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Title: Molecular basis of endosomal-membrane association for the dengue virus envelope protein

Abstract

Dengue virus is coated by an icosahedral shell of 90 envelope protein dimers that convert to trimers at low pH and promote fusion of its membrane with the membrane of the host endosome. We provide the first estimates for the free energy barrier and minimum for two key steps in this process: host membrane bending and protein–membrane binding. Both are studied using complementary membrane elastic, continuum electrostatics and all-atom molecular dynamics simulations. The predicted host membrane bending required to form an initial fusion stalk presents a 22–30 kcal/mol free energy barrier according to a constrained membrane elastic model. Combined continuum and molecular dynamics results predict a 15 kcal/mol free energy decrease on binding of each trimer of dengue envelope protein to a membrane with 30% anionic phosphatidylglycerol lipid. The bending cost depends on the preferred curvature of the lipids composing the host membrane leaflets, while the free energy gained for protein binding depends on the surface charge density of the host membrane. The fusion loop of the envelope protein inserts exactly at the level of the interface between the membrane's hydrophobic and head-group regions. As a result, the methods used in this work provide a means for further characterization ofmore » the structures and free energies of protein-assisted membrane fusion.« less

Authors:
; ;
Publication Date:
Research Org.:
Sandia National Laboratories (SNL), Albuquerque, NM, and Livermore, CA (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1242426
Alternate Identifier(s):
OSTI ID: 1214661
Grant/Contract Number:  
AC04-94AL85000
Resource Type:
Published Article
Journal Name:
Biochimica et Biophysica Acta. Biomembranes
Additional Journal Information:
Journal Name: Biochimica et Biophysica Acta. Biomembranes Journal Volume: 1848 Journal Issue: 4; Journal ID: ISSN 0005-2736
Publisher:
Elsevier
Country of Publication:
Netherlands
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; fusion; free energy; multi-scale models; membrane bending

Citation Formats

Rogers, David M., Kent, Michael S., and Rempe, Susan B. Molecular basis of endosomal-membrane association for the dengue virus envelope protein. Netherlands: N. p., 2015. Web. doi:10.1016/j.bbamem.2014.12.018.
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Rogers, David M., Kent, Michael S., & Rempe, Susan B. Molecular basis of endosomal-membrane association for the dengue virus envelope protein. Netherlands. https://doi.org/10.1016/j.bbamem.2014.12.018
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Rogers, David M., Kent, Michael S., and Rempe, Susan B. Wed . "Molecular basis of endosomal-membrane association for the dengue virus envelope protein". Netherlands. https://doi.org/10.1016/j.bbamem.2014.12.018.
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@article{osti_1242426,
title = {Molecular basis of endosomal-membrane association for the dengue virus envelope protein},
author = {Rogers, David M. and Kent, Michael S. and Rempe, Susan B.},
abstractNote = {Dengue virus is coated by an icosahedral shell of 90 envelope protein dimers that convert to trimers at low pH and promote fusion of its membrane with the membrane of the host endosome. We provide the first estimates for the free energy barrier and minimum for two key steps in this process: host membrane bending and protein–membrane binding. Both are studied using complementary membrane elastic, continuum electrostatics and all-atom molecular dynamics simulations. The predicted host membrane bending required to form an initial fusion stalk presents a 22–30 kcal/mol free energy barrier according to a constrained membrane elastic model. Combined continuum and molecular dynamics results predict a 15 kcal/mol free energy decrease on binding of each trimer of dengue envelope protein to a membrane with 30% anionic phosphatidylglycerol lipid. The bending cost depends on the preferred curvature of the lipids composing the host membrane leaflets, while the free energy gained for protein binding depends on the surface charge density of the host membrane. The fusion loop of the envelope protein inserts exactly at the level of the interface between the membrane's hydrophobic and head-group regions. As a result, the methods used in this work provide a means for further characterization of the structures and free energies of protein-assisted membrane fusion.},
doi = {10.1016/j.bbamem.2014.12.018},
journal = {Biochimica et Biophysica Acta. Biomembranes},
number = 4,
volume = 1848,
place = {Netherlands},
year = {Wed Apr 01 00:00:00 EDT 2015},
month = {Wed Apr 01 00:00:00 EDT 2015}
}
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Journal Article:
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Publisher's Version of Record
https://doi.org/10.1016/j.bbamem.2014.12.018
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Cited by: 22 works
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Figures / Tables:

Fig. 1 Fig. 1: Possible hemifusion route to virus (upper)–host (lower) membrane fusion, illustrated through alignment of E protein to: a) dimeric, mature viral assembly (3C6R ); b) an intermediate structure during trimerization approximated by the two cryo-EM structures with exposed fusion loops, 3C6D and 3IXY; c) target, fused state with trimericmore » form (1OK8) as proposed in earlier works, arbitrarily positioned to interact with a catenoid-shaped, zero mean curvature, membrane. Panels (b) and (d) are marked by * to illustrate the state defining the free energy barrier for this process. Panel (d) shows a red outline for the minimal energy dimple shape of the host membrane, h(r), explained further in Fig. 2, and an outline of the 3IXY E protein structure used to constrain the host membrane shape. Two radii measured from the virus center identify the distance to the E protein fusion loop (Rfus) and N-terminal alpha-carbon (Rterm). The actual conformation of the protein at steps (b–c), and the mechanism promoting the membrane dimple, are unknown. For clarity, only five trimers (i.e. from one pentagon in Fig. 2) are shown in (a)–(c), and the far three are colored gray. Protein domains I, II, III are colored (red, yellow, blue). Although not modeled in this work, the C-terminal stem and the perimembrane part of its anchor are shown for reference (green) for one Emonomer in (a)–(c). This stem region would sit between the E protein and the viral membrane. All E protein fusion peptides are colored magenta. Binding and conformational transitions of the fusion envelope protein may assist in lipid rearrangement or curvature formation during membrane fusion.« less
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