Highly Basic Clusters in the Herpes Simplex Virus 1 Nuclear Egress Complex Drive Membrane Budding by Inducing Lipid Ordering

Thorsen, Michael K.; Lai, Alex; Lee, Michelle W.; Hoogerheide, David P.; Wong, Gerard L.; Freed, Jack H.; Heldwein, Ekaterina E.

doi:10.1128/mbio.01548-21

Title: Highly Basic Clusters in the Herpes Simplex Virus 1 Nuclear Egress Complex Drive Membrane Budding by Inducing Lipid Ordering

Journal Article · 23 August 2021 · mBio (Online)

DOI: https://doi.org/10.1128/mbio.01548-21 · OSTI ID:1903984

Thorsen, Michael K. ^[1]; Lai, Alex ^[2]; Lee, Michelle W. ^[3]; Hoogerheide, David P. ^[4]; Wong, Gerard L. ^[3]; Freed, Jack H. ^[2];

^[5]

Tufts University, Medford, MA (United States); OSTI
Cornell University, Ithaca, NY (United States)
University of California, Los Angeles, CA (United States)
National Institute of Standards and Technology (NIST), Gaithersburg, MD (United States)
Tufts University, Medford, MA (United States)

During replication of herpesviruses, capsids escape from the nucleus into the cytoplasm by budding at the inner nuclear membrane. This unusual process is mediated by the viral nuclear egress complex (NEC) that deforms the membrane around the capsid by oligomerizing into a hexagonal, membrane-bound scaffold. Here, we found that highly basic membrane-proximal regions (MPRs) of the NEC alter lipid order by inserting into the lipid headgroups and promote negative Gaussian curvature. We also find that the electrostatic interactions between the MPRs and the membranes are essential for membrane deformation. One of the MPRs is phosphorylated by a viral kinase during infection, and the corresponding phosphomimicking mutations block capsid nuclear egress. We show that the same phosphomimicking mutations disrupt the NEC-membrane interactions and inhibit NEC-mediated budding in vitro, providing a biophysical explanation for the in vivo phenomenon. Our data suggest that the NEC generates negative membrane curvature by both lipid ordering and protein scaffolding and that phosphorylation acts as an off switch that inhibits the membrane-budding activity of the NEC to prevent capsid-less budding.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States); Tufts University, Medford, MA (United States)

Sponsoring Organization:: Howard Hughes Medical Institute; National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1903984

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 4 Vol. 12; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

References (132)

