A small-angle neutron scattering study of the physical mechanism that drives the action of a viral fusion peptide

Heller, William T.

doi:10.1016/j.chemphyslip.2020.105022

Title: A small-angle neutron scattering study of the physical mechanism that drives the action of a viral fusion peptide

Journal Article · Fri Nov 27 00:00:00 EST 2020 · Chemistry and Physics of Lipids

DOI:https://doi.org/10.1016/j.chemphyslip.2020.105022· OSTI ID:1735436

^[1]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Viruses have evolved a variety of ways for delivering their genetic cargo to a target cell. One mechanism relies on a short sequence from a protein of the virus that is referred to as a fusion peptide. In some cases, the isolated fusion peptide is also capable of causing membranes to fuse. Infection by HIV-1 involves the 23 amino acid N-terminal sequence of its gp41 envelope protein, which is capable of causing membranes to fuse by itself, but the mechanism by which it does so is not fully understood. In this study, a variant of the gp41 fusion peptide that does not strongly promote fusion was studied in the presence of vesicles composed of a mixture of unsaturated lipids and cholesterol by small-angle neutron scattering and circular dichroism spectroscopy to improve the understanding of the mechanism that drives vesicle fusion. The peptide concentration and cholesterol content govern both the peptide conformation and its impact on the bilayer structure. The results indicate that the mechanism that drives vesicle fusion by the peptide is a strong distortion of the bilayer structure by the peptide when it adopts the β-sheet conformation.

View Accepted Manuscript (DOE)

View Accepted Manuscript (Publisher)

Cite

Export

Save

Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1735436

Alternate ID(s):: OSTI ID: 1775639

Journal Information:: Chemistry and Physics of Lipids, Vol. 234, Issue 1; ISSN 0009-3084

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (62)

