VEGFA-VEGFR2 Signaling Pathway (Homo sapiens)

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   <Comment Source="WikiPathways-description">Angiogenesis, the formation of new blood vessels from pre-existing vasculature, is central to a number of physiological conditions, from embryogenesis to wound healing in adults and is a hallmark of pathological conditions such as tumorigenesis [1-3]. Angiogenesis is mediated by the coordinated action of a variety of growth factors, metabolites and cell adhesion molecules in endothelial cells [4-6]. Vascular endothelial growth factor (VEGF) is the principal angiogenic growth factor modulating neovascularization [7].
   <Comment Source="WikiPathways-description">Angiogenesis, the formation of new blood vessels from pre-existing vasculature, is central to a number of physiological conditions, from embryogenesis to wound healing in adults and is a hallmark of pathological conditions such as tumorigenesis [1-3]. Angiogenesis is mediated by the coordinated action of a variety of growth factors, metabolites and cell adhesion molecules in endothelial cells [4-6]. Vascular endothelial growth factor (VEGF) is the principal angiogenic growth factor modulating neovascularization [7].
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The biological effect of VEGF is mediated through specific VEGF receptors on endothelial cell surface. VEGFs (VEGF-A, VEGF-B, VEGF-C and VEGF-D) interact with VEGF receptors such as VEGFR1, VEGFR2 and VEGFR3. Among them, VEGFA/VEGFR2 signaling appears to mediate cellular responses involved in angiogenesis prominently. Further, VEGF/VEGFR1 signaling, though weak, converges to VEGFR2 signaling pathway. VEGFA binding to VEGFR2 at the surface of endothelial cells leads to dimerization and auto-phosphorylation of specific tyrosine residues in the cytoplasmic domain of VEGFR2. It leads to activation of multiple downstream signaling cascades and promotes endothelial cell proliferation, migration, and tube formation relevant to angiogenesis [8]. VEGFR2 dependent activation of PI3K-AKT-mTOR signaling regulates cell survival, cell proliferation, anti-apoptotic and cell permeability functions [9]. Another important pathway of VEGF mediated cell proliferation appears to be through PLCγ-mediated activation of PKC and downstream induction of the ERK and other PKC-dependent pathways [10]. Endothelial cell migration is induced by VEGFA/VEGFR2 signaling through activation of p38MAPK (actin polymerization) and FAK (focal adhesion turnover) which is particularly important in directed migration [11, 12]. Phosphosite specificity towards downstream signalling has also been documented. Phosphosite mapping documented seven phosphosites in VEGFR2 receptor: Y1054, Y1214, Y801, Y1175, Y951, Y1059 and Y996. Phosphorylation of Y1214 and Y1054 regulates signaling events involved in cell migration. Y801 phosphorylation regulates cell survival. Y1175 regulates both cell proliferation and migration. Y951 and Y1059 phosphorylation regulates cell survival, cell migration and cell proliferation.  
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The biological effect of VEGF is mediated through specific VEGF receptors on endothelial cell surface. VEGFs (VEGF-A, VEGF-B, VEGF-C and VEGF-D) interact with VEGF receptors such as VEGFR1, VEGFR2 and VEGFR3. Among them, VEGFA/VEGFR2 signaling appears to mediate cellular responses involved in angiogenesis prominently. Further, VEGF/VEGFR1 signaling, though weak, converges to VEGFR2 signaling pathway. VEGFA binding to VEGFR2 at the surface of endothelial cells leads to dimerization and auto-phosphorylation of specific tyrosine residues in the cytoplasmic domain of VEGFR2. It leads to activation of multiple downstream signaling cascades and promotes endothelial cell proliferation, migration, and tube formation relevant to angiogenesis [8]. VEGFR2 dependent activation of PI3K-AKT-mTOR signaling regulates cell survival, cell proliferation, anti-apoptotic and cell permeability functions [9]. Another important pathway of VEGF mediated cell proliferation appears to be through PLCγ-mediated activation of PKC and downstream induction of the ERK and other PKC-dependent pathways [10]. Endothelial cell migration is induced by VEGFA/VEGFR2 signaling through activation of p38MAPK (actin polymerization) and FAK (focal adhesion turnover) which is particularly important in directed migration [11, 12]. Phosphosite specificity towards downstream signalling has also been documented. Phosphosite mapping documented seven phosphosites in VEGFR2 receptor: Y1054, Y1214, Y801, Y1175, Y951, Y1059 and Y996. Phosphorylation of Y1214 and Y1054 regulates signaling events involved in cell migration. Y801 phosphorylation regulates cell survival. Y1175 regulates both cell proliferation and migration. Y951 and Y1059 phosphorylation regulates cell survival, cell migration and cell proliferation.  
VEGFA/VEGFR2 signaling network compiles data available in the literature with respect to VEGFA signaling (especially VEGFA-165) through VEGFR2 in endothelial cells. The signaling events involving these proteins were derived from experimentally validated data involving multiple experimental techniques and approaches. Individual signaling events in VEGFR2 signaling networks leading to cell proliferation, migration and survival were identified and categorized into protein-protein interactions, enzyme-catalyzed events, activation/inhibition reactions, transport of protein across subcellular compartments, and gene regulation events. Signaling molecules involved in VEGFA/VEGFR2 signaling were categorized to enzymes, receptors and transcription factors and the contextual activation/deactivation of these molecules downstream to VEGFA/ VEGFR2 signaling, in modulating angiogenesis, is documented.