Nonlinear-Least-Squares Analysis of Slow-Motion EPR Spectra in One and Two Dimensions Using a Modified Levenberg–Marquardt Algorithm Budil, David E.; Lee, Sanghyuk; Saxena, Sunil Journal of Magnetic Resonance, Series A, Vol. 120, Issue 2 https://doi.org/10.1006/jmra.1996.0113	journal	June 1996
Nuclear Import and Export of Viruses and Virus Genomes Whittaker, Gary R.; Helenius, Ari Virology, Vol. 246, Issue 1 https://doi.org/10.1006/viro.1998.9165	journal	June 1998
The Equine Herpesvirus 1 UL34 Gene Product Is Involved in an Early Step in Virus Egress and Can Be Efficiently Replaced by a UL34-GFP Fusion Protein Neubauer, Antonie; Rudolph, Jens; Brandmüller, Christine Virology, Vol. 300, Issue 2 https://doi.org/10.1006/viro.2002.1488	journal	September 2002
Lipid composition of nuclear membranes isolated from bovine liver Keenna, T. W.; Berezney, Ronald; Funk, Linda K. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 203, Issue 3 https://doi.org/10.1016/0005-2736(70)90191-4	journal	June 1970
Phospholipid composition, phospholipase A2 and sphingomyelinase activities in rat liver nuclear membrane and matrix Neitcheva, Tania; Peeva, Diana The International Journal of Biochemistry & Cell Biology, Vol. 27, Issue 10 https://doi.org/10.1016/1357-2725(95)00087-6	journal	October 1995
Membrane Fission: Model for Intermediate Structures Kozlovsky, Yonathan; Kozlov, Michael M. Biophysical Journal, Vol. 85, Issue 1 https://doi.org/10.1016/S0006-3495(03)74457-9	journal	July 2003
Hydration, Structure, and Molecular Interactions in the Headgroup Region of Dioleoylphosphatidylcholine Bilayers: An Electron Spin Resonance Study Ge, Mingtao; Freed, Jack H. Biophysical Journal, Vol. 85, Issue 6 https://doi.org/10.1016/S0006-3495(03)74816-4	journal	December 2003
Evidence for Membrane Thinning Effect as the Mechanism for Peptide-Induced Pore Formation Chen, Fang-Yu; Lee, Ming-Tao; Huang, Huey W. Biophysical Journal, Vol. 84, Issue 6 https://doi.org/10.1016/S0006-3495(03)75103-0	journal	June 2003
Phosphorylation reverses the membrane association of peptides that correspond to the basic domains of MARCKS and neuromodulin Kim, J.; Blackshear, P. J.; Johnson, J. D. Biophysical Journal, Vol. 67, Issue 1 https://doi.org/10.1016/S0006-3495(94)80473-4	journal	July 1994
Phosphorylation, high ionic strength, and calmodulin reverse the binding of MARCKS to phospholipid vesicles. Kim, J.; Shishido, T.; Jiang, X. Journal of Biological Chemistry, Vol. 269, Issue 45 https://doi.org/10.1016/S0021-9258(18)46916-5	journal	November 1994
Measuring Distances by Pulsed Dipolar ESR Spectroscopy: Spin‐Labeled Histidine Kinases Borbat, Peter P.; Freed, Jack H. Methods in Enzymology, p. 52-116 https://doi.org/10.1016/S0076-6879(07)23003-4	book	January 2007
Recent advances in site-directed spin labeling of proteins Hubbell, Wayne L.; Gross, Adrian; Langen, Ralf Current Opinion in Structural Biology, Vol. 8, Issue 5 https://doi.org/10.1016/S0959-440X(98)80158-9	journal	October 1998
The role of electrostatics in protein–membrane interactions Mulgrewnesbitt, A.; Diraviyam, K.; Wang, J. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1761, Issue 8 https://doi.org/10.1016/j.bbalip.2006.07.002	journal	August 2006
Insertion of Dengue E into lipid bilayers studied by neutron reflectivity and molecular dynamics simulations Vanegas, Juan M.; Heinrich, Frank; Rogers, David M. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1860, Issue 5 https://doi.org/10.1016/j.bbamem.2018.02.012	journal	May 2018
