Adhesion to nanofibers drives cell membrane remodeling through one-dimensional wetting

• Published in: Nature communications Vol. 9; no. 1; pp. 4450 - 14
• Main Authors: Charles-Orszag, Arthur, Tsai, Feng-Ching, Bonazzi, Daria, Manriquez, Valeria, Sachse, Martin, Mallet, Adeline, Salles, Audrey, Melican, Keira, Staneva, Ralitza, Bertin, Aurélie, Millien, Corinne, Goussard, Sylvie, Lafaye, Pierre, Shorte, Spencer, Piel, Matthieu, Krijnse-Locker, Jacomine, Brochard-Wyart, Françoise, Bassereau, Patricia, Duménil, Guillaume
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 25.10.2018; Nature Publishing Group; Nature Portfolio
• Subjects: 14/19; 14/28; 14/35; 14/63; 147/135; 147/143; 147/28; 631/326/41/88; 631/326/421; 631/57/2270; 631/80; 64/60; Actin; Animals; Bacteria; Bacterial Adhesion; Cell division; Cell Membrane - metabolism; Cell membranes; Cell Surface Extensions - metabolism; Cell Surface Extensions - ultrastructure; Endothelial cells; Extracellular matrix; Human Umbilical Vein Endothelial Cells - metabolism; Human Umbilical Vein Endothelial Cells - ultrastructure; Humanities and Social Sciences; Humans; Immunology; Immunotherapy; Infections; Life Sciences; Liposomes; Medicin och hälsovetenskap; Membranes; Mice, SCID; Models, Biological; multidisciplinary; Nanofibers; Nanofibers - chemistry; Nanofibers - ultrastructure; Neisseria meningitidis - metabolism; Neisseria meningitidis - ultrastructure; Pathogenesis; Pathogens; Pili; Plasma; Scanning electron microscopy; Science; Science (multidisciplinary); Wettability; Wetting
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-018-06948-x

The shape of cellular membranes is highly regulated by a set of conserved mechanisms that can be manipulated by bacterial pathogens to infect cells. Remodeling of the plasma membrane of endothelial cells by the bacterium Neisseria meningitidis is thought to be essential during the blood phase of meningococcal infection, but the underlying mechanisms are unclear. Here we show that plasma membrane remodeling occurs independently of F-actin, along meningococcal type IV pili fibers, by a physical mechanism that we term ‘one-dimensional’ membrane wetting. We provide a theoretical model that describes the physical basis of one-dimensional wetting and show that this mechanism occurs in model membranes interacting with nanofibers, and in human cells interacting with extracellular matrix meshworks. We propose one-dimensional wetting as a new general principle driving the interaction of cells with their environment at the nanoscale that is diverted by meningococci during infection. Meningococci remodel the plasma membrane of host cells during infection. Here, Charles-Orszag et al. show that plasma membrane remodeling occurs independently of F-actin, along meningococcal type IV pili fibers, by a physical mechanism that they term ‘one-dimensional’ membrane wetting.