VEGFA/VEGFR2 signaling network compiles data available in the literature with respect to VEGFA signaling (especially VEGFA-165) through VEGFR2 in endothelial cells. The signaling events involving these proteins were derived from experimentally validated data involving multiple experimental techniques and approaches. Individual signaling events in VEGFR2 signaling networks leading to cell proliferation, migration and survival were identified and categorized into protein-protein interactions, enzyme-catalyzed events, activation/inhibition reactions, transport of protein across subcellular compartments, and gene regulation events. Signaling molecules involved in VEGFA/VEGFR2 signaling were categorized to enzymes, receptors and transcription factors and the contextual activation/deactivation of these molecules downstream to VEGFA/ VEGFR2 signaling, in modulating angiogenesis, is documented.
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VEGFA dependent angiogenesis pathway map depicts the integration of  signaling pathways regulating cell survival, cell migration, cell proliferation, cellular interactions downstream of VEGFA/VEGFR2 signaling relevant to angiogenesis, regulation of VEGFR2, phosphosite specificity of VEGFR2 towards downstream signaling, post-translational modifications, molecular function-based information, cross-talks among proteins in the canonical signaling modules and the information on the compartmentalization of proteins. The map of VEGFA/VEGFR2 signaling network is interactive to help investigators to add new information as it becomes available in the future for analysis or representation.  
VEGFA dependent angiogenesis pathway map depicts the integration of  signaling pathways regulating cell survival, cell migration, cell proliferation, cellular interactions downstream of VEGFA/VEGFR2 signaling relevant to angiogenesis, regulation of VEGFR2, phosphosite specificity of VEGFR2 towards downstream signaling, post-translational modifications, molecular function-based information, cross-talks among proteins in the canonical signaling modules and the information on the compartmentalization of proteins. The map of VEGFA/VEGFR2 signaling network is interactive to help investigators to add new information as it becomes available in the future for analysis or representation.  
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VEGFA dependent angiogenesis pathway map can be cited as ‘Abhinand CS , Raju R, Soumya SJ, Arya PS, Sudhakaran PR (2016). VEGF-A/VEGFR2 signaling network in endothelial cells relevant to angiogenesis. J Cell Commun Signal. doi: 10.1007/s12079-016-0352-8’.
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VEGFA dependent angiogenesis pathway map can be cited as ‘Abhinand CS , Raju R, Soumya SJ, Arya PS, Sudhakaran PR (2016). VEGF-A/VEGFR2 signaling network in endothelial cells relevant to angiogenesis. J Cell Commun Signal. doi: 10.1007/s12079-016-0352-8’.
References
References
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4. Kumar VB, Binu S, Soumya SJ et al., 2014. Regulation of vascular endothelial growth factor by metabolic context of the cell. Glycoconj J. 31:427-434.
4. Kumar VB, Binu S, Soumya SJ et al., 2014. Regulation of vascular endothelial growth factor by metabolic context of the cell. Glycoconj J. 31:427-434.
5. Kitazume S, Imamaki R, Ogawa K et al., 2014. Sweet role of platelet endothelial cell adhesion molecule in understanding angiogenesis. Glycobiology. 24:1260-1264.
5. Kitazume S, Imamaki R, Ogawa K et al., 2014. Sweet role of platelet endothelial cell adhesion molecule in understanding angiogenesis. Glycobiology. 24:1260-1264.
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6. Kunhiraman H, Edatt L, Thekkeveedu S et al., 2016.  2‐Deoxy Glucose Modulates Expression and Biological Activity of VEGF in a SIRT‐1 Dependent Mechanism. J Cell Biochem.  
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6. Kunhiraman H, Edatt L, Thekkeveedu S et al., 2016.  2â€�Deoxy Glucose Modulates Expression and Biological Activity of VEGF in a SIRTâ€�1 Dependent Mechanism. J Cell Biochem.  
7. Lohela M, Bry M, Tammela T et al., 2009. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol. 21:154-165.  
7. Lohela M, Bry M, Tammela T et al., 2009. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol. 21:154-165.  
8. Koch S, Claesson-Welsh L, 2012. Signal transduction by vascular endothelial growth factor receptors. Cold Spring Harbor perspectives in medicine. 2(7):a006502.
8. Koch S, Claesson-Welsh L, 2012. Signal transduction by vascular endothelial growth factor receptors. Cold Spring Harbor perspectives in medicine. 2(7):a006502.
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    <Graphics RelX="-1.0" RelY="-1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 1,744: Line 1,740:
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
-
   <State GraphRef="a0347" TextLabel="S498" GraphId="cb2ae">
+
   <State GraphRef="f36ea" TextLabel="S738" GraphId="c6869">
-
     <Graphics RelX="1.0" RelY="1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
+
     <Graphics RelX="-1.0" RelY="-1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="a0347" TextLabel="S259" GraphId="a82d4">
   <State GraphRef="a0347" TextLabel="S259" GraphId="a82d4">
     <Graphics RelX="-0.5333333333333333" RelY="1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="-0.5333333333333333" RelY="1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 +
    <Xref Database="" ID="" />
 +
  </State>
 +
  <State GraphRef="a0347" TextLabel="S498" GraphId="cb2ae">
 +
    <Graphics RelX="1.0" RelY="1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 1,783: Line 1,783:
     <BiopaxRef>fcc</BiopaxRef>
     <BiopaxRef>fcc</BiopaxRef>
     <Graphics RelX="-1.0" RelY="1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="-1.0" RelY="1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
-
    <Xref Database="" ID="" />
 