How to study proteins by circular dichroism Kelly, Sharon M.; Jess, Thomas J.; Price, Nicholas C. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1751, Issue 2 https://doi.org/10.1016/j.bbapap.2005.06.005	journal	August 2005
Fusion Peptide from Influenza Hemagglutinin Increases Membrane Surface Order: An Electron-Spin Resonance Study Ge, Mingtao; Freed, Jack H. Biophysical Journal, Vol. 96, Issue 12 https://doi.org/10.1016/j.bpj.2009.04.015	journal	June 2009
ADF/Cofilin Binds Phosphoinositides in a Multivalent Manner to Act as a PIP2-Density Sensor Zhao, Hongxia; Hakala, Markku; Lappalainen, Pekka Biophysical Journal, Vol. 98, Issue 10 https://doi.org/10.1016/j.bpj.2010.01.046	journal	May 2010
Two Conserved Residues Are Important for Inducing Highly Ordered Membrane Domains by the Transmembrane Domain of Influenza Hemagglutinin Ge, Mingtao; Freed, Jack H. Biophysical Journal, Vol. 100, Issue 1 https://doi.org/10.1016/j.bpj.2010.11.014	journal	January 2011
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
Tau Binds to Lipid Membrane Surfaces via Short Amphipathic Helices Located in Its Microtubule-Binding Repeats Georgieva, Elka R.; Xiao, Shifeng; Borbat, Peter P. Biophysical Journal, Vol. 107, Issue 6 https://doi.org/10.1016/j.bpj.2014.07.046	journal	September 2014
The Interaction between Influenza HA Fusion Peptide and Transmembrane Domain Affects Membrane Structure Lai, Alex L.; Freed, Jack H. Biophysical Journal, Vol. 109, Issue 12 https://doi.org/10.1016/j.bpj.2015.10.044	journal	December 2015
Influenza Virus M2 Protein Mediates ESCRT-Independent Membrane Scission Rossman, Jeremy S.; Jing, Xianghong; Leser, George P. Cell, Vol. 142, Issue 6 https://doi.org/10.1016/j.cell.2010.08.029	journal	September 2010
Structural Basis of Vesicle Formation at the Inner Nuclear Membrane Hagen, Christoph; Dent, Kyle C.; Zeev-Ben-Mordehai, Tzviya Cell, Vol. 163, Issue 7 https://doi.org/10.1016/j.cell.2015.11.029	journal	December 2015
Crystal Structure of the Herpesvirus Nuclear Egress Complex Provides Insights into Inner Nuclear Membrane Remodeling Zeev-Ben-Mordehai, Tzviya; Weberruß, Marion; Lorenz, Michael Cell Reports, Vol. 13, Issue 12 https://doi.org/10.1016/j.celrep.2015.11.008	journal	December 2015
Virus Budding and the ESCRT Pathway Votteler, Jörg; Sundquist, Wesley I. Cell Host & Microbe, Vol. 14, Issue 3 https://doi.org/10.1016/j.chom.2013.08.012	journal	September 2013
Phase-sensitive specular neutron reflectometry for imaging the nanometer scale composition depth profile of thin-film materials Kirby, B. J.; Kienzle, P. A.; Maranville, B. B. Current Opinion in Colloid & Interface Science, Vol. 17, Issue 1 https://doi.org/10.1016/j.cocis.2011.11.001	journal	February 2012
Relating structure to evolution in class II viral membrane fusion proteins Modis, Yorgo Current Opinion in Virology, Vol. 5 https://doi.org/10.1016/j.coviro.2014.01.009	journal	April 2014
Structure-Function Studies Link Class II Viral Fusogens with the Ancestral Gamete Fusion Protein HAP2 Pinello, Jennifer Fricke; Lai, Alex L.; Millet, Jean K. Current Biology, Vol. 27, Issue 5 https://doi.org/10.1016/j.cub.2017.01.049	journal	March 2017
Dynamin and the Actin Cytoskeleton Cooperatively Regulate Plasma Membrane Invagination by BAR and F-BAR Proteins Itoh, Toshiki; Erdmann, Kai S.; Roux, Aurelien Developmental Cell, Vol. 9, Issue 6 https://doi.org/10.1016/j.devcel.2005.11.005	journal	December 2005
