TY - JOUR
T1 - SopB-Mediated Recruitment of SNX18 Facilitates Salmonella Typhimurium Internalization by the Host Cell
AU - Liebl, David
AU - Qi, Xiaying
AU - Zhe, Yang
AU - Barnett, Timothy C
AU - Teasdale, Rohan D
PY - 2017/6/15
Y1 - 2017/6/15
N2 - To invade epithelial cells, Salmonella enterica serovar Typhimurium (S. Typhimurium) induces macropinocytosis through the action of virulence proteins delivered across the host cell membrane via a type III secretion system. We show that after docking at the plasma membrane S. Typhimurium triggers rapid recruitment of cytosolic SNX18, a SH3-PX-BAR domain sorting nexin protein, to the bacteria-induced membrane ruffles and to the nascent Salmonella-containing vacuole. SNX18 recruitment required the inositol-phosphatase activity of the Salmonella effector SopB and an intact phosphoinositide-binding site within the PX domain of SNX18, but occurred independently of Rho-GTPases Rac1 and Cdc42 activation. SNX18 promotes formation of the SCV from the plasma membrane by acting as a scaffold to recruit Dynamin-2 and N-WASP in a process dependent on the SH3 domain of SNX18. Quantification of bacteria uptake revealed that overexpression of SNX18 increased bacteria internalization, whereas a decrease was detected in cells overexpressing the phosphoinositide-binding mutant R303Q, the ΔSH3 mutant, and in cells where endogenous levels of SNX18 were knocked-down. This study identifies SNX18 as a novel target of SopB and suggests a mechanism where S. Typhimurium engages host factors via local manipulation of phosphoinositide composition at the site of invasion to orchestrate the internalization process.
AB - To invade epithelial cells, Salmonella enterica serovar Typhimurium (S. Typhimurium) induces macropinocytosis through the action of virulence proteins delivered across the host cell membrane via a type III secretion system. We show that after docking at the plasma membrane S. Typhimurium triggers rapid recruitment of cytosolic SNX18, a SH3-PX-BAR domain sorting nexin protein, to the bacteria-induced membrane ruffles and to the nascent Salmonella-containing vacuole. SNX18 recruitment required the inositol-phosphatase activity of the Salmonella effector SopB and an intact phosphoinositide-binding site within the PX domain of SNX18, but occurred independently of Rho-GTPases Rac1 and Cdc42 activation. SNX18 promotes formation of the SCV from the plasma membrane by acting as a scaffold to recruit Dynamin-2 and N-WASP in a process dependent on the SH3 domain of SNX18. Quantification of bacteria uptake revealed that overexpression of SNX18 increased bacteria internalization, whereas a decrease was detected in cells overexpressing the phosphoinositide-binding mutant R303Q, the ΔSH3 mutant, and in cells where endogenous levels of SNX18 were knocked-down. This study identifies SNX18 as a novel target of SopB and suggests a mechanism where S. Typhimurium engages host factors via local manipulation of phosphoinositide composition at the site of invasion to orchestrate the internalization process.
KW - Animals
KW - Bacterial Proteins/metabolism
KW - Benzylamines/pharmacology
KW - Cell Membrane/metabolism
KW - Cell Surface Extensions
KW - Cytosol/metabolism
KW - Dynamin II/metabolism
KW - Gene Knockdown Techniques
KW - HEK293 Cells
KW - Host-Pathogen Interactions/physiology
KW - Humans
KW - Mice
KW - Mutation
KW - Phosphatidylinositols/metabolism
KW - Phosphoric Monoester Hydrolases/metabolism
KW - Pinocytosis
KW - Quinoxalines/pharmacology
KW - RAW 264.7 Cells
KW - Salmonella Infections/metabolism
KW - Salmonella typhimurium/metabolism
KW - Sorting Nexins/genetics
KW - Type III Secretion Systems/metabolism
KW - Vacuoles
KW - Virulence
KW - Wiskott-Aldrich Syndrome Protein, Neuronal/metabolism
KW - cdc42 GTP-Binding Protein/metabolism
KW - rac1 GTP-Binding Protein/metabolism
UR - http://www.scopus.com/inward/record.url?scp=85027584903&partnerID=8YFLogxK
U2 - 10.3389/fcimb.2017.00257
DO - 10.3389/fcimb.2017.00257
M3 - Article
C2 - 28664153
SN - 2235-2988
VL - 7
SP - 257
JO - Frontiers in Cellular and Infection Microbiology
JF - Frontiers in Cellular and Infection Microbiology
IS - JUN
M1 - 257
ER -