Journal of Virology, volume 90, issue 1, pages 575-585

pH-Dependent Formation and Disintegration of the Influenza A Virus Protein Scaffold To Provide Tension for Membrane Fusion

Batishchev O. V. ^{1, 2}

Shilova L A ^{1, 2}

Kachala M V ¹

Tashkin V Y ¹

SOKOLOV V. S. ¹

Fedorova N. V. ³

Baratova L A ³

Knyazev D G ⁴

Zimmerberg J ⁵

Chizmadzhev Y A ¹

Hide authors affiliations Show authors affiliations: 5 affiliations

A. N. Frumkin Institute of Physical Chemistry and Electrochemistry, Russian Academy of Sciences, Moscow, Russia |

Moscow Institute of Physics and Technology, Dolgoprudniy, Russia |

A. N. Belozersky Institute of Physico-chemical Biology, Moscow State University, Moscow, Russia |

⁴

Johannes Kepler University Linz, Institute of Biophysics, Linz, Austria |

⁵

Section on Cellular and Membrane Biophysics, Program in Physical Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland, USA |

Publication type: Journal Article

Publication date: 2016-01-01

American Society for Microbiology

Journal: Journal of Virology

Quartile SCImago

Quartile WOS

Impact factor: 5.4

ISSN: 0022538X, 10985514

DOI: 10.1128/jvi.01539-15

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PubMed ID: 26468548

Microbiology

Immunology

Insect Science

Virology

Abstract

ABSTRACT

Influenza virus is taken up from a pH-neutral extracellular milieu into an endosome, whose contents then acidify, causing changes in the viral matrix protein (M1) that coats the inner monolayer of the viral lipid envelope. At a pH of ∼6, M1 interacts with the viral ribonucleoprotein (RNP) in a putative priming stage; at this stage, the interactions of the M1 scaffold coating the lipid envelope are intact. The M1 coat disintegrates as acidification continues to a pH of ∼5 to clear a physical path for the viral genome to transit from the viral interior to the cytoplasm. Here we investigated the physicochemical mechanism of M1's pH-dependent disintegration. In neutral media, the adsorption of M1 protein on the lipid bilayer was electrostatic in nature and reversible. The energy of the interaction of M1 molecules with each other in M1 dimers was about 10 times as weak as that of the interaction of M1 molecules with the lipid bilayer. Acidification drives conformational changes in M1 molecules due to changes in the M1 charge, leading to alterations in their electrostatic interactions. Dropping the pH from 7.1 to 6.0 did not disturb the M1 layer; dropping it lower partially desorbed M1 because of increased repulsion between M1 monomers still stuck to the membrane. Lipid vesicles coated with M1 demonstrated pH-dependent rupture of the vesicle membrane, presumably because of the tension generated by this repulsive force. Thus, the disruption of the vesicles coincident with M1 protein scaffold disintegration at pH 5 likely stretches the lipid membrane to the point of rupture, promoting fusion pore widening for RNP release.

IMPORTANCE Influenza remains a top killer of human beings throughout the world, in part because of the influenza virus's rapid binding to cells and its uptake into compartments hidden from the immune system. To attack the influenza virus during this time of hiding, we need to understand the physical forces that allow the internalized virus to infect the cell. In particular, we need to know how the protective coat of protein inside the viral surface reacts to the changes in acid that come soon after internalization. We found that acid makes the molecules of the protein coat push each other while they are still stuck to the virus, so that they would like to rip the membrane apart. This ripping force is known to promote membrane fusion, the process by which infection actually occurs.

