M-sec regulates polarized secretion of inflammatory endothelial chemokines and facilitates CCL2-mediated lymphocyte transendothelial migration

J Leukoc Biol. 2016 Jun;99(6):1045-55. doi: 10.1189/jlb.3VMA0915-427R. Epub 2015 Dec 23.

Abstract

Activation of endothelial cells by IL-1β triggers the expression of multiple inflammatory cytokines and leukocyte-attracting chemokines. The machineries involved in the secretion of these inducible proteins are poorly understood. With the use of genome-wide transcriptional analysis of inflamed human dermal microvascular endothelial cells, we identified several IL-1β-induced candidate regulators of these machineries and chose to focus our study on TNF-α-induced protein 2 (myeloid-secretory). The silencing of myeloid-secretory did not affect the ability of inflamed endothelial cells to support the adhesion and crawling of effector T lymphocytes. However, the ability of these lymphocytes to complete transendothelial migration across myeloid-secretory-silenced human dermal microvascular endothelial cells was inhibited significantly. These observed effects on lymphocyte transendothelial migration were recovered completely when exogenous promigratory chemokine CXCL12 was overlaid on the endothelial barrier. A polarized secretion assay suggested that the silencing of endothelial myeloid-secretory impairs T effector transendothelial migration by reducing the preferential secretion of endothelial-produced CCL2, a key transendothelial migration-promoting chemokine for these lymphocytes, into the basolateral endothelial compartment. Myeloid-secretory silencing also impaired the preferential secretion of other endothelial-produced inflammatory chemokines, as well as cytokines, such as IL-6 and GM-CSF, into the basolateral endothelial compartment. This is the first evidence of a novel inflammation-inducible machinery that regulates polarized secretion of endothelial CCL2 and other inflammatory chemokines and cytokines into basolateral endothelial compartments and facilitates the ability of endothelial CCL2 to promote T cell transendothelial migration.

Keywords: cytokines; endothelial cells; inflammation; leukocyte trafficking.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism
  • Cell Polarity* / drug effects
  • Chemokine CCL2 / metabolism*
  • Cytokines / metabolism*
  • Dermis / cytology
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism*
  • Gene Expression Profiling
  • Gene Expression Regulation / drug effects
  • Gene Silencing / drug effects
  • Genetic Association Studies
  • Humans
  • Inflammation / metabolism
  • Inflammation / pathology*
  • Interleukin-1beta / pharmacology
  • Lymphocytes / cytology*
  • Microvessels / cytology
  • Protein Interaction Mapping
  • Transcription, Genetic / drug effects
  • Transendothelial and Transepithelial Migration* / drug effects
  • Vascular Endothelial Growth Factor A / pharmacology

Substances

  • Actins
  • Chemokine CCL2
  • Cytokines
  • Interleukin-1beta
  • TNFAIP2 protein, human
  • Vascular Endothelial Growth Factor A