Modeling membrane shaping by proteins: Focus on EHD2 and N-BAR domains Campelo, Felix; Fabrikant, Gur; McMahon, Harvey T. FEBS Letters, Vol. 584, Issue 9 https://doi.org/10.1016/j.febslet.2009.10.023	journal	October 2009
Breaching the Barrier—The Nuclear Envelope in Virus Infection Mettenleiter, Thomas C. Journal of Molecular Biology, Vol. 428, Issue 10 https://doi.org/10.1016/j.jmb.2015.10.001	journal	May 2016
The SARS-CoV Fusion Peptide Forms an Extended Bipartite Fusion Platform that Perturbs Membrane Order in a Calcium-Dependent Manner Lai, Alex L.; Millet, Jean K.; Daniel, Susan Journal of Molecular Biology, Vol. 429, Issue 24 https://doi.org/10.1016/j.jmb.2017.10.017	journal	December 2017
The determination of pair distance distributions by pulsed ESR using Tikhonov regularization Chiang, Yun-Wei; Borbat, Peter P.; Freed, Jack H. Journal of Magnetic Resonance, Vol. 172, Issue 2 https://doi.org/10.1016/j.jmr.2004.10.012	journal	February 2005
Dephosphorylation of F-BAR Protein Cdc15 Modulates Its Conformation and Stimulates Its Scaffolding Activity at the Cell Division Site Roberts-Galbraith, Rachel H.; Ohi, Melanie D.; Ballif, Bryan A. Molecular Cell, Vol. 39, Issue 1 https://doi.org/10.1016/j.molcel.2010.06.012	journal	July 2010
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
Recent advances and applications of site-directed spin labeling Fanucci, G.; Cafiso, D. Current Opinion in Structural Biology, Vol. 16, Issue 5 https://doi.org/10.1016/j.sbi.2006.08.008	journal	October 2006
Influenza virus assembly and budding Rossman, Jeremy S.; Lamb, Robert A. Virology, Vol. 411, Issue 2 https://doi.org/10.1016/j.virol.2010.12.003	journal	March 2011
Herpesvirus assembly: An update Mettenleiter, Thomas C.; Klupp, Barbara G.; Granzow, Harald Virus Research, Vol. 143, Issue 2 https://doi.org/10.1016/j.virusres.2009.03.018	journal	August 2009
A New Wavelet Denoising Method for Experimental Time-Domain Signals: Pulsed Dipolar Electron Spin Resonance Srivastava, Madhur; Georgieva, Elka R.; Freed, Jack H. The Journal of Physical Chemistry A, Vol. 121, Issue 12 https://doi.org/10.1021/acs.jpca.7b00183	journal	March 2017
Singular Value Decomposition Method To Determine Distance Distributions in Pulsed Dipolar Electron Spin Resonance: II. Estimating Uncertainty Srivastava, Madhur; Freed, Jack H. The Journal of Physical Chemistry A, Vol. 123, Issue 1 https://doi.org/10.1021/acs.jpca.8b07673	journal	December 2018
Singular Value Decomposition Method to Determine Distance Distributions in Pulsed Dipolar Electron Spin Resonance Srivastava, Madhur; Freed, Jack H. The Journal of Physical Chemistry Letters, Vol. 8, Issue 22 https://doi.org/10.1021/acs.jpclett.7b02379	journal	November 2017
Molecular Motor Dnm1 Synergistically Induces Membrane Curvature To Facilitate Mitochondrial Fission Lee, Michelle W.; Lee, Ernest Y.; Lai, Ghee Hwee ACS Central Science, Vol. 3, Issue 11 https://doi.org/10.1021/acscentsci.7b00338	journal	November 2017
Calcium Ions Directly Interact with the Ebola Virus Fusion Peptide To Promote Structure–Function Changes That Enhance Infection Nathan, Lakshmi; Lai, Alex L.; Millet, Jean Kaoru ACS Infectious Diseases, Vol. 6, Issue 2 https://doi.org/10.1021/acsinfecdis.9b00296	journal	November 2019
Phosphatidylinositol 4,5-Bisphosphate Alters Synaptotagmin 1 Membrane Docking and Drives Opposing Bilayers Closer Together Kuo, Weiwei; Herrick, Dawn Z.; Cafiso, David S. Biochemistry, Vol. 50, Issue 13 https://doi.org/10.1021/bi200049c	journal	April 2011
