Binding of CIB1 to the αIIb tail of αIIbβ3 is required for FAK recruitment and activation in platelets

PLoS One. 2017 May 24;12(5):e0176602. doi: 10.1371/journal.pone.0176602. eCollection 2017.

Abstract

Background: It is believed that activation of c-Src bound to the integrin β3 subunit initiates outside-in signaling. The involvement of αIIb in outside-in signaling is poorly understood.

Objectives: We have previously shown that CIB1 specifically interacts with the cytoplasmic domain of αIIb and is required for αIIbβ3 outside-in signaling. Here we evaluated the role of CIB1 in regulating outside-in signaling in the absence of inside-out signaling.

Methods: We used αIIb cytoplasmic domain peptide and CIB1-function blocking antibody to inhibit interaction of CIB1 with αIIb subunit as well as Cib1-/- platelets to evaluate the consequence of CIB1 interaction with αIIb on outside-in signaling.

Results: Fibrinogen binding to αIIbβ3 results in calcium-dependent interaction of CIB1 with αIIb, which is not required for filopodia formation. Dynamic rearrangement of cytoskeleton results in CIB1-dependent recruitment of FAK to the αIIb complex and its activation. Disruption of the association of CIB1 and αIIb by incorporation of αIIb peptide or anti-CIB1 inhibited both FAK association and activation. Furthermore, FAK recruitment to the integrin complex was required for c-Src activation. Inhibition of c-Src had no effect on CIB1 accumulation with the integrin at the filopodia, suggesting that c-Src activity is not required for the formation of CIB1-αIIb-FAK complex.

Conclusion: Our results suggest that interaction of CIB1 with αIIb is one of the early events occurring during outside-in signaling. Furthermore, CIB1 recruits FAK to the αIIbβ3 complex at the filopodia where FAK is activated, which in turn activates c-Src, resulting in propagation of outside-in signaling leading to platelet spreading.

MeSH terms

  • Animals
  • Blood Platelets / cytology
  • Blood Platelets / metabolism*
  • Blotting, Western
  • CSK Tyrosine-Protein Kinase
  • Calcium-Binding Proteins / genetics
  • Calcium-Binding Proteins / metabolism*
  • Cytoskeleton / metabolism
  • Enzyme Activation
  • Fluorescent Antibody Technique
  • Focal Adhesion Kinase 1 / metabolism*
  • Humans
  • Immunoprecipitation
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Fluorescence
  • Platelet Activation
  • Platelet Glycoprotein GPIIb-IIIa Complex / metabolism*
  • Platelet Membrane Glycoprotein IIb / metabolism*
  • Protein Binding
  • Pseudopodia / metabolism
  • Signal Transduction
  • src-Family Kinases / metabolism

Substances

  • CIB1 protein, human
  • Calcium-Binding Proteins
  • Cib1 protein, mouse
  • Platelet Glycoprotein GPIIb-IIIa Complex
  • Platelet Membrane Glycoprotein IIb
  • CSK Tyrosine-Protein Kinase
  • Focal Adhesion Kinase 1
  • PTK2 protein, human
  • Ptk2 protein, mouse
  • src-Family Kinases
  • CSK protein, human