Structure and orientation study of Ebola fusion peptide inserted in lipid membrane models Agopian, Audrey; Castano, Sabine Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1838, Issue 1 https://doi.org/10.1016/j.bbamem.2013.09.003	journal	January 2014
Mantid—Data analysis and visualization package for neutron scattering and $μ$ SR experiments Arnold, O.; Bilheux, J. C.; Borreguero, J. M. Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 764 https://doi.org/10.1016/j.nima.2014.07.029	journal	November 2014
Target cell-specific determinants of membrane fusion within the human immunodeficiency virus type 1 gp120 third variable region and gp41 amino terminus. Bergeron, L.; Sullivan, N.; Sodroski, J. Journal of Virology, Vol. 66, Issue 4 https://doi.org/10.1128/JVI.66.4.2389-2397.1992	journal	January 1992
C13–C13 and N15–C13 correlation spectroscopy of membrane-associated and uniformly labeled human immunodeficiency virus and influenza fusion peptides: Amino acid-type assignments and evidence for multiple conformations Bodner, Michele L.; Gabrys, Charles M.; Struppe, Jochem O. The Journal of Chemical Physics, Vol. 128, Issue 5 https://doi.org/10.1063/1.2829984	journal	February 2008
Determination of protein secondary structure in solution by vacuum ultraviolet circular dichroism Brahms, S.; Brahms, J. Journal of Molecular Biology, Vol. 138, Issue 2 https://doi.org/10.1016/0022-2836(80)90282-X	journal	April 1980
Effect of Cholesterol on the Interaction of the HIV GP41 Fusion Peptide with Model Membranes. Importance of the Membrane Dipole Potential ^† Buzón, Víctor; Cladera, Josep Biochemistry, Vol. 45, Issue 51 https://doi.org/10.1021/bi060622i	journal	December 2006
Structure and orientation study of fusion peptide FP23 of gp41 from HIV-1 alone or inserted into various lipid membrane models (mono-, bi- and multibi-layers) by FT-IR spectroscopies and Brewster angle microscopy Castano, Sabine; Desbat, Bernard Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1715, Issue 2 https://doi.org/10.1016/j.bbamem.2005.07.008	journal	September 2005
The interactions of the N-terminal fusogenic peptide of HIV-1 gp41 with neutral phospholipids Curtain, C.; Separovic, Frances; Nielsen, Katherine European Biophysics Journal, Vol. 28, Issue 5 https://doi.org/10.1007/s002490050225	journal	June 1999
Understanding inelastically scattered neutrons from water on a time-of-flight small-angle neutron scattering (SANS) instrument Do, Changwoo; Heller, William T.; Stanley, Christopher Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 737 https://doi.org/10.1016/j.nima.2013.11.030	journal	February 2014
A syncytia assay for human immunodeficiency virus type I(H IV-I) envelope protein and its use in studying HIV-I mutations Felser, James M.; Klimkait, Thomas; Silver, Jonathan Virology, Vol. 170, Issue 2 https://doi.org/10.1016/0042-6822(89)90448-0	journal	June 1989
The Role of Human Immunodeficiency Virus Type 1 Envelope Glycoproteins in Virus Infection Freed, Eric O.; Martin, Malcolm A. Journal of Biological Chemistry, Vol. 270, Issue 41 https://doi.org/10.1074/jbc.270.41.23883	journal	October 1995
Characterization of the fusion domain of the human immunodeficiency virus type 1 envelope glycoprotein gp41. Freed, E. O.; Myers, D. J.; Risser, R. Proceedings of the National Academy of Sciences, Vol. 87, Issue 12 https://doi.org/10.1073/pnas.87.12.4650	journal	June 1990
A mutation in the human immunodeficiency virus type 1 transmembrane glycoprotein gp41 dominantly interferes with fusion and infectivity. Freed, E. O.; Delwart, E. L.; Buchschacher, G. L. Proceedings of the National Academy of Sciences, Vol. 89, Issue 1 https://doi.org/10.1073/pnas.89.1.70	journal	January 1992
Small-angle scattering model for multilamellar vesicles Frielinghaus, Henrich Physical Review E, Vol. 76, Issue 5 https://doi.org/10.1103/PhysRevE.76.051603	journal	November 2007
2H nuclear magnetic resonance spectroscopy supports larger amplitude fast motion and interference with lipid chain ordering for membrane that contains β sheet human immunodeficiency virus gp41 fusion peptide or helical hairpin influenza virus hemagglutinin fusion peptide at fusogenic pH Ghosh, Ujjayini; Weliky, David P. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1862, Issue 10 https://doi.org/10.1016/j.bbamem.2020.183404	journal	October 2020