-
  </State>
 
-
  <State GraphRef="cb1ec" TextLabel="S1105" GraphId="fd892">
 
-
    <Graphics RelX="1.0" RelY="1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="cb1ec" TextLabel="S537" GraphId="ef145">
   <State GraphRef="cb1ec" TextLabel="S537" GraphId="ef145">
     <Graphics RelX="1.0" RelY="-1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="1.0" RelY="-1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 +
    <Xref Database="" ID="" />
 +
  </State>
 +
  <State GraphRef="cb1ec" TextLabel="S1105" GraphId="fd892">
 +
    <Graphics RelX="1.0" RelY="1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 1,840: Line 1,840:
     <BiopaxRef>cd2</BiopaxRef>
     <BiopaxRef>cd2</BiopaxRef>
     <Graphics RelX="0.8333333333333334" RelY="1.0" Width="15.0" Height="15.0" FillColor="ffff00" ShapeType="Oval" />
     <Graphics RelX="0.8333333333333334" RelY="1.0" Width="15.0" Height="15.0" FillColor="ffff00" ShapeType="Oval" />
 +
    <Xref Database="" ID="" />
 +
  </State>
 +
  <State GraphRef="c2188" TextLabel="S114" GraphId="baab8">
 +
    <Graphics RelX="1.0" RelY="1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 1,845: Line 1,849:
     <BiopaxRef>d77</BiopaxRef>
     <BiopaxRef>d77</BiopaxRef>
     <Graphics RelX="-1.0" RelY="0.9" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="-1.0" RelY="0.9" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
-
    <Xref Database="" ID="" />
 
-
  </State>
 
-
  <State GraphRef="c2188" TextLabel="S114" GraphId="baab8">
 
-
    <Graphics RelX="1.0" RelY="1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 1,865: Line 1,865:
   <State GraphRef="ad552" TextLabel="Y129" GraphId="d58ac">
   <State GraphRef="ad552" TextLabel="Y129" GraphId="d58ac">
     <Graphics RelX="-1.0" RelY="1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="-1.0" RelY="1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
-
    <Xref Database="" ID="" />
 
-
  </State>
 
-
  <State GraphRef="f807e" TextLabel="T69" GraphId="dce6c">
 
-
    <Graphics RelX="-1.0" RelY="-1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="f807e" TextLabel="T71" GraphId="bf8c9">
   <State GraphRef="f807e" TextLabel="T71" GraphId="bf8c9">
     <Graphics RelX="-1.0" RelY="1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="-1.0" RelY="1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 +
    <Xref Database="" ID="" />
 +
  </State>
 +
  <State GraphRef="f807e" TextLabel="T69" GraphId="dce6c">
 +
    <Graphics RelX="-1.0" RelY="-1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 1,886: Line 1,886:
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
-
   <State GraphRef="dfc05" TextLabel="S279" GraphId="e2da6">
+
   <State GraphRef="dfc05" TextLabel="S255" GraphId="a21ea">
-
     <Graphics RelX="1.0" RelY="-1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
+
     <Graphics RelX="0.03333333333333333" RelY="1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
-
    <Xref Database="" ID="" />
+
-
  </State>
+
-
  <State GraphRef="dfc05" TextLabel="S368" GraphId="fba0b">
+
-
    <Graphics RelX="1.0" RelY="0.019092412267839375" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
+
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="dfc05" TextLabel="S262" GraphId="ddd41">
   <State GraphRef="dfc05" TextLabel="S262" GraphId="ddd41">
     <Graphics RelX="0.0" RelY="-1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="0.0" RelY="-1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 +
    <Xref Database="" ID="" />
 +
  </State>
 +
  <State GraphRef="dfc05" TextLabel="S279" GraphId="e2da6">
 +
    <Graphics RelX="1.0" RelY="-1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 1,903: Line 1,903:
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
-
   <State GraphRef="dfc05" TextLabel="S255" GraphId="a21ea">
+
   <State GraphRef="dfc05" TextLabel="S368" GraphId="fba0b">
-
     <Graphics RelX="0.03333333333333333" RelY="1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
+
     <Graphics RelX="1.0" RelY="0.019092412267839375" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
-
   <State GraphRef="edf85" TextLabel="S368" GraphId="f96d3">
+
   <State GraphRef="edf85" TextLabel="S279" GraphId="ba895">
-
     <Graphics RelX="-1.0" RelY="1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
+
     <Graphics RelX="1.0" RelY="-1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
-
    <Xref Database="" ID="" />
+
-
  </State>
+
-
  <State GraphRef="edf85" TextLabel="S262" GraphId="c8d34">
+
-
    <Graphics RelX="-1.0" RelY="-0.9421044892581895" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
+
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 1,919: Line 1,915:
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
-
   <State GraphRef="edf85" TextLabel="S279" GraphId="ba895">
+
   <State GraphRef="edf85" TextLabel="S262" GraphId="c8d34">
-
     <Graphics RelX="1.0" RelY="-1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
+
     <Graphics RelX="-1.0" RelY="-0.9421044892581895" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 +
    <Xref Database="" ID="" />
 +
  </State>
 +
  <State GraphRef="edf85" TextLabel="S368" GraphId="f96d3">
 +
    <Graphics RelX="-1.0" RelY="1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 2,022: Line 2,022:
   <State GraphRef="c94a6" TextLabel="S665" GraphId="f7511">
   <State GraphRef="c94a6" TextLabel="S665" GraphId="f7511">
     <Graphics RelX="-0.5238640265531053" RelY="1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="-0.5238640265531053" RelY="1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
-
    <Xref Database="" ID="" />
 
