Triggering receptor expressed on myeloid cells 1 (TREM-1)-mediated Bcl-2 induction prolongs macrophage survival

J Biol Chem. 2014 May 23;289(21):15118-29. doi: 10.1074/jbc.M113.536490. Epub 2014 Apr 7.

Abstract

Triggering receptor expressed on myeloid cells 1 (TREM-1) is a superimmunoglobulin receptor expressed on myeloid cells that plays an important role in the amplification of inflammation. Recent studies suggest a role for TREM-1 in tumor-associated macrophages with relationship to tumor growth and progression. Whether the effects of TREM-1 on inflammation and tumor growth are mediated by an alteration in cell survival signaling is not known. In these studies, we show that TREM-1 knock-out macrophages exhibit an increase in apoptosis of cells in response to lipopolysaccharide (LPS) suggesting a role for TREM-1 in macrophage survival. Specific ligation of TREM-1 with monoclonal TREM-1 (mTREM-1) or overexpression of TREM-1 with adeno-TREM-1 induced B-cell lymphoma-2 (Bcl-2) with depletion of the key executioner caspase-3 prevents the cleavage of poly(ADP-ribose) polymerase. TREM-1 knock-out cells showed lack of induction of Bcl2 with an increase in caspase-3 activation in response to lipopolysaccharide. In addition overexpression of TREM-1 with adeno-TREM-1 led to an increase in mitofusins (MFN1 and MFN2) and knockdown of TREM-1 decreased the expression of mitofusins suggesting that TREM-1 contributes to the maintenance of mitochondrial integrity favoring cell survival. Investigations into potential mechanisms by which TREM-1 alters cell survival showed that TREM-1-induced Bcl-2 in an Egr2-dependent manner. Furthermore, our data shows that expression of Egr2 in response to specific ligation of TREM-1 is ERK mediated. These data for the first time provide novel mechanistic insights into the role of TREM-1 as an anti-apoptotic protein that prolongs macrophage survival.

Keywords: Cell Death; Inflammation; Lipopolysaccharide (LPS); Macrophage; Macrophages; Tumor.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism
  • Blotting, Western
  • Caspase 3 / metabolism
  • Cell Line
  • Cell Survival / genetics
  • Cells, Cultured
  • Early Growth Response Protein 2 / genetics
  • Early Growth Response Protein 2 / metabolism
  • Enzyme Inhibitors / pharmacology
  • Flow Cytometry
  • Gene Expression Profiling
  • Humans
  • MAP Kinase Kinase 1 / antagonists & inhibitors
  • MAP Kinase Kinase 1 / metabolism
  • Macrophages / cytology
  • Macrophages / metabolism*
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Oligonucleotide Array Sequence Analysis
  • Poly(ADP-ribose) Polymerases / metabolism
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Proto-Oncogene Proteins c-bcl-2 / metabolism*
  • RNA Interference
  • Receptors, Immunologic / genetics
  • Receptors, Immunologic / metabolism*
  • Triggering Receptor Expressed on Myeloid Cells-1

Substances

  • Apoptosis Regulatory Proteins
  • Early Growth Response Protein 2
  • Egr2 protein, mouse
  • Enzyme Inhibitors
  • Membrane Glycoproteins
  • Proto-Oncogene Proteins c-bcl-2
  • Receptors, Immunologic
  • TREM1 protein, mouse
  • Triggering Receptor Expressed on Myeloid Cells-1
  • Poly(ADP-ribose) Polymerases
  • MAP Kinase Kinase 1
  • Map2k1 protein, mouse
  • Caspase 3