How the Parasitic Bacterium Legionella Pneumophila Modifies Its Phagosome and Transforms It Into Rough ER: Implications for Conversion of Plasma Membrane to the ER Membrane

J Cell Sci. 2001 Dec;114(Pt 24):4637-50.

Abstract

Within five minutes of macrophage infection by Legionella pneumophila, the bacterium responsible for Legionnaires' disease, elements of the rough endoplasmic reticulum (RER) and mitochondria attach to the surface of the bacteria-enclosed phagosome. Connecting these abutting membranes are tiny hairs, which are frequently periodic like the rungs of a ladder. These connections are stable and of high affinity - phagosomes from infected macrophages remain connected to the ER and mitochondria (as they were in situ) even after infected macrophages are homogenized. Thin sections through the plasma and phagosomal membranes show that the phagosomal membrane is thicker (72+/-2 A) than the ER and mitochondrial membranes (60+/-2 A), presumably owing to the lack of cholesterol, sphingolipids and glycolipids in the ER. Interestingly, within 15 minutes of infection, the phagosomal membrane changes thickness to resemble that of the attached ER vesicles. Only later (e.g. after six hours) does the ER-phagosome association become less frequent. Instead ribosomes stud the former phagosomal membrane and L. pneumophila reside directly in the rough ER. Examination of phagosomes of various L. pneumophila mutants suggests that this membrane conversion is a four-stage process used by L. pneumophila to establish itself in the RER and to survive intracellularly. But what is particularly interesting is that L. pneumophila is exploiting a poorly characterized naturally occurring cellular process.

Publication types

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

MeSH terms

  • Bacterial Proteins / physiology
  • Carrier Proteins / genetics
  • Carrier Proteins / physiology
  • Cell Fractionation
  • Cell Membrane / genetics
  • Cell Membrane / microbiology
  • Cell Membrane / physiology
  • Cell Membrane / ultrastructure
  • Gram-Positive Bacteria / pathogenicity
  • Gram-Positive Bacteria / physiology
  • Gram-Positive Bacteria / ultrastructure
  • Humans
  • Intracellular Membranes / microbiology*
  • Intracellular Membranes / physiology*
  • Intracellular Membranes / ultrastructure
  • Legionella pneumophila / genetics
  • Legionella pneumophila / physiology*
  • Legionella pneumophila / ultrastructure*
  • Lipid Metabolism
  • Lysosomes / physiology
  • Membrane Proteins / genetics
  • Membrane Proteins / physiology
  • Microscopy, Electron
  • Mitochondria / genetics
  • Mitochondria / microbiology
  • Mitochondria / physiology
  • Mitochondria / ultrastructure
  • Molecular Chaperones / genetics
  • Molecular Chaperones / physiology
  • Mutation
  • Organelles
  • Phagosomes / genetics
  • Phagosomes / microbiology*
  • Phagosomes / physiology*
  • Phagosomes / ultrastructure
  • Ribosomes / physiology
  • Time Factors
  • U937 Cells / microbiology
  • U937 Cells / physiology
  • U937 Cells / ultrastructure

Substances

  • Bacterial Proteins
  • Carrier Proteins
  • DotA protein, Legionella pneumophila
  • IcmR protein, Legionella pneumophila
  • Membrane Proteins
  • Molecular Chaperones