Criterion for Amino Acid Composition of Defensins and Antimicrobial Peptides Based on Geometry of Membrane Destabilization Schmidt, Nathan W.; Mishra, Abhijit; Lai, Ghee Hwee Journal of the American Chemical Society, Vol. 133, Issue 17 https://doi.org/10.1021/ja200079a	journal	May 2011
Influenza Virus A M2 Protein Generates Negative Gaussian Membrane Curvature Necessary for Budding and Scission Schmidt, Nathan W.; Mishra, Abhijit; Wang, Jun Journal of the American Chemical Society, Vol. 135, Issue 37 https://doi.org/10.1021/ja400146z	journal	September 2013
Structure and Function in Antimicrobial Piscidins: Histidine Position, Directionality of Membrane Insertion, and pH-Dependent Permeabilization Mihailescu, Mihaela; Sorci, Mirco; Seckute, Jolita Journal of the American Chemical Society, Vol. 141, Issue 25 https://doi.org/10.1021/jacs.9b00440	journal	May 2019
Modulation of the Spontaneous Curvature and Bending Rigidity of Lipid Membranes by Interfacially Adsorbed Amphipathic Peptides Zemel, Assaf; Ben-Shaul, Avinoam; May, Sylvio The Journal of Physical Chemistry B, Vol. 112, Issue 23 https://doi.org/10.1021/jp711107y	journal	May 2008
Determination of Tie-Line Fields for Coexisting Lipid Phases: An ESR Study ^† Smith, Andrew K.; Freed, Jack H. The Journal of Physical Chemistry B, Vol. 113, Issue 12 https://doi.org/10.1021/jp808412x	journal	March 2009
An Assessment of the Applicability of Multifrequency ESR to Study the Complex Dynamics of Biomolecules Liang, Zhichun; Freed, Jack H. The Journal of Physical Chemistry B, Vol. 103, Issue 30 https://doi.org/10.1021/jp9907746	journal	July 1999
Improved Sensitivity for Long-Distance Measurements in Biomolecules: Five-Pulse Double Electron–Electron Resonance Borbat, Peter P.; Georgieva, Elka R.; Freed, Jack H. The Journal of Physical Chemistry Letters, Vol. 4, Issue 1 https://doi.org/10.1021/jz301788n	journal	December 2012
Structure and Function of the Membrane Anchoring Self-Assembled Monolayers Rakovska, Bozena; Ragaliauskas, Tadas; Mickevicius, Mindaugas Langmuir, Vol. 31, Issue 2 https://doi.org/10.1021/la503715b	journal	January 2015
A cost–benefit analysis of the physical mechanisms of membrane curvature Stachowiak, Jeanne C.; Brodsky, Frances M.; Miller, Elizabeth A. Nature Cell Biology, Vol. 15, Issue 9 https://doi.org/10.1038/ncb2832	journal	September 2013
Membrane deformation and scission by the HSV-1 nuclear egress complex Bigalke, Janna M.; Heuser, Thomas; Nicastro, Daniela Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5131	journal	June 2014
Using circular dichroism spectra to estimate protein secondary structure Greenfield, Norma J Nature Protocols, Vol. 1, Issue 6, p. 2876-2890 https://doi.org/10.1038/nprot.2006.202	journal	January 2007
How proteins produce cellular membrane curvature Zimmerberg, Joshua; Kozlov, Michael M. Nature Reviews Molecular Cell Biology, Vol. 7, Issue 1 https://doi.org/10.1038/nrm1784	journal	November 2005
Herpesviruses remodel host membranes for virus egress Johnson, David C.; Baines, Joel D. Nature Reviews Microbiology, Vol. 9, Issue 5 https://doi.org/10.1038/nrmicro2559	journal	April 2011
Cryo-electron microscopy reconstruction of a poliovirus-receptor-membrane complex Bubeck, Doryen; Filman, David J.; Hogle, James M. Nature Structural & Molecular Biology, Vol. 12, Issue 7 https://doi.org/10.1038/nsmb955	journal	June 2005
