Fungal Mimicry of a Mammalian Aminopeptidase Disables Innate Immunity and Promotes Pathogenicity

Cell Host Microbe. 2016 Mar 9;19(3):361-74. doi: 10.1016/j.chom.2016.02.001. Epub 2016 Feb 25.

Abstract

Systemic fungal infections trigger marked immune-regulatory disturbances, but the mechanisms are poorly understood. We report that the pathogenic yeast of Blastomyces dermatitidis elaborates dipeptidyl-peptidase IVA (DppIVA), a close mimic of the mammalian ectopeptidase CD26, which modulates critical aspects of hematopoiesis. We show that, like the mammalian enzyme, fungal DppIVA cleaved C-C chemokines and GM-CSF. Yeast producing DppIVA crippled the recruitment and differentiation of monocytes and prevented phagocyte activation and ROS production. Silencing fungal DppIVA gene expression curtailed virulence and restored recruitment of CCR2(+) monocytes, generation of TipDC, and phagocyte killing of yeast. Pharmacological blockade of DppIVA restored leukocyte effector functions and stemmed infection, while addition of recombinant DppIVA to gene-silenced yeast enabled them to evade leukocyte defense. Thus, fungal DppIVA mediates immune-regulatory disturbances that underlie invasive fungal disease. These findings reveal a form of molecular piracy by a broadly conserved aminopeptidase during disease pathogenesis.

Keywords: DppIV; TipDCs; fungal; macrophages; neutrophils.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aminopeptidases / metabolism*
  • Animals
  • Biological Mimicry
  • Blastomyces / enzymology*
  • Blastomyces / pathogenicity
  • Chemokines / metabolism
  • Dipeptidyl-Peptidases and Tripeptidyl-Peptidases / genetics
  • Dipeptidyl-Peptidases and Tripeptidyl-Peptidases / metabolism*
  • Gene Silencing
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism
  • Immune Evasion*
  • Immune Tolerance*
  • Immunity, Innate / drug effects*
  • Macrophages / immunology
  • Mice
  • Microbial Viability
  • Monocytes / immunology
  • Phagocytosis
  • Reactive Oxygen Species / metabolism
  • Sequence Homology, Amino Acid
  • Virulence Factors / genetics
  • Virulence Factors / metabolism*

Substances

  • Chemokines
  • Reactive Oxygen Species
  • Virulence Factors
  • Granulocyte-Macrophage Colony-Stimulating Factor
  • Aminopeptidases
  • Dipeptidyl-Peptidases and Tripeptidyl-Peptidases