By date By citations

Citations by journals

	1 2 3 4 5
Journal of Virology	Journal of Virology, 5, 13.89% Journal of Virology 5 publications, 13.89%
PLoS ONE	PLoS ONE, 4, 11.11% PLoS ONE 4 publications, 11.11%
International Journal of Molecular Sciences	International Journal of Molecular Sciences, 2, 5.56% International Journal of Molecular Sciences 2 publications, 5.56%
Membranes	Membranes, 2, 5.56% Membranes 2 publications, 5.56%
Scientific Reports	Scientific Reports, 2, 5.56% Scientific Reports 2 publications, 5.56%
Journal of Chemical Physics	Journal of Chemical Physics, 1, 2.78% Journal of Chemical Physics 1 publication, 2.78%
Bioscience Reports	Bioscience Reports, 1, 2.78% Bioscience Reports 1 publication, 2.78%
Biologicheskie Membrany	Biologicheskie Membrany, 1, 2.78% Biologicheskie Membrany 1 publication, 2.78%
Biomolecules	Biomolecules, 1, 2.78% Biomolecules 1 publication, 2.78%
Russian Chemical Bulletin	Russian Chemical Bulletin, 1, 2.78% Russian Chemical Bulletin 1 publication, 2.78%
Biochimica et Biophysica Acta - Biomembranes	Biochimica et Biophysica Acta - Biomembranes, 1, 2.78% Biochimica et Biophysica Acta - Biomembranes 1 publication, 2.78%
Seminars in Cell and Developmental Biology	Seminars in Cell and Developmental Biology, 1, 2.78% Seminars in Cell and Developmental Biology 1 publication, 2.78%
Journal of Biological Chemistry	Journal of Biological Chemistry, 1, 2.78% Journal of Biological Chemistry 1 publication, 2.78%
Science of the Total Environment	Science of the Total Environment, 1, 2.78% Science of the Total Environment 1 publication, 2.78%
Structure	Structure, 1, 2.78% Structure 1 publication, 2.78%
FEBS Letters	FEBS Letters, 1, 2.78% FEBS Letters 1 publication, 2.78%
Traffic	Traffic, 1, 2.78% Traffic 1 publication, 2.78%
Journal of Physical Chemistry Letters	Journal of Physical Chemistry Letters, 1, 2.78% Journal of Physical Chemistry Letters 1 publication, 2.78%
Frontiers in Molecular Biosciences	Frontiers in Molecular Biosciences, 1, 2.78% Frontiers in Molecular Biosciences 1 publication, 2.78%
Russian Journal of Physical Chemistry A	Russian Journal of Physical Chemistry A, 1, 2.78% Russian Journal of Physical Chemistry A 1 publication, 2.78%
Crystallography Reports	Crystallography Reports, 1, 2.78% Crystallography Reports 1 publication, 2.78%
Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology	Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology, 1, 2.78% Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology 1 publication, 2.78%
Emerging Microbes and Infections	Emerging Microbes and Infections, 1, 2.78% Emerging Microbes and Infections 1 publication, 2.78%
Journal of Biomolecular Structure and Dynamics	Journal of Biomolecular Structure and Dynamics, 1, 2.78% Journal of Biomolecular Structure and Dynamics 1 publication, 2.78%
	1 2 3 4 5

Citations by publishers

	1 2 3 4 5
Springer Nature	Springer Nature, 5, 13.89% Springer Nature 5 publications, 13.89%
Multidisciplinary Digital Publishing Institute (MDPI)	Multidisciplinary Digital Publishing Institute (MDPI), 5, 13.89% Multidisciplinary Digital Publishing Institute (MDPI) 5 publications, 13.89%
American Society for Microbiology	American Society for Microbiology, 5, 13.89% American Society for Microbiology 5 publications, 13.89%
Public Library of Science (PLoS)	Public Library of Science (PLoS), 4, 11.11% Public Library of Science (PLoS) 4 publications, 11.11%
Elsevier	Elsevier, 4, 11.11% Elsevier 4 publications, 11.11%
Pleiades Publishing	Pleiades Publishing, 3, 8.33% Pleiades Publishing 3 publications, 8.33%
Wiley	Wiley, 2, 5.56% Wiley 2 publications, 5.56%
American Institute of Physics (AIP)	American Institute of Physics (AIP), 1, 2.78% American Institute of Physics (AIP) 1 publication, 2.78%
Akademizdatcenter Nauka	Akademizdatcenter Nauka, 1, 2.78% Akademizdatcenter Nauka 1 publication, 2.78%
American Society for Biochemistry and Molecular Biology	American Society for Biochemistry and Molecular Biology, 1, 2.78% American Society for Biochemistry and Molecular Biology 1 publication, 2.78%
American Chemical Society (ACS)	American Chemical Society (ACS), 1, 2.78% American Chemical Society (ACS) 1 publication, 2.78%
Frontiers Media S.A.	Frontiers Media S.A., 1, 2.78% Frontiers Media S.A. 1 publication, 2.78%
Taylor & Francis	Taylor & Francis, 1, 2.78% Taylor & Francis 1 publication, 2.78%
	1 2 3 4 5

