Orai1 function is essential for T cell homing to lymph nodes

J Immunol. 2013 Apr 1;190(7):3197-206. doi: 10.4049/jimmunol.1202212. Epub 2013 Mar 1.

Abstract

In T lymphocytes, Ca(2+) release-activated Ca(2+) (CRAC) channels composed of Orai1 subunits trigger Ag-induced gene expression and cell proliferation through the NFAT pathway. We evaluated the requirement of CRAC channel function for lymphocyte homing using expression of a dominant-negative Orai1-E106A mutant to suppress Ca(2+) signaling. To investigate homing and motility of human lymphocytes in immunocompromised mouse hosts, we transferred human lymphocytes either acutely or after stable engraftment after a second transfer from the same blood donor. Human and mouse lymphocyte homing was assessed, and cells were tracked within lymph nodes (LNs) by two-photon microscopy. Our results demonstrate that human T and B lymphocytes home into and migrate within the LNs of immunocompromised NOD.SCID mice similar to murine lymphocytes. Human T and B cells colocalized in atrophied or reconstituted mouse LNs, where T cells migrated in a random walk at velocities of 9-13 μm/min and B cells at 6 μm/min. Expression of Orai1-E106A inhibited CRAC channel function in human and mouse T cells, and prevented homing from high endothelial venules into murine LNs. Ca(2+) signals induced by CCL21 were also inhibited in T cells expressing Orai1-E106A. With CRAC channels inhibited, the high-affinity form of LFA-1 failed to become active, and T cells failed to migrate across endothelial cells in a transwell model. These results establish a requirement for CRAC channel-mediated Ca(2+) influx for T cell homing to LNs mediated by high-affinity integrin activation and chemokine-induced transendothelial migration.

Publication types

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

MeSH terms

  • Animals
  • Calcium Channels / genetics
  • Calcium Channels / metabolism*
  • Calcium Signaling
  • Cell Movement / immunology
  • Cell Tracking
  • Chemokine CCL21 / metabolism
  • Humans
  • Immunocompromised Host
  • Lymph Nodes / immunology*
  • Lymph Nodes / metabolism*
  • Lymphocyte Function-Associated Antigen-1 / metabolism
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Mutation
  • ORAI1 Protein
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism*

Substances

  • Calcium Channels
  • Chemokine CCL21
  • Lymphocyte Function-Associated Antigen-1
  • ORAI1 Protein
  • Orai1 protein, mouse