Heparan sulfates are critical regulators of the inhibitory megakaryocyte-platelet receptor G6b-B

Elife. 2019 Aug 22:8:e46840. doi: 10.7554/eLife.46840.

Abstract

The immunoreceptor tyrosine-based inhibition motif (ITIM)-containing receptor G6b-B is critical for platelet production and activation. Loss of G6b-B results in severe macrothrombocytopenia, myelofibrosis and aberrant platelet function in mice and humans. Using a combination of immunohistochemistry, affinity chromatography and proteomics, we identified the extracellular matrix heparan sulfate (HS) proteoglycan perlecan as a G6b-B binding partner. Subsequent in vitro biochemical studies and a cell-based genetic screen demonstrated that the interaction is specifically mediated by the HS chains of perlecan. Biophysical analysis revealed that heparin forms a high-affinity complex with G6b-B and mediates dimerization. Using platelets from humans and genetically modified mice, we demonstrate that binding of G6b-B to HS and multivalent heparin inhibits platelet and megakaryocyte function by inducing downstream signaling via the tyrosine phosphatases Shp1 and Shp2. Our findings provide novel insights into how G6b-B is regulated and contribute to our understanding of the interaction of megakaryocytes and platelets with glycans.

Keywords: G6b-B; ITIM-receptor; biochemistry; cell biology; chemical biology; heparan sulfate; heparin; human; mouse; perlecan; platelets.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Platelets / physiology*
  • Heparitin Sulfate / metabolism*
  • Humans
  • Megakaryocytes / physiology*
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Protein Binding
  • Protein Multimerization
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / metabolism
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6 / metabolism
  • Receptors, Immunologic / deficiency
  • Receptors, Immunologic / genetics
  • Receptors, Immunologic / metabolism*
  • Signal Transduction

Substances

  • G6b-B receptor, mouse
  • MPIG6B protein, human
  • Receptors, Immunologic
  • Heparitin Sulfate
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6

Associated data

  • PDB/6R0X
  • PDB/4R9W
  • PDB/4RDA
  • PDB/2VRA
  • PDB/1E0O
  • PDB/1FQ9