Journal
BIOPHYSICAL JOURNAL
Volume 106, Issue 11, Pages 2395-2407Publisher
CELL PRESS
DOI: 10.1016/j.bpj.2014.04.016
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Funding
- Los Alamos National Security, LLC, for the National Nuclear Security Administration of the United States Department of Energy [DE-AC52-06NA25396]
- Photosynthetic Antenna Research Center, an Energy Frontier Research Center - United States Department of Energy, Office of Science, Basic Energy Sciences [SC0001035]
- Agriculture and Food Research Initiative Competitive - United States Department of Agriculture's National Institute of Food and Agriculture [2012-68003-30155]
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Lipopolysaccharide (LPS) is a unique lipoglycan, with two major physiological roles: 1), as a major structural component of the outer membrane of Gram-negative bacteria and 2), as a highly potent mammalian toxin when released from cells into solution (endotoxin). LPS is an amphiphile that spontaneously inserts into the outer leaflet of lipid bilayers to bury its hydrophobic lipidic domain, leaving the hydrophilic polysaccharide chain exposed to the exterior polar solvent. Divalent cations have long been known to neutralize and stabilize LPS in the outer membrane, whereas LPS in the presence of monovalent cations forms highly mobile negatively-charged aggregates. Yet, much of our understanding of LPS and its interactions with the cell membrane does not take into account its amphiphilic biochemistry and charge polarization. Herein, we report fluorescence microscopy and atomic force microscopy analysis of the interaction between LPS and fluid-phase supported lipid bilayer assemblies (sLBAs), as model membranes. Depending on cation availability, LPS induces three remarkably different effects on simple sLBAs. Net-negative LPS-N+ leads to the formation of 100-mu m-long flexible lipid tubules from surface-associated lipid vesicles and the destabilization of the sLBA resulting in micron-size hole formation. Neutral LPS-Ca2+ gives rise to 100-mu m-wide single- or multilamellar planar sheets of lipid and LPS formed from surface-associated lipid vesicles. Our findings have important implications about the physical interactions between LPS and lipids and demonstrate that sLBAs can be useful platforms to study the interactions of amphiphilic virulence factors with cell membranes. Additionally, our study supports the general phenomenon that lipids with highly charged or bulky headgroups can promote highly curved membrane architectures due to electrostatic and/or steric repulsions.
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