-
  </State>
 
-
  <State GraphRef="a761a" TextLabel="S252" GraphId="fc520">
 
-
    <Graphics RelX="-1.0" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="a761a" TextLabel="S268" GraphId="fc12f">
   <State GraphRef="a761a" TextLabel="S268" GraphId="fc12f">
     <Graphics RelX="1.0" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="1.0" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 +
    <Xref Database="" ID="" />
 +
  </State>
 +
  <State GraphRef="a761a" TextLabel="S252" GraphId="fc520">
 +
    <Graphics RelX="-1.0" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="a249d" TextLabel="S453" GraphId="b44c7">
   <State GraphRef="a249d" TextLabel="S453" GraphId="b44c7">
     <Graphics RelX="1.0" RelY="1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="1.0" RelY="1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
-
    <Xref Database="" ID="" />
 
-
  </State>
 
-
  <State GraphRef="bff25" TextLabel="S218" GraphId="de879">
 
-
    <Graphics RelX="-1.0" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="bff25" TextLabel="S222" GraphId="aac3d">
   <State GraphRef="bff25" TextLabel="S222" GraphId="aac3d">
     <Graphics RelX="1.0" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="1.0" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 +
    <Xref Database="" ID="" />
 +
  </State>
 +
  <State GraphRef="bff25" TextLabel="S218" GraphId="de879">
 +
    <Graphics RelX="-1.0" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 2,070: Line 2,070:
   <State GraphRef="babe9" TextLabel="Y1214" GraphId="e4c3a">
   <State GraphRef="babe9" TextLabel="Y1214" GraphId="e4c3a">
     <Graphics RelX="1.0" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="1.0" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
-
    <Xref Database="" ID="" />
 
-
  </State>
 
-
  <State GraphRef="fe519" TextLabel="Y416" GraphId="ee83f">
 
-
    <Graphics RelX="-1.0" RelY="-1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="fe519" TextLabel="Y527" GraphId="cb827">
   <State GraphRef="fe519" TextLabel="Y527" GraphId="cb827">
     <Graphics RelX="1.0" RelY="-1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="1.0" RelY="-1.0" Width="30.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 +
    <Xref Database="" ID="" />
 +
  </State>
 +
  <State GraphRef="fe519" TextLabel="Y416" GraphId="ee83f">
 +
    <Graphics RelX="-1.0" RelY="-1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 2,150: Line 2,150:
   <State GraphRef="f19a0" TextLabel="S197" GraphId="a251d">
   <State GraphRef="f19a0" TextLabel="S197" GraphId="a251d">
     <Graphics RelX="-0.5185185185185185" RelY="1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="-0.5185185185185185" RelY="1.0" Width="32.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
-
    <Xref Database="" ID="" />
 
-
  </State>
 
-
  <State GraphRef="d214e" TextLabel="S490" GraphId="bb5ab">
 
-
    <Graphics RelX="-1.0" RelY="1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="d214e" TextLabel="Ub" GraphId="af2cd">
   <State GraphRef="d214e" TextLabel="Ub" GraphId="af2cd">
     <Graphics RelX="1.0" RelY="1.0" Width="20.0" Height="15.0" FillColor="cc6600" ShapeType="Oval" />
     <Graphics RelX="1.0" RelY="1.0" Width="20.0" Height="15.0" FillColor="cc6600" ShapeType="Oval" />
 +
    <Xref Database="" ID="" />
 +
  </State>
 +
  <State GraphRef="d214e" TextLabel="S490" GraphId="bb5ab">
 +
    <Graphics RelX="-1.0" RelY="1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="c3ca9" TextLabel="S194" GraphId="a112b">
   <State GraphRef="c3ca9" TextLabel="S194" GraphId="a112b">
     <Graphics RelX="-0.804373725394762" RelY="1.0" Width="37.33125816785014" Height="15.743090401308095" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="-0.804373725394762" RelY="1.0" Width="37.33125816785014" Height="15.743090401308095" FillColor="ffff00" ShapeType="RoundedRectangle" />
-
    <Xref Database="" ID="" />
 
