ArticleThe Journal of experimental medicine2014
Chemokine-coupled β2 integrin-induced macrophage Rac2-Myosin IIA interaction regulates VEGF-A mRNA stability and arteriogenesis.
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Article in The Journal of experimental medicine, 2014. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 35 papers.
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35 citing papers in PubMed, 53 citations in OpenAlex.
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Authors and funding
13 authors at 4 institutions in 4 countries.
Alan R MorrisonSection of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511.
Timur O YarovinskySection of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511.
Bryan D YoungSection of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511.
Filipa MoraesSection of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511.
Tyler D RossSection of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511.
Nicolle CeneriSection of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511.
Jiasheng ZhangSection of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511.
Zhen W ZhuangSection of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511.
Albert J SinusasSection of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511.
Ruggero PardiDepartment of Molecular Pathology, Universita Vita Salute School of Medicine, San Raffaele Scientific Institute, 20123 Milan, Italy.
Martin A SchwartzSection of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511.
Michael SimonsSection of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511.
Jeffrey R BenderSection of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 Section of Cardiovascular Medicine, Department of Internal Medicine and the Yale Cardiovascular Research Center, Department of Immunobiology, Department of Cell Biology, and the Raymond and Beverly Sackler Foundation Cardiovascular Laboratory, Yale University School of Medicine, New Haven, CT 06511 jeffrey.bender@yale.edu.
Yale University · USCardiovascular Research Center · BRInstitute of Cell Biology · UAVita-Salute San Raffaele University · IT
Funding
Yale University Clinical and Translational Science Award ProgramUL1TR000142 · NCATS · YALE UNIVERSITY · PI SHERWIN, ROBERT S · 2012 to 2015
$31.8MVascular Training GrantT32HL007950 · NHLBI · YALE UNIVERSITY · PI JEFFREY R. BENDER, Daniel Greif · 2000 to 2026
$9.6MArteriogenesis and BranchingR01HL084619 · NHLBI · YALE UNIVERSITY · PI SIMONS, MICHAEL · 2007 to 2018
$6.7MThe Rho Family GTPases in Integrin SignalingR01GM047214 · NIGMS · YALE UNIVERSITY · PI SCHWARTZ, MARTIN A · 1991 to 2020
$6.3MIntegrins in the Endothelial Response to Fluid Shear StressR01HL075092 · NHLBI · YALE UNIVERSITY · PI SCHWARTZ, MARTIN A · 2004 to 2019
$5.1MMOLECULAR MODELS OF IMMUNE-MEDIATED VASCULAR INJURYR01HL043331 · NHLBI · YALE UNIVERSITY · PI BENDER, JEFFREY R. · 1991 to 2012
$4.9MThe Rac-2-induced macrophage proteome and vascular pathologyF32HL097422 · NHLBI · YALE UNIVERSITY · PI MORRISON, ALAN ROSS · 2009 to 2011
$168kNCATS NIH HHS UL1 TR000142NHLBI NIH HHS F32 HL097422NHLBI NIH HHS L30 HL115713NHLBI NIH HHS R01 HL043331NHLBI NIH HHS R01 HL075092NHLBI NIH HHS R01 HL084619NHLBI NIH HHS T32 HL007950NIGMS NIH HHS R01 GM047214NIGMS NIH HHS R01 GM47214
Abstract
Myeloid cells are important contributors to arteriogenesis, but their key molecular triggers and cellular effectors are largely unknown. We report, in inflammatory monocytes, that the combination of chemokine receptor (CCR2) and adhesion receptor (β2 integrin) engagement leads to an interaction between activated Rac2 and Myosin 9 (Myh9), the heavy chain of Myosin IIA, resulting in augmented vascular endothelial growth factor A (VEGF-A) expression and induction of arteriogenesis. In human monocytes, CCL2 stimulation coupled to ICAM-1 adhesion led to rapid nuclear-to-cytosolic translocation of the RNA-binding protein HuR. This activation of HuR and its stabilization of VEGF-A mRNA were Rac2-dependent, and proteomic analysis for Rac2 interactors identified the 226 kD protein Myh9. The level of induced Rac2-Myh9 interaction strongly correlated with the degree of HuR translocation. CCL2-coupled ICAM-1 adhesion-driven HuR translocation and consequent VEGF-A mRNA stabilization were absent in Myh9(-/-) macrophages. Macrophage VEGF-A production, ischemic tissue VEGF-A levels, and flow recovery to hind limb ischemia were impaired in myeloid-specific Myh9(-/-) mice, despite preserved macrophage recruitment to the ischemic muscle. Micro-CT arteriography determined the impairment to be defective induced arteriogenesis, whereas developmental vasculogenesis was unaffected. These results place the macrophage at the center of ischemia-induced arteriogenesis, and they establish a novel role for Myosin IIA in signal transduction events modulating VEGF-A expression in tissue.
Indexed as
AnimalsArteriesCD18 AntigensDNA PrimersFlow CytometryHumansMiceMice, Inbred C57BLMonocytesNeovascularization, PhysiologicNonmuscle Myosin Type IIARAC2 GTP-Binding Proteinrac GTP-Binding ProteinsReal-Time Polymerase Chain ReactionReceptors, CCR2RNA StabilityCcr2 protein, mouseCD18 AntigensDNA PrimersNonmuscle Myosin Type IIARAC2 GTP-Binding Proteinrac GTP-Binding ProteinsReceptors, CCR2Vascular Endothelial Growth Factor A
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