ESCRT-III mediates budding across the inner nuclear membrane and regulates its integrity Arii, Jun; Watanabe, Mizuki; Maeda, Fumio Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05889-9	journal	August 2018
Membrane constriction and thinning by sequential ESCRT-III polymerization Nguyen, Henry C.; Talledge, Nathaniel; McCullough, John Nature Structural & Molecular Biology, Vol. 27, Issue 4 https://doi.org/10.1038/s41594-020-0404-x	journal	April 2020
Mechanism of influenza A M2 transmembrane domain assembly in lipid membranes Georgieva, Elka R.; Borbat, Peter P.; Norman, Haley D. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep11757	journal	July 2015
Inside job: how the ESCRTs release HIV-1 from infected cells Hurley, James H.; Cada, A. King Biochemical Society Transactions, Vol. 46, Issue 5 https://doi.org/10.1042/BST20180019	journal	August 2018
AND/R: Advanced neutron diffractometer/reflectometer for investigation of thin films and multilayers for the life sciences Dura, Joseph A.; Pierce, Donald J.; Majkrzak, Charles F. Review of Scientific Instruments, Vol. 77, Issue 7 https://doi.org/10.1063/1.2219744	journal	July 2006
Continuous distribution model for the investigation of complex molecular architectures near interfaces with scattering techniques Shekhar, Prabhanshu; Nanda, Hirsh; Lösche, Mathias Journal of Applied Physics, Vol. 110, Issue 10 https://doi.org/10.1063/1.3661986	journal	November 2011
Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins Klupp, B. G.; Granzow, H.; Fuchs, W. Proceedings of the National Academy of Sciences, Vol. 104, Issue 17 https://doi.org/10.1073/pnas.0701757104	journal	April 2007
Membrane-binding and activation mechanism of PTEN Das, S.; Dixon, J. E.; Cho, W. Proceedings of the National Academy of Sciences, Vol. 100, Issue 13 https://doi.org/10.1073/pnas.0932835100	journal	June 2003
Phosphorylation of syndapin I F-BAR domain at two helix-capping motifs regulates membrane tubulation Quan, Annie; Xue, Jing; Wielens, Jerome Proceedings of the National Academy of Sciences, Vol. 109, Issue 10 https://doi.org/10.1073/pnas.1108294109	journal	February 2012
Translocation of HIV TAT peptide and analogues induced by multiplexed membrane and cytoskeletal interactions Mishra, A.; Lai, G. H.; Schmidt, N. W. Proceedings of the National Academy of Sciences, Vol. 108, Issue 41 https://doi.org/10.1073/pnas.1108795108	journal	October 2011
Structural interactions of a voltage sensor toxin with lipid membranes Mihailescu, Mihaela; Krepkiy, Dmitriy; Milescu, Mirela Proceedings of the National Academy of Sciences, Vol. 111, Issue 50 https://doi.org/10.1073/pnas.1415324111	journal	December 2014
Viral fusion protein transmembrane domain adopts β-strand structure to facilitate membrane topological changes for virus–cell fusion Yao, Hongwei; Lee, Michelle W.; Waring, Alan J. Proceedings of the National Academy of Sciences, Vol. 112, Issue 35 https://doi.org/10.1073/pnas.1501430112	journal	August 2015
Mapping membrane activity in undiscovered peptide sequence space using machine learning Lee, Ernest Y.; Fulan, Benjamin M.; Wong, Gerard C. L. Proceedings of the National Academy of Sciences, Vol. 113, Issue 48 https://doi.org/10.1073/pnas.1609893113	journal	November 2016
Amino-terminal basic residues of Src mediate membrane binding through electrostatic interaction with acidic phospholipids. Sigal, C. T.; Zhou, W.; Buser, C. A. Proceedings of the National Academy of Sciences, Vol. 91, Issue 25 https://doi.org/10.1073/pnas.91.25.12253	journal	December 1994