-
  </State>
 
-
  <State GraphRef="c3ca9" TextLabel="S397" GraphId="e5f07">
 
-
    <Graphics RelX="0.72" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="c3ca9" TextLabel="S479" GraphId="b073c">
   <State GraphRef="c3ca9" TextLabel="S479" GraphId="b073c">
     <Graphics RelX="0.68" RelY="1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="0.68" RelY="1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 +
    <Xref Database="" ID="" />
 +
  </State>
 +
  <State GraphRef="c3ca9" TextLabel="S397" GraphId="e5f07">
 +
    <Graphics RelX="0.72" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="e6329" TextLabel="K1147" GraphId="c80ff">
   <State GraphRef="e6329" TextLabel="K1147" GraphId="c80ff">
     <Graphics RelX="-1.0" RelY="1.0" Width="40.0" Height="15.0" FillColor="cc6600" ShapeType="RoundedRectangle" />
     <Graphics RelX="-1.0" RelY="1.0" Width="40.0" Height="15.0" FillColor="cc6600" ShapeType="RoundedRectangle" />
-
    <Xref Database="" ID="" />
 
-
  </State>
 
-
  <State GraphRef="ddb85" TextLabel="S194" GraphId="db4aa">
 
-
    <Graphics RelX="1.0" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 2,188: Line 2,184:
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
-
   <State GraphRef="d926e" TextLabel="S245" GraphId="f5006">
+
   <State GraphRef="ddb85" TextLabel="S194" GraphId="db4aa">
-
     <Graphics RelX="-0.43333333333333335" RelY="1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
+
     <Graphics RelX="1.0" RelY="-1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 2,196: Line 2,192:
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
-
   <State GraphRef="b0a3d" TextLabel="S 246" GraphId="f5f60">
+
   <State GraphRef="d926e" TextLabel="S245" GraphId="f5006">
-
     <Graphics RelX="-0.5" RelY="0.9199852568062687" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
+
     <Graphics RelX="-0.43333333333333335" RelY="1.0" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
   <State GraphRef="b0a3d" TextLabel="S467" GraphId="b5ae3">
   <State GraphRef="b0a3d" TextLabel="S467" GraphId="b5ae3">
     <Graphics RelX="1.0" RelY="0.9199852568062687" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Graphics RelX="1.0" RelY="0.9199852568062687" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
 +
    <Xref Database="" ID="" />
 +
  </State>
 +
  <State GraphRef="b0a3d" TextLabel="S 246" GraphId="f5f60">
 +
    <Graphics RelX="-0.5" RelY="0.9199852568062687" Width="35.0" Height="15.0" FillColor="ffff00" ShapeType="RoundedRectangle" />
     <Xref Database="" ID="" />
     <Xref Database="" ID="" />
   </State>
   </State>
Line 2,214: Line 2,214:
   <State GraphRef="bdafd" TextLabel="P" GraphId="b0e29">
   <State GraphRef="bdafd" TextLabel="P" GraphId="b0e29">
     <Graphics RelX="-1.0" RelY="1.0" Width="15.0" Height="15.0" FillColor="ffff00" ShapeType="Oval" />
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">The angiogenic function of nucleolin is mediated by vascular endothelial growth factor and nonmuscle myosin.</bp:TITLE>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Connective tissue growth factor binds vascular endothelial growth factor (VEGF) and inhibits VEGF-induced angiogenesis.</bp:TITLE>
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       <bp:SOURCE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Blood</bp:SOURCE>
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       <bp:YEAR rdf:datatype="http://www.w3.org/2001/XMLSchema#string">2006</bp:YEAR>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Huang Y</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Inoki I</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Shi H</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Shiomi T</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Zhou H</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Song X</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Enomoto H</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Yuan S</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Luo Y</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Makino K</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Ikeda E</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Takata S</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Kobayashi K</bp:AUTHORS>
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      <bp:DB rdf:datatype="http://www.w3.org/2001/XMLSchema#string">PubMed</bp:DB>
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     <bp:PublicationXref xmlns:bp="http://www.biopax.org/release/biopax-level3.owl#" xmlns:rdf="http://www.w3.org/1999/02/22-rdf-syntax-ns#" rdf:id="a72">
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       <bp:ID rdf:datatype="http://www.w3.org/2001/XMLSchema#string">15920022</bp:ID>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">New role for the protein tyrosine phosphatase DEP-1 in Akt activation and endothelial cell survival.</bp:TITLE>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Angiopoietin-1 opposes VEGF-induced increase in endothelial permeability by inhibiting TRPC1-dependent Ca2 influx.</bp:TITLE>
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      <bp:DB rdf:datatype="http://www.w3.org/2001/XMLSchema#string">PubMed</bp:DB>
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       <bp:SOURCE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Mol Cell Biol</bp:SOURCE>
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     <bp:PublicationXref xmlns:bp="http://www.biopax.org/release/biopax-level3.owl#" xmlns:rdf="http://www.w3.org/1999/02/22-rdf-syntax-ns#" rdf:id="bb1">
