Phagocytosis-induced apoptosis in macrophages is mediated by up-regulation and activation of the Bcl-2 homology domain 3-only protein Bim

J Immunol. 2005 Jan 15;174(2):671-9. doi: 10.4049/jimmunol.174.2.671.

Abstract

Cell death by apoptosis is important in immune cell homeostasis and in the defense against infectious microorganisms. The physiological event of uptake and intracellular destruction of bacteria is a powerful apoptotic stimulus to macrophages and neutrophil granulocytes. In this study, we provide a molecular analysis of phagocytosis-induced apoptosis. Apoptosis was blocked by Bcl-2 in a mouse macrophage cell line and in primary mouse macrophages. Analysis of the upstream mechanisms revealed that apoptosis was triggered by the Bcl-2 homology domain 3-only protein Bim/Bod. Contact with bacteria or bacterial components induced a strong increase in Bim-expression through TLR and MyD88. Inhibition of the MAPK p38 and JNK reduced both up-regulation of Bim and apoptosis. Phosphorylation of Bim was further observed in mouse macrophages, which appeared to be the result of TLR-dependent phosphatase inhibition. Although TLR-induced Bim was, unlike Bim in resting cells, not bound to the microtubuli cytoskeleton, the up-regulation of Bim was not sufficient to cause apoptosis. A second signal was required that was generated in the process of phagocytosis. Phagocytosis-induced apoptosis was strongly reduced in Bim(-/-) macrophages. These data provide the molecular context of a form of apoptosis that may serve to dispose of terminally differentiated phagocytes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Antigens, Differentiation / physiology
  • Apoptosis / genetics
  • Apoptosis / immunology*
  • Apoptosis Regulatory Proteins
  • BH3 Interacting Domain Death Agonist Protein
  • Bcl-2-Like Protein 11
  • Carrier Proteins / biosynthesis
  • Carrier Proteins / metabolism
  • Carrier Proteins / physiology*
  • Cell Line
  • Granulocytes / cytology
  • Granulocytes / immunology
  • Granulocytes / metabolism
  • JNK Mitogen-Activated Protein Kinases / physiology
  • Macrophage Activation / immunology*
  • Macrophages / cytology
  • Macrophages / immunology
  • Macrophages / metabolism*
  • Macrophages / microbiology
  • Membrane Glycoproteins / physiology
  • Membrane Proteins / biosynthesis
  • Membrane Proteins / deficiency
  • Membrane Proteins / metabolism
  • Membrane Proteins / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Myeloid Differentiation Factor 88
  • Phagocytosis / genetics
  • Phagocytosis / immunology*
  • Phosphorylation
  • Protein Isoforms / metabolism
  • Proto-Oncogene Proteins / biosynthesis
  • Proto-Oncogene Proteins / deficiency
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins / physiology*
  • Proto-Oncogene Proteins c-bcl-2 / metabolism*
  • Receptors, Cell Surface / physiology
  • Receptors, Immunologic / physiology
  • Structural Homology, Protein
  • Toll-Like Receptors
  • Up-Regulation / genetics
  • Up-Regulation / immunology*
  • p38 Mitogen-Activated Protein Kinases / physiology

Substances

  • Adaptor Proteins, Signal Transducing
  • Antigens, Differentiation
  • Apoptosis Regulatory Proteins
  • BH3 Interacting Domain Death Agonist Protein
  • Bcl-2-Like Protein 11
  • Bcl2l11 protein, mouse
  • Bid protein, mouse
  • Carrier Proteins
  • Membrane Glycoproteins
  • Membrane Proteins
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Protein Isoforms
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • Receptors, Cell Surface
  • Receptors, Immunologic
  • Toll-Like Receptors
  • JNK Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases