Distinct roles for talin-1 and kindlin-3 in LFA-1 extension and affinity regulation

Blood. 2012 May 3;119(18):4275-82. doi: 10.1182/blood-2011-08-373118. Epub 2012 Mar 19.

Abstract

In inflammation, neutrophils and other leukocytes roll along the microvascular endothelium before arresting and transmigrating into inflamed tissues. Arrest requires conformational activation of the integrin lymphocyte function-associated antigen-1 (LFA-1). Mutations of the FERMT3 gene encoding kindlin-3 underlie the human immune deficiency known as leukocyte adhesion deficiency-III. Both kindlin-3 and talin-1, another FERM domain-containing cytoskeletal protein, are required for integrin activation, but their individual roles in the induction of specific integrin conformers are unclear. Here, we induce differential LFA-1 activation in neutrophils through engagement of the selectin ligand P-selectin glycoprotein ligand-1 or the chemokine receptor CXCR2. We find that talin-1 is required for inducing LFA-1 extension, which corresponds to intermediate affinity and induces neutrophil slow rolling, whereas both talin-1 and kindlin-3 are required for induction of the high-affinity conformation of LFA-1 with an open headpiece, which results in neutrophil arrest. In vivo, both slow rolling and arrest are defective in talin-1-deficient neutrophils, whereas only arrest is defective in kindlin-3-deficient neutrophils. We conclude that talin-1 and kindlin-3 serve distinct functions in LFA-1 activation.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Marrow Transplantation
  • Cell Adhesion
  • Chemotaxis, Leukocyte / physiology*
  • Cytoskeletal Proteins / antagonists & inhibitors
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / physiology*
  • Green Fluorescent Proteins / analysis
  • HL-60 Cells
  • Humans
  • Intercellular Adhesion Molecule-1 / metabolism
  • K562 Cells
  • Lymphocyte Function-Associated Antigen-1 / chemistry
  • Lymphocyte Function-Associated Antigen-1 / metabolism*
  • Membrane Proteins / antagonists & inhibitors
  • Membrane Proteins / genetics
  • Membrane Proteins / physiology
  • Mice
  • Mice, Inbred C57BL
  • Neoplasm Proteins / antagonists & inhibitors
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / physiology
  • Neutrophils / metabolism*
  • Peritonitis / chemically induced
  • Peritonitis / immunology
  • Peritonitis / metabolism
  • Protein Binding
  • Protein Conformation
  • RNA Interference
  • RNA, Small Interfering / pharmacology
  • Radiation Chimera
  • Specific Pathogen-Free Organisms
  • Talin / antagonists & inhibitors
  • Talin / genetics
  • Talin / physiology*

Substances

  • Cytoskeletal Proteins
  • FERMT3 protein, human
  • Icam1 protein, mouse
  • Lymphocyte Function-Associated Antigen-1
  • Membrane Proteins
  • Neoplasm Proteins
  • RNA, Small Interfering
  • TLN1 protein, human
  • Talin
  • kindlin-3 protein, mouse
  • Tln1 protein, mouse
  • Intercellular Adhesion Molecule-1
  • Green Fluorescent Proteins