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Growth factor stimulation induces cell survival by c-Jun. ATF2-dependent activation of Bcl-XL.</bp:TITLE>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Regulation of VEGF-induced endothelial cell migration by mitochondrial reactive oxygen species.</bp:TITLE>
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     <bp:PublicationXref xmlns:bp="http://www.biopax.org/release/biopax-level3.owl#" xmlns:rdf="http://www.w3.org/1999/02/22-rdf-syntax-ns#" rdf:id="f44">
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      <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Glypican-1 is a VEGF165 binding proteoglycan that acts as an extracellular chaperone for VEGF165.</bp:TITLE>
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      <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">New role for the protein tyrosine phosphatase DEP-1 in Akt activation and endothelial cell survival.</bp:TITLE>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">IQGAP1-dependent signaling pathway regulates endothelial cell proliferation and angiogenesis.</bp:TITLE>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Nck and Crk mediate distinct VEGF-induced signaling pathways that serve overlapping functions in focal adhesion turnover and integrin activation.</bp:TITLE>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">IQGAP1-dependent signaling pathway regulates endothelial cell proliferation and angiogenesis.</bp:TITLE>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Nck and Crk mediate distinct VEGF-induced signaling pathways that serve overlapping functions in focal adhesion turnover and integrin activation.</bp:TITLE>
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       <bp:SOURCE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">PLoS One</bp:SOURCE>
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       <bp:SOURCE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Exp Cell Res</bp:SOURCE>
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      <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Nck and Crk mediate distinct VEGF-induced signaling pathways that serve overlapping functions in focal adhesion turnover and integrin activation.</bp:TITLE>
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      <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Nck and Crk mediate distinct VEGF-induced signaling pathways that serve overlapping functions in focal adhesion turnover and integrin activation.</bp:TITLE>
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      <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Nck and Crk mediate distinct VEGF-induced signaling pathways that serve overlapping functions in focal adhesion turnover and integrin activation.</bp:TITLE>
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      <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Signal transduction by vascular endothelial growth factor receptors.</bp:TITLE>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Gale D</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">White GC 2nd</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Vansluys J</bp:AUTHORS>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases.</bp:TITLE>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Ligand-stimulated VEGFR2 signaling is regulated by co-ordinated trafficking and proteolysis.</bp:TITLE>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">VEGF-induced activation of phosphoinositide 3-kinase is dependent on focal adhesion kinase.</bp:TITLE>
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       <bp:SOURCE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Traffic</bp:SOURCE>
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       <bp:SOURCE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Exp Cell Res</bp:SOURCE>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Bruns AF</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Qi JH</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Herbert SP</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Odell AF</bp:AUTHORS>
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       <bp:AUTHORS rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Jopling HM</bp:AUTHORS>
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    <bp:PublicationXref xmlns:bp="http://www.biopax.org/release/biopax-level3.owl#" xmlns:rdf="http://www.w3.org/1999/02/22-rdf-syntax-ns#" rdf:id="ae7">
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      <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">VEGF binding to NRP1 is essential for VEGF stimulation of endothelial cell migration, complex formation between NRP1 and VEGFR2, and signaling via FAK Tyr407 phosphorylation.</bp:TITLE>
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      <bp:SOURCE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Mol Biol Cell</bp:SOURCE>
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      <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">VEGF binding to NRP1 is essential for VEGF stimulation of endothelial cell migration, complex formation between NRP1 and VEGFR2, and signaling via FAK Tyr407 phosphorylation.</bp:TITLE>
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      <bp:SOURCE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Mol Biol Cell</bp:SOURCE>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">Inhibition of Rho-dependent kinases ROCK I/II activates VEGF-driven retinal neovascularization and sprouting angiogenesis.</bp:TITLE>
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       <bp:TITLE rdf:datatype="http://www.w3.org/2001/XMLSchema#string">The novel Src kinase inhibitor M475271 inhibits VEGF-induced vascular endothelial-cadherin and beta-catenin phosphorylation but increases their association.</bp:TITLE>
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