CXCR7 functions as a scavenger for CXCL12 and CXCL11

CXCR7 (RDC1), the recently discovered second receptor for CXCL12, is phylogenetically closely related to chemokine receptors, but fails to couple to G-proteins and to induce typical chemokine receptor mediated cellular responses. The function of CXCR7 is controversial. Some studies suggest a signali...

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Veröffentlicht in:PloS one 2010-02, Vol.5 (2), p.e9175-e9175
Hauptverfasser: Naumann, Ulrike, Cameroni, Elisabetta, Pruenster, Monika, Mahabaleshwar, Harsha, Raz, Erez, Zerwes, Hans-Günter, Rot, Antal, Thelen, Marcus
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container_issue 2
container_start_page e9175
container_title PloS one
container_volume 5
creator Naumann, Ulrike
Cameroni, Elisabetta
Pruenster, Monika
Mahabaleshwar, Harsha
Raz, Erez
Zerwes, Hans-Günter
Rot, Antal
Thelen, Marcus
description CXCR7 (RDC1), the recently discovered second receptor for CXCL12, is phylogenetically closely related to chemokine receptors, but fails to couple to G-proteins and to induce typical chemokine receptor mediated cellular responses. The function of CXCR7 is controversial. Some studies suggest a signaling activity in mammalian cells and zebrafish embryos, while others indicate a decoy activity in fish. Here we investigated the two propositions in human tissues. We provide evidence and mechanistic insight that CXCR7 acts as specific scavenger for CXCL12 and CXCL11 mediating effective ligand internalization and targeting of the chemokine cargo for degradation. Consistently, CXCR7 continuously cycles between the plasma membrane and intracellular compartments in the absence and presence of ligand, both in mammalian cells and in zebrafish. In accordance with the proposed activity as a scavenger receptor CXCR7-dependent chemokine degradation does not become saturated with increasing ligand concentrations. Active CXCL12 sequestration by CXCR7 is demonstrated in adult mouse heart valves and human umbilical vein endothelium. The finding that CXCR7 specifically scavenges CXCL12 suggests a critical function of the receptor in modulating the activity of the ubiquitously expressed CXCR4 in development and tumor formation. Scavenger activity of CXCR7 might also be important for the fine tuning of the mobility of hematopoietic cells in the bone marrow and lymphoid organs.
doi_str_mv 10.1371/journal.pone.0009175
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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Naumann, Ulrike</au><au>Cameroni, Elisabetta</au><au>Pruenster, Monika</au><au>Mahabaleshwar, Harsha</au><au>Raz, Erez</au><au>Zerwes, Hans-Günter</au><au>Rot, Antal</au><au>Thelen, Marcus</au><au>Pockley, Graham</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>CXCR7 functions as a scavenger for CXCL12 and CXCL11</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2010-02-11</date><risdate>2010</risdate><volume>5</volume><issue>2</issue><spage>e9175</spage><epage>e9175</epage><pages>e9175-e9175</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>CXCR7 (RDC1), the recently discovered second receptor for CXCL12, is phylogenetically closely related to chemokine receptors, but fails to couple to G-proteins and to induce typical chemokine receptor mediated cellular responses. The function of CXCR7 is controversial. Some studies suggest a signaling activity in mammalian cells and zebrafish embryos, while others indicate a decoy activity in fish. Here we investigated the two propositions in human tissues. We provide evidence and mechanistic insight that CXCR7 acts as specific scavenger for CXCL12 and CXCL11 mediating effective ligand internalization and targeting of the chemokine cargo for degradation. Consistently, CXCR7 continuously cycles between the plasma membrane and intracellular compartments in the absence and presence of ligand, both in mammalian cells and in zebrafish. In accordance with the proposed activity as a scavenger receptor CXCR7-dependent chemokine degradation does not become saturated with increasing ligand concentrations. Active CXCL12 sequestration by CXCR7 is demonstrated in adult mouse heart valves and human umbilical vein endothelium. The finding that CXCR7 specifically scavenges CXCL12 suggests a critical function of the receptor in modulating the activity of the ubiquitously expressed CXCR4 in development and tumor formation. Scavenger activity of CXCR7 might also be important for the fine tuning of the mobility of hematopoietic cells in the bone marrow and lymphoid organs.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>20161793</pmid><doi>10.1371/journal.pone.0009175</doi><tpages>e9175</tpages><oa>free_for_read</oa></addata></record>
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subjects Amino acids
Animal tissues
Animals
B cells
Biochemistry
Biochemistry/Cell Signaling and Trafficking Structures
Biomedical research
Bone marrow
Cell adhesion & migration
Cell Biology
Cell Biology/Membranes and Sorting
Cell Line
Cell Line, Tumor
Cell Membrane - metabolism
Cells, Cultured
Chemokine CXCL11 - genetics
Chemokine CXCL11 - metabolism
Chemokine CXCL12 - genetics
Chemokine CXCL12 - metabolism
Chemokine receptors
Chemokines
CXCL11 protein
CXCL12 protein
CXCR4 protein
Danio rerio
Degradation
Embryo, Nonmammalian - metabolism
Embryos
Endocytosis - physiology
Endothelial Cells - cytology
Endothelial Cells - metabolism
Endothelium
Female
Flow Cytometry
Green Fluorescent Proteins - genetics
Green Fluorescent Proteins - metabolism
Heart
HeLa Cells
Human tissues
Humans
Immunology
Immunology/Immunomodulation
Internalization
Kinases
Ligands
Male
Mammalian cells
Mammals
Metastasis
Mice
Mice, Inbred BALB C
Microscopy, Confocal
Mutation
Myocardium - metabolism
Organs
Penicillin
Phylogeny
Plasmids
Prostate cancer
Proteins
Receptors
Receptors, CXCR - genetics
Receptors, CXCR - metabolism
Receptors, CXCR - physiology
Recombinant Fusion Proteins - genetics
Recombinant Fusion Proteins - metabolism
Rodents
Scavenger receptors
Signal transduction
Signaling
Transfection
Umbilical vein
Zebrafish
title CXCR7 functions as a scavenger for CXCL12 and CXCL11
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