A new nucleocytoplasmic RhoGAP protein contributes to control the pathogenicity of Entamoeba histolytica by regulating EhRacC and EhRacD activity

Cell Microbiol. 2016 Nov;18(11):1653-1672. doi: 10.1111/cmi.12603. Epub 2016 May 25.

Abstract

Small GTPases are signalling molecules that regulate important cellular processes. GTPases are deactivated by GTPase-activating proteins (GAPs). While human GAPs have been intensively studied, no GAP has yet been characterized in Entamoeba histolytica. In this study, we identified and characterized a novel nucleocytoplasmic RhoGAP in E. histolytica termed EhRhoGAPnc. In silico analyses of the domain structure revealed a previously undescribed peptide region within the carboxy-terminal region of EhRhoGAPnc capable of interacting with phosphatidic acid and phosphatidylinositol 3,5-bisphosphate. The full structural GAP domain showed increase GAP activity compared with the minimum region able to display GAP activity, as analysed both by experimental assays and molecular dynamics simulations. Furthermore, we identified amino acid residues that promote interactions between EhRhoGAPnc and its target GTPases EhRacC and EhRacD. Immunofluorescence studies revealed that EhRhoGAPnc colocalized with EhRacC and EhRacD during uroid formation but not during erythrophagocytosis. Interestingly, during erythrophagocytosis of red blood cells, EhRhoGAPnc colocalized with phosphatidic acid and phosphatidylinositol 3,5-bisphosphate. Overexpression of EhRhoGAPnc in E. histolytica led to inhibition of actin adhesion plate formation, migration, adhesion of E. histolytica to MDCK cells and consequently to an impairment of the cytopathic activity.

MeSH terms

  • Amino Acid Sequence
  • Binding Sites
  • Cell Nucleus / metabolism
  • Conserved Sequence
  • Cytoplasm / metabolism
  • Entamoeba histolytica / enzymology
  • Entamoeba histolytica / pathogenicity*
  • Erythrocytes / parasitology
  • GTPase-Activating Proteins / chemistry
  • GTPase-Activating Proteins / physiology*
  • Humans
  • Molecular Dynamics Simulation
  • Phagocytosis
  • Protein Transport
  • Protozoan Proteins / chemistry
  • Protozoan Proteins / physiology*
  • rac GTP-Binding Proteins / metabolism*

Substances

  • GTPase-Activating Proteins
  • Protozoan Proteins
  • rho GTPase-activating protein
  • rac GTP-Binding Proteins