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Batishchev O. V. et al. pH-Dependent Formation and Disintegration of the Influenza A Virus Protein Scaffold To Provide Tension for Membrane Fusion // Journal of Virology. 2016. Vol. 90. No. 1. pp. 575-585.

GOST all authors (up to 50) Copy

Batishchev O. V., Shilova L. A., Kachala M. V., Tashkin V. Y., SOKOLOV V. S., Fedorova N. V., Baratova L. A., Knyazev D. G., Zimmerberg J., Chizmadzhev Y. A. pH-Dependent Formation and Disintegration of the Influenza A Virus Protein Scaffold To Provide Tension for Membrane Fusion // Journal of Virology. 2016. Vol. 90. No. 1. pp. 575-585.

RIS |

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RIS Copy

TY - JOUR

DO - 10.1128/jvi.01539-15

UR - https://doi.org/10.1128%2Fjvi.01539-15

TI - pH-Dependent Formation and Disintegration of the Influenza A Virus Protein Scaffold To Provide Tension for Membrane Fusion

T2 - Journal of Virology

AU - Batishchev, O. V.

AU - Shilova, L A

AU - Kachala, M V

AU - Tashkin, V Y

AU - SOKOLOV, V. S.

AU - Fedorova, N. V.

AU - Baratova, L A

AU - Knyazev, D G

AU - Zimmerberg, J

AU - Chizmadzhev, Y A

PY - 2016

DA - 2016/01/01 00:00:00

PB - American Society for Microbiology

SP - 575-585

IS - 1

VL - 90

PMID - 26468548

SN - 0022-538X

SN - 1098-5514

ER -

BibTex |

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@article{2016_Batishchev,

author = {O. V. Batishchev and L A Shilova and M V Kachala and V Y Tashkin and V. S. SOKOLOV and N. V. Fedorova and L A Baratova and D G Knyazev and J Zimmerberg and Y A Chizmadzhev},

title = {pH-Dependent Formation and Disintegration of the Influenza A Virus Protein Scaffold To Provide Tension for Membrane Fusion},

journal = {Journal of Virology},

year = {2016},

volume = {90},

publisher = {American Society for Microbiology},

month = {jan},

url = {https://doi.org/10.1128%2Fjvi.01539-15},

number = {1},

pages = {575--585},

doi = {10.1128/jvi.01539-15}

}

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MLA Copy

Batishchev, O. V., et al. “pH-Dependent Formation and Disintegration of the Influenza A Virus Protein Scaffold To Provide Tension for Membrane Fusion.” Journal of Virology, vol. 90, no. 1, Jan. 2016, pp. 575-585. https://doi.org/10.1128%2Fjvi.01539-15.

Found error?

Publisher

American Society for Microbiology

Journal

Journal of Virology

Quartile SCImago

Quartile WOS

Impact factor

5.4

ISSN

0022538X (Print)
10985514 (Electronic)

Labs

Bioelectrochemistry Laboratory

Profiles

Batishchev, Oleg Vyacheslavovich