A collision gradient method to determine the immersion depth of nitroxides in lipid bilayers: application to spin-labeled mutants of bacteriorhodopsin. Altenbach, C.; Greenhalgh, D. A.; Khorana, H. G. Proceedings of the National Academy of Sciences, Vol. 91, Issue 5 https://doi.org/10.1073/pnas.91.5.1667	journal	March 1994
Phosphorylation of Dynamin I on Ser-795 by Protein Kinase C Blocks Its Association with Phospholipids Powell, Kate A.; Valova, Valentina A.; Malladi, Chandra S. Journal of Biological Chemistry, Vol. 275, Issue 16 https://doi.org/10.1074/jbc.275.16.11610	journal	April 2000
Crystal Structure of the Human Cytomegalovirus pUL50-pUL53 Core Nuclear Egress Complex Provides Insight into a Unique Assembly Scaffold for Virus-Host Protein Interactions Walzer, Sascha A.; Egerer-Sieber, Claudia; Sticht, Heinrich Journal of Biological Chemistry, Vol. 290, Issue 46 https://doi.org/10.1074/jbc.C115.686527	journal	November 2015
The Lipid-binding Domain of Wild Type and Mutant α-Synuclein Georgieva, Elka R.; Ramlall, Trudy F.; Borbat, Peter P. Journal of Biological Chemistry, Vol. 285, Issue 36 https://doi.org/10.1074/jbc.M110.157214	journal	September 2010
The Ebola Virus Matrix Protein VP40 Selectively Induces Vesiculation from Phosphatidylserine-enriched Membranes Soni, Smita P.; Stahelin, Robert V. Journal of Biological Chemistry, Vol. 289, Issue 48 https://doi.org/10.1074/jbc.M114.586396	journal	October 2014
A Single Herpesvirus Protein Can Mediate Vesicle Formation in the Nuclear Envelope Lorenz, Michael; Vollmer, Benjamin; Unsay, Joseph D. Journal of Biological Chemistry, Vol. 290, Issue 11 https://doi.org/10.1074/jbc.M114.627521	journal	January 2015
Involvement of Vacuolar Protein Sorting Pathway in Ebola Virus Release Independent of TSG101 Interaction Silvestri, Lynn S.; Ruthel, Gordon; Kallstrom, George The Journal of Infectious Diseases, Vol. 196, Issue s2 https://doi.org/10.1086/520610	journal	November 2007
Inverse lyotropic phases of lipids and membrane curvature Shearman, G. C.; Ces, O.; Templer, R. H. Journal of Physics: Condensed Matter, Vol. 18, Issue 28 https://doi.org/10.1088/0953-8984/18/28/S01	journal	June 2006
The 2018 biomembrane curvature and remodeling roadmap Bassereau, Patricia; Jin, Rui; Baumgart, Tobias Journal of Physics D: Applied Physics, Vol. 51, Issue 34 https://doi.org/10.1088/1361-6463/aacb98	journal	July 2018
The EMBL-EBI search and sequence analysis tools APIs in 2019 Madeira, Fábio; Park, Young mi; Lee, Joon Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz268	journal	April 2019
Membrane curvature induced by polymer adsorption Kim, Yong Woon; Sung, Wokyung Physical Review E, Vol. 63, Issue 4 https://doi.org/10.1103/PhysRevE.63.041910	journal	March 2001
Nika : software for two-dimensional data reduction Ilavsky, Jan Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812004037	journal	March 2012
A New Wavelet Denoising Method for Selecting Decomposition Levels and Noise Thresholds Srivastava, Madhur; Anderson, C. Lindsay; Freed, Jack H. IEEE Access, Vol. 4 https://doi.org/10.1109/ACCESS.2016.2587581	journal	January 2016
XSEDE: Accelerating Scientific Discovery Towns, John; Cockerill, Timothy; Dahan, Maytal Computing in Science & Engineering, Vol. 16, Issue 5 https://doi.org/10.1109/MCSE.2014.80	journal	September 2014
ESCRT-III CHMP2A and CHMP3 form variable helical polymers in vitro and act synergistically during HIV-1 budding : Structure of CHMP2A-CHMP3 tubes and HIV-1 budding Effantin, Grégory; Dordor, Aurélien; Sandrