Activation of hypoxia-inducible factor-1 in bacillary angiomatosis: evidence for a role of hypoxia-inducible factor-1 in bacterial infections

Circulation. 2005 Mar 1;111(8):1054-62. doi: 10.1161/01.CIR.0000155608.07691.B7. Epub 2005 Feb 21.

Abstract

Background: Bartonella species are the only known bacterial pathogens causing vasculoproliferative disorders in humans (bacillary angiomatosis [BA]). Cellular and bacterial pathogenetic mechanisms underlying the induction of BA are largely unknown.

Methods and results: Activation of hypoxia-inducible factor-1 (HIF-1), the key transcription factor involved in angiogenesis, was detected in Bartonella henselae-infected host cells in vitro by immunofluorescence, Western blotting, electrophoretic mobility shift, and reporter gene assays and by immunohistochemistry in BA tissue lesions in vivo. Gene microarray analysis revealed that a B henselae infection resulted in the activation of genes typical for the cellular response to hypoxia. HIF-1 was essential for B henselae-induced expression of vascular endothelial growth factor as shown by inhibition with the use of HIF-1-specific short-interfering RNA. Moreover, infection with B henselae resulted in increased oxygen consumption, cellular hypoxia, and decreased ATP levels in host cells. Infection with a pilus-negative variant of B henselae did not lead to cellular hypoxia or activation of HIF-1 or vascular endothelial growth factor secretion, suggesting a crucial role of this bacterial surface protein in the angiogenic reprogramming of the host cells.

Conclusions: B henselae induces a proangiogenic host cell response via HIF-1. Our data provide for the first time evidence that HIF-1 may play a role in bacterial infections.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Angiomatosis, Bacillary / pathology*
  • Bartonella henselae / isolation & purification
  • Bartonella henselae / pathogenicity
  • Cell Hypoxia / physiology
  • DNA-Binding Proteins / immunology
  • DNA-Binding Proteins / metabolism
  • DNA-Binding Proteins / physiology*
  • Endothelial Cells / microbiology
  • Endothelium, Vascular / cytology
  • Fimbriae, Bacterial / metabolism
  • Fimbriae, Bacterial / physiology
  • HeLa Cells / chemistry
  • HeLa Cells / metabolism
  • HeLa Cells / microbiology
  • Histiocytes / chemistry
  • Histiocytes / pathology
  • Humans
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Immunohistochemistry / methods
  • Macrophages / chemistry
  • Macrophages / pathology
  • Neovascularization, Pathologic / microbiology
  • Nuclear Proteins / immunology
  • Nuclear Proteins / metabolism
  • Nuclear Proteins / physiology*
  • Transcription Factors / immunology
  • Transcription Factors / metabolism
  • Transcription Factors / physiology*
  • Umbilical Veins / cytology
  • Up-Regulation / physiology

Substances

  • DNA-Binding Proteins
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Nuclear Proteins
  • Transcription Factors
  • Adenosine Triphosphate