><topic>Nervous system</topic><topic>Neural Tube - blood supply</topic><topic>Neural Tube - embryology</topic><topic>Neural Tube - metabolism</topic><topic>Prosencephalon - blood supply</topic><topic>Prosencephalon - embryology</topic><topic>Prosencephalon - metabolism</topic><topic>Proteins</topic><topic>Receptors</topic><topic>Receptors, G-Protein-Coupled - genetics</topic><topic>Receptors, G-Protein-Coupled - metabolism</topic><topic>Rhombencephalon - blood supply</topic><topic>Rhombencephalon - embryology</topic><topic>Rhombencephalon - metabolism</topic><topic>Sprouts</topic><topic>Telencephalon</topic><topic>Telencephalon - blood supply</topic><topic>Telencephalon - embryology</topic><topic>Telencephalon - metabolism</topic><topic>Tropism</topic><topic>Vascular malformations</topic><topic>Veins & arteries</topic><topic>Vertebrates: cardiovascular system</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kuhnert, Frank</creatorcontrib><creatorcontrib>Mancuso, Michael R</creatorcontrib><creatorcontrib>Shamloo, Amir</creatorcontrib><creatorcontrib>Wang, Hsiao-Ting</creatorcontrib><creatorcontrib>Choksi, Vir</creatorcontrib><creatorcontrib>Florek, Mareike</creatorcontrib><creatorcontrib>Su, Hua</creatorcontrib><creatorcontrib>Fruttiger, Marcus</creatorcontrib><creatorcontrib>Young, William L</creatorcontrib><creatorcontrib>Heilshorn, Sarah C</creatorcontrib><creatorcontrib>Kuo, Calvin J</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kuhnert, Frank</au><au>Mancuso, Michael R</au><au>Shamloo, Amir</au><au>Wang, Hsiao-Ting</au><au>Choksi, Vir</au><au>Florek, Mareike</au><au>Su, Hua</au><au>Fruttiger, Marcus</au><au>Young, William L</au><au>Heilshorn, Sarah C</au><au>Kuo, Calvin J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Essential Regulation of CNS Angiogenesis by the Orphan G Protein-Coupled Receptor GPR124</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2010-11-12</date><risdate>2010</risdate><volume>330</volume><issue>6006</issue><spage>985</spage><epage>989</epage><pages>985-989</pages><issn>0036-8075</issn><eissn>1095-9203</eissn><coden>SCIEAS</coden><abstract>The orphan G protein-coupled receptor (GPCR) GPR124/tumor endothelial marker 5 is highly expressed in central nervous system (CNS) endothelium. Here, we show that complete null or endothelial-specific GPR124 deletion resulted in embryonic lethality from CNS-specific angiogenesis arrest in forebrain and neural tube. Conversely, GPR124 overexpression throughout all adult vascular beds produced CNS-specific hyperproliferative vascular malformations. In vivo, GPR124 functioned cell-autonomously in endothelium to regulate sprouting, migration, and developmental expression of the blood-brain barrier marker Glut1, whereas in vitro, GPR124 mediated Cdc42-dependent directional migration to forebrain-derived, vascular endothelial growth factor-independent cues. Our results demonstrate CNS-specific angiogenesis regulation by an endothelial receptor and illuminate functions of the poorly understood adhesion GPCR subfamily. Further, the functional tropism of GPR124 marks this receptor as a therapeutic target for CNS-related vascular pathologies.</abstract><cop>Washington, DC</cop><pub>American Association for the Advancement of Science</pub><pmid>21071672</pmid><doi>10.1126/science.1196554</doi><tpages>5</tpages><oa>free_for_read</oa></addata></record> |
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| issn | 0036-8075 1095-9203 |
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| source | MEDLINE; Science Magazine; Jstor Complete Legacy |
| subjects | Adhesion Anatomy Angiogenesis Animals Biological and medical sciences Blood Vessels - abnormalities Blood-Brain Barrier - metabolism Brain Brain research Cell Movement Central nervous system Control Embryonic Development Embryos Endothelial cells Endothelial Cells - physiology Endothelium Endothelium, Vascular - embryology Endothelium, Vascular - metabolism Forebrain Fundamental and applied biological sciences. Psychology Gene Deletion General aspects Glucose Transporter Type 1 - metabolism Markers Mesencephalon - blood supply Mesencephalon - embryology Mesencephalon - metabolism Mice Mice, Knockout Mice, Transgenic Migration Neovascularization, Physiologic Nervous system Neural Tube - blood supply Neural Tube - embryology Neural Tube - metabolism Prosencephalon - blood supply Prosencephalon - embryology Prosencephalon - metabolism Proteins Receptors Receptors, G-Protein-Coupled - genetics Receptors, G-Protein-Coupled - metabolism Rhombencephalon - blood supply Rhombencephalon - embryology Rhombencephalon - metabolism Sprouts Telencephalon Telencephalon - blood supply Telencephalon - embryology Telencephalon - metabolism Tropism Vascular malformations Veins & arteries Vertebrates: cardiovascular system |
| title | Essential Regulation of CNS Angiogenesis by the Orphan G Protein-Coupled Receptor GPR124 |
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