The amino-terminal peptide of HIV-1 glycoprotein 41 interacts with human erythrocyte membranes: peptide conformation, orientation and aggregation Gordon, L. M.; Curtain, C. C.; Zhong, Y. C. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1139, Issue 4 https://doi.org/10.1016/0925-4439(92)90099-9	journal	August 1992
Elastic Properties of Lipid Bilayers: Theory and Possible Experiments Helfrich, W. Zeitschrift für Naturforschung C, Vol. 28, Issue 11-12 https://doi.org/10.1515/znc-1973-11-1209	journal	December 1973
ELLSTAT : shape modeling for solution small-angle scattering of proteins and protein complexes with automated statistical characterization Heller, William T. Journal of Applied Crystallography, Vol. 39, Issue 5 https://doi.org/10.1107/S0021889806029591	journal	September 2006
Changes in lipid bilayer structure caused by the helix-to-sheet transition of an HIV-1 gp41 fusion peptide derivative Heller, William T.; Rai, Durgesh K. Chemistry and Physics of Lipids, Vol. 203 https://doi.org/10.1016/j.chemphyslip.2017.01.004	journal	March 2017
Membrane Thinning Effect of the β-Sheet Antimicrobial Protegrin ^† Heller, William T.; Waring, Alan J.; Lehrer, Robert I. Biochemistry, Vol. 39, Issue 1 https://doi.org/10.1021/bi991892m	journal	January 2000
The helix-to-sheet transition of an HIV-1 fusion peptide derivative changes the mechanical properties of lipid bilayer membranes Heller, William T.; Zolnierczuk, Piotr A. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1861, Issue 3 https://doi.org/10.1016/j.bbamem.2018.12.004	journal	March 2019
The Condensing Effect of Cholesterol in Lipid Bilayers Hung, Wei-Chin; Lee, Ming-Tao; Chen, Fang-Yu Biophysical Journal, Vol. 92, Issue 11 https://doi.org/10.1529/biophysj.106.099234	journal	June 2007
Membrane Fusion Jahn, Reinhard; Lang, Thorsten; Südhof, Thomas C. Cell, Vol. 112, Issue 4 https://doi.org/10.1016/S0092-8674(03)00112-0	journal	February 2003
REDOR solid-state NMR as a probe of the membrane locations of membrane-associated peptides and proteins Jia, Lihui; Liang, Shuang; Sackett, Kelly Journal of Magnetic Resonance, Vol. 253 https://doi.org/10.1016/j.jmr.2014.12.020	journal	April 2015
HIV gp41 Fusion Peptide Increases Membrane Ordering in a Cholesterol-Dependent Fashion Lai, Alex L.; Freed, Jack H. Biophysical Journal, Vol. 106, Issue 1 https://doi.org/10.1016/j.bpj.2013.11.027	journal	January 2014
Fusion Activity of HIV gp41 Fusion Domain Is Related to Its Secondary Structure and Depth of Membrane Insertion in a Cholesterol-Dependent Fashion Lai, Alex L.; Moorthy, Anna Eswara; Li, Yinling Journal of Molecular Biology, Vol. 418, Issue 1-2 https://doi.org/10.1016/j.jmb.2012.02.010	journal	April 2012
Membrane-Mediated Peptide Conformation Change from α-Monomers to β-Aggregates Lee, Chang-Chun; Sun, Yen; Huang, Huey W. Biophysical Journal, Vol. 98, Issue 10 https://doi.org/10.1016/j.bpj.2010.02.001	journal	May 2010
How Type II Diabetes-Related Islet Amyloid Polypeptide Damages Lipid Bilayers Lee, Chang-Chun; Sun, Yen; Huang, Huey W. Biophysical Journal, Vol. 102, Issue 5 https://doi.org/10.1016/j.bpj.2012.01.039	journal	March 2012
Membrane thinning caused by magainin 2 Ludtke, Steve; He, Ke; Huang, Huey Biochemistry, Vol. 34, Issue 51 https://doi.org/10.1021/bi00051a026	journal	December 1995
Membrane interactions of the synthetic N-terminal peptide of HIV-1 gp41 and its structural analogs Mobley, Patrick W.; Waring, Alan J.; Sherman, Mark A. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1418, Issue 1 https://doi.org/10.1016/S0005-2736(99)00014-0	journal	April 1999
Combined influence of cholesterol and synthetic amphiphillic peptides upon bilayer thickness in model membranes Nezil, F. A.; Bloom, M. Biophysical Journal, Vol. 61, Issue 5 https://doi.org/10.1016/S0006-3495(92)81926-4	journal	May 1992
Interaction of the HIV-1 Fusion Peptide with Phospholipid Vesicles: Different Structural Requirements for Fusion and Leakage Nieva, Jose L.; Nir, Shlomo; Muga, Arturo Biochemistry, Vol. 33, Issue 11 https://doi.org/10.1021/bi00177a009	journal	March 1994
Method of separated form factors for polydisperse vesicles Pencer, Jeremy; Krueger, Susan; Adams, Carl P. Journal of Applied Crystallography, Vol. 39, Issue 3 https://doi.org/10.1107/S0021889806005255	journal	May 2006
Permeabilization and fusion of uncharged lipid vesicles induced by the HIV-1 fusion peptide adopting an extended conformation: dose and sequence effects Pereira, F. B.; Goñi, F. M.; Muga, A. Biophysical Journal, Vol. 73, Issue 4 https://doi.org/10.1016/S0006-3495(97)78228-6	journal	October 1997
Peptide-Induced Asymmetric Distribution of Charged Lipids in a Vesicle Bilayer Revealed by Small-Angle Neutron Scattering Qian, Shuo; Heller, William T. The Journal of Physical Chemistry B, Vol. 115, Issue 32 https://doi.org/10.1021/jp204045t	journal	August 2011
HIV Fusion Peptide and Its Cross-Linked Oligomers: Efficient Syntheses, Significance of the Trimer in Fusion Activity, Correlation of β Strand Conformation with Membrane Cholesterol, and Proximity to Lipid Headgroups ^† Qiang, Wei; Weliky, David P. Biochemistry, Vol. 48, Issue 2 https://doi.org/10.1021/bi8015668	journal	January 2009
Solid-State Nuclear Magnetic Resonance Measurements of HIV Fusion Peptide to Lipid Distances Reveal the Intimate Contact of β Strand Peptide with Membranes and the Proximity of the Ala-14−Gly-16 Region with Lipid Headgroups Qiang, Wei; Yang, Jun; Weliky, David P. Biochemistry, Vol. 46, Issue 17 https://doi.org/10.1021/bi6024808	journal	April 2007
Solid-State NMR Spectroscopy of Human Immunodeficiency Virus Fusion Peptides Associated with Host-Cell-Like Membranes: 2D Correlation Spectra and Distance Measurements Support a Fully Extended Conformation and Models for Specific Antiparallel Strand Registries Qiang, Wei; Bodner, Michele L.; Weliky, David P. Journal of the American Chemical Society, Vol. 130, Issue 16 https://doi.org/10.1021/ja077302m	journal	March 2008
A strong correlation between fusogenicity and membrane insertion depth of the HIV fusion peptide Qiang, W.; Sun, Y.; Weliky, D. P. Proceedings of the National Academy of Sciences, Vol. 106, Issue 36 https://doi.org/10.1073/pnas.0907360106	journal	August 2009
Phospholipid interactions of synthetic peptides representing the N-terminus of HIV gp41 Rafalski, M.; Lear, J. D.; DeGrado, W. F. Biochemistry, Vol. 29, Issue 34 https://doi.org/10.1021/bi00486a020	journal	August 1990
The Interaction of Melittin with Dimyristoyl Phosphatidylcholine-Dimyristoyl Phosphatidylserine Lipid Bilayer Membranes Rai, Durgesh K.; Qian, Shuo; Heller, William T. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 11 https://doi.org/10.1016/j.bbamem.2016.08.006	journal	November 2016
The HIV Fusion Peptide Adopts Intermolecular Parallel β-Sheet Structure in Membranes when Stabilized by the Adjacent N-Terminal Heptad Repeat: A 13C FTIR Study Sackett, Kelly; Shai, Yechiel Journal of Molecular Biology, Vol. 350, Issue 4 https://doi.org/10.1016/j.jmb.2005.05.030	journal	July 2005
Comparative Analysis of Membrane-Associated Fusion Peptide Secondary Structure and Lipid Mixing Function of HIV gp41 Constructs that Model the Early Pre-Hairpin Intermediate and Final Hairpin Conformations Sackett, Kelly; Nethercott, Matthew J.; Epand, Raquel F. Journal of Molecular Biology, Vol. 397, Issue 1 https://doi.org/10.1016/j.jmb.2010.01.018	journal	March 2010
Solid-State NMR Spectroscopy of the HIV gp41 Membrane Fusion Protein Supports Intermolecular Antiparallel β Sheet Fusion Peptide Structure in the Final Six-Helix Bundle State Sackett, Kelly; Nethercott, Matthew J.; Zheng, Zhaoxiong Journal of Molecular Biology, Vol. 426, Issue 5 https://doi.org/10.1016/j.jmb.2013.11.010	journal	March 2014
Conformational transitions of membrane-bound HIV-1 fusion peptide Sáez-Cirión, Asier; Nieva, José L. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1564, Issue 1 https://doi.org/10.1016/S0005-2736(02)00400-5	journal	August 2002
Major Antiparallel and Minor Parallel β Sheet Populations Detected in the Membrane-Associated Human Immunodeficiency Virus Fusion Peptide Schmick, Scott D.; Weliky, David P. Biochemistry, Vol. 49, Issue 50 https://doi.org/10.1021/bi101389r	journal	December 2010
Interaction of human immunodeficiency virus (HIV-1) fusion peptides with artificial lipid membranes Slepushkin, V. A.; Melikyan, G. B.; Sidorova, M. S. Biochemical and Biophysical Research Communications, Vol. 172, Issue 2 https://doi.org/10.1016/0006-291X(90)90768-I	journal	October 1990
Kinetic Process of β-Amyloid Formation via Membrane Binding Sun, Yen; Lee, Chang-Chun; Chen, Tzu-Hsuan Biophysical Journal, Vol. 99, Issue 2 https://doi.org/10.1016/j.bpj.2010.04.045	journal	July 2010
ORNL_SAS : software for calculation of small-angle scattering intensities of proteins and protein complexes Tjioe, Elina; Heller, William T. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S002188980702420X	journal	July 2007
HIV-1 Fusion Peptide Decreases Bending Energy and Promotes Curved Fusion Intermediates Tristram-Nagle, Stephanie; Nagle, John F. Biophysical Journal, Vol. 93, Issue 6 https://doi.org/10.1529/biophysj.107.109181	journal	September 2007
HIV Fusion Peptide Penetrates, Disorders, and Softens T-Cell Membrane Mimics Tristram-Nagle, Stephanie; Chan, Rob; Kooijman, Edgar Journal of Molecular Biology, Vol. 402, Issue 1 https://doi.org/10.1016/j.jmb.2010.07.026	journal	September 2010
Solid-state nuclear magnetic resonance studies of HIV and influenza fusion peptide orientations in membrane bilayers using stacked glass plate samples Wasniewski, Christopher M.; Parkanzky, Paul D.; Bodner, Michele L. Chemistry and Physics of Lipids, Vol. 132, Issue 1 https://doi.org/10.1016/j.chemphyslip.2004.09.008	journal	November 2004
Two States of Cyclic Antimicrobial Peptide RTD-1 in Lipid Bilayers Weiss, Thomas M.; Yang, Lin; Ding, Lai Biochemistry, Vol. 41, Issue 31 https://doi.org/10.1021/bi025853d	journal	August 2002
Absolute calibration of small-angle neutron scattering data Wignall, G. D.; Bates, F. S. Journal of Applied Crystallography, Vol. 20, Issue 1 https://doi.org/10.1107/S0021889887087181	journal	February 1987
X-ray diffraction study of lipid bilayer membranes interacting with amphiphilic helical peptides: diphytanoyl phosphatidylcholine with alamethicin at low concentrations Wu, Y.; He, K.; Ludtke, S. J. Biophysical Journal, Vol. 68, Issue 6 https://doi.org/10.1016/S0006-3495(95)80418-2	journal	June 1995
Observation of a Membrane Fusion Intermediate Structure Yang, L. Science, Vol. 297, Issue 5588 https://doi.org/10.1126/science.1074354	journal	September 2002
A Rhombohedral Phase of Lipid Containing a Membrane Fusion Intermediate Structure Yang, Lin; Huang, Huey W. Biophysical Journal, Vol. 84, Issue 3 https://doi.org/10.1016/S0006-3495(03)74988-1	journal	March 2003
Solid-State Nuclear Magnetic Resonance Evidence for Parallel and Antiparallel Strand Arrangements in the Membrane-Associated HIV-1 Fusion Peptide ^† Yang, Jun; Weliky, David P. Biochemistry, Vol. 42, Issue 40 https://doi.org/10.1021/bi0348157	journal	October 2003
Solid-State Nuclear Magnetic Resonance Evidence for an Extended β Strand Conformation of the Membrane-Bound HIV-1 Fusion Peptide Yang, Jun; Gabrys, Charles M.; Weliky, David P. Biochemistry, Vol. 40, Issue 27 https://doi.org/10.1021/bi0100283	journal	June 2001
Solid state NMR measurements of conformation and conformational distributions in the membrane-bound HIV-1 fusion peptide Yang, Jun; Parkanzky, Paul D.; Khunte, Bhagyashree A. Journal of Molecular Graphics and Modelling, Vol. 19, Issue 1 https://doi.org/10.1016/S1093-3263(00)00128-5	journal	February 2001
Membrane-Dependent Conformation, Dynamics, and Lipid Interactions of the Fusion Peptide of the Paramyxovirus PIV5 from Solid-State NMR Yao, Hongwei; Hong, Mei Journal of Molecular Biology, Vol. 425, Issue 3 https://doi.org/10.1016/j.jmb.2012.11.027	journal	February 2013
The extended Q -range small-angle neutron scattering diffractometer at the SNS Zhao, J. K.; Gao, C. Y.; Liu, D. Journal of Applied Crystallography, Vol. 43, Issue 5 https://doi.org/10.1107/S002188981002217X	journal	July 2010

Similar Records

The helix-to-sheet transition of an HIV-1 fusion peptide derivative changes the mechanical properties of lipid bilayer membranes

Journal Article · Wed Dec 12 00:00:00 EST 2018 · Biochimica et Biophysica Acta. Biomembranes · OSTI ID:1735436

Heller, William T.; Zolnierczuk, Piotr A.

Changes in lipid bilayer structure caused by the helix-to-sheet transition of an HIV-1 gp41 fusion peptide derivative

Journal Article · Mon Jan 16 00:00:00 EST 2017 · Chemistry and Physics of Lipids · OSTI ID:1735436

Heller, William T.; Rai, Durgesh K.

Structural and functional characterization of EIAV gp45 fusion peptide proximal region and asparagine-rich layer

Journal Article · Fri Apr 15 00:00:00 EDT 2016 · Virology · OSTI ID:1735436

Duan, Liangwei; Du, Jiansen; Wang, Xuefeng; +3 more

Related Subjects

60 APPLIED LIFE SCIENCES
HIV-1
viral fusion peptide
small-angle neutron scattering
membrane deformation

Title: A small-angle neutron scattering study of the physical mechanism that drives the action of a viral fusion peptide

Citation Formats

References (62)

Similar Records

Related Subjects