Epithelial microvilli establish an electrostatic barrier to microbial adhesion.
Microvilli are membrane extensions on the apical surface of polarized epithelia, such as intestinal enterocytes and tubule and duct epithelia. One notable exception in mucosal epithelia is M cells, which are specialized for capturing luminal microbial particles; M cells display a unique apical membrane lacking microvilli. Based on studies of M cell uptake under different ionic conditions, we hypothesized that microvilli may augment the mucosal barrier by providing an increased surface charge density from the increased membrane surface and associated glycoproteins. Thus, electrostatic charges may repel microbes from epithelial cells bearing microvilli, while M cells are more susceptible to microbial adhesion. To test the role of microvilli in bacterial adhesion and uptake, we developed polarized intestinal epithelial cells with reduced microvilli ("microvillus-minus," or MVM) but retaining normal tight junctions. When tested for interactions with microbial particles in suspension, MVM cells showed greatly enhanced adhesion and uptake of particles compared to microvillus-positive cells. This preference showed a linear relationship to bacterial surface charge, suggesting that microvilli resist binding of microbes by using electrostatic repulsion. Moreover, this predicts that pathogen modification of electrostatic forces may contribute directly to virulence. Accordingly, the effacement effector protein Tir from enterohemorrhagic Escherichia coli O157:H7 expressed in epithelial cells induced a loss of microvilli with consequent enhanced microbial binding. These results provide a new context for microvillus function in the host-pathogen relationship, based on electrostatic interactions.
Division of Biomedical Sciences, School of Medicine, University of California-Riverside, Riverside, California, USA Bioengineering Interdepartmental Graduate Program, University of California-Riverside, Riverside, California, USA.
Kaila M
KM
Bennett
Department of Chemical and Environmental Engineering, University of California-Riverside, Riverside, California, USA.
Sharon L
SL
Walker
Division of Biomedical Sciences, School of Medicine, University of California-Riverside, Riverside, California, USA david.lo@ucr.edu.
David D
DD
Lo
D001422:Bacterial Adhesion / Q000502:physiology*; D045744:Cell Line, Tumor; D003001:Cloning, Molecular; D054324:Enterohemorrhagic Escherichia coli / Q000502:physiology*; D004847:Epithelial Cells / Q000382:microbiology / Q000502:physiology*; D029968:Escherichia coli Proteins; D006801:Humans; D008871:Microvilli / Q000502:physiology*; D055672:Static Electricity; D013499:Surface Properties
D029968:Escherichia coli Proteins