Ezrin-radixin-moesin-binding sequence of PSGL-1 glycoprotein regulates leukocyte rolling on selectins and activation of extracellular signal-regulated kinases

J Biol Chem. 2012 Mar 23;287(13):10693-10702. doi: 10.1074/jbc.M111.318022. Epub 2012 Feb 6.

Abstract

P-selectin glycoprotein ligand-1 (PSGL-1) mediates the capture (tethering) of free-flowing leukocytes and subsequent rolling on selectins. PSGL-1 interactions with endothelial selectins activate Src kinases and spleen tyrosine kinase (Syk), leading to α(L)β(2) integrin-dependent leukocyte slow rolling, which promotes leukocyte recruitment into tissues. In addition, but through a distinct pathway, PSGL-1 engagement activates ERK. Because ezrin, radixin and moesin proteins (ERMs) link PSGL-1 to actin cytoskeleton and because they serve as adaptor molecules between PSGL-1 and Syk, we examined the role of PSGL-1 ERM-binding sequence (EBS) on cell capture, rolling, and signaling through Syk and MAPK pathways. We carried out mutational analysis and observed that deletion of EBS severely reduced 32D leukocyte tethering and rolling on L-, P-, and E-selectin and slightly increased rolling velocity. Alanine substitution of Arg-337 and Lys-338 showed that these residues play a key role in supporting leukocyte tethering and rolling on selectins. Importantly, EBS deletion or Arg-337 and Lys-338 mutations abrogated PSGL-1-induced ERK activation, whereas they did not prevent Syk phosphorylation or E-selectin-induced leukocyte slow rolling. These studies demonstrate that PSGL-1 EBS plays a critical role in recruiting leukocytes on selectins and in activating the MAPK pathway, whereas it is dispensable to phosphorylate Syk and to lead to α(L)β(2)-dependent leukocyte slow rolling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CHO Cells
  • Cell Line
  • Cricetinae
  • Cricetulus
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism
  • Enzyme Activation / physiology
  • Extracellular Signal-Regulated MAP Kinases / genetics
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Leukocyte Rolling / physiology*
  • Leukocytes / cytology
  • Leukocytes / metabolism*
  • Lymphocyte Function-Associated Antigen-1 / genetics
  • Lymphocyte Function-Associated Antigen-1 / metabolism
  • MAP Kinase Signaling System / physiology*
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism
  • Phosphorylation / physiology
  • Protein-Tyrosine Kinases / genetics
  • Protein-Tyrosine Kinases / metabolism
  • Selectins / genetics
  • Selectins / metabolism*
  • Sequence Deletion
  • Syk Kinase
  • src-Family Kinases / genetics
  • src-Family Kinases / metabolism

Substances

  • Cytoskeletal Proteins
  • Intracellular Signaling Peptides and Proteins
  • Lymphocyte Function-Associated Antigen-1
  • Membrane Glycoproteins
  • Membrane Proteins
  • Microfilament Proteins
  • P-selectin ligand protein
  • Selectins
  • ezrin
  • moesin
  • radixin
  • Protein-Tyrosine Kinases
  • SYK protein, human
  • Syk Kinase
  • src-Family Kinases
  • Extracellular Signal-Regulated MAP Kinases