EhRacM differentially regulates macropinocytosis and motility in the enteric protozoan parasite Entamoeba histolytica

PLoS Pathog. 2024 Nov 13;20(11):e1012364. doi: 10.1371/journal.ppat.1012364. eCollection 2024 Nov.

Abstract

Macropinocytosis is an evolutionarily conserved endocytic process that plays a vital role in internalizing extracellular fluids and particles in cells. This non-selective endocytic pathway is crucial for various physiological functions such as nutrient uptake, sensing, signaling, antigen presentation, and cell migration. While macropinocytosis has been extensively studied in macrophages and cancer cells, the molecular mechanisms of macropinocytosis in pathogens are less understood. It has been known that Entamoeba histolytica, the causative agent of amebiasis, exploits macropinocytosis for survival and pathogenesis. Since macropinocytosis is initiated by actin polymerization, leading to the formation of membrane ruffles and the subsequent trapping of solutes in macropinosomes, actin cytoskeleton regulation is crucial. Thus, this study focuses on unraveling the role of well-conserved actin cytoskeleton regulators, Rho small GTPase family proteins, in macropinocytosis in E. histolytica. Through gene silencing of highly transcribed Ehrho/Ehrac genes and following flow cytometry analysis, we identified that silencing EhracM enhances dextran macropinocytosis and affects cellular migration persistence. Live imaging and interactome analysis unveiled the cytosolic and vesicular localization of EhRacM, along with its interaction with signaling and membrane traffic-related proteins, shedding light on EhRacM's multiple roles. Our findings provide insights into the specific regulatory mechanisms of macropinocytosis among endocytic pathways in E. histolytica, highlighting the significance of EhRacM in both macropinocytosis and cellular migration.

MeSH terms

  • Animals
  • Cell Movement*
  • Entamoeba histolytica* / metabolism
  • Entamoeba histolytica* / physiology
  • Entamoebiasis / metabolism
  • Entamoebiasis / parasitology
  • Humans
  • Pinocytosis* / physiology
  • Protozoan Proteins* / genetics
  • Protozoan Proteins* / metabolism
  • rho GTP-Binding Proteins / metabolism

Substances

  • Protozoan Proteins
  • rho GTP-Binding Proteins

Grants and funding

This research was funded by Grants-in-Aid for Scientific Research (B) from the Japan Society for the Promotion of Science (JSPS) (JP18H02650 and JP21H02723 to T.N.), Fostering Joint International Research (B) from JSPS (JP19H03463 to K.N-T), Grant for Science and Technology Research Partnership for Sustainable Development (SATREPS) from Japan Agency for Medical Research and Development (AMED) and Japan International Cooperation Agency (JICA) (JP24jm0110022) to T.N., Grant for research on emerging and re-emerging infectious diseases from AMED (JP24fk0108680 to T.N., P23fk0108680j0401 and JP24fk0108683j0302 to K.N-T), NCGM International Research Fund from National Center for Global Health and Medicine (23A2017 to K.N-T), support from the University of Tokyo Pandemic Preparedness, Infection, and Advanced Research Center (UTOPIA) and AMED (JP243fa627001) to T.N., research grant from Ohyama Health Foundation to K.N-T, and research grant from JSPS for the world-leading innovative graduate study program for life science and technology (WINGS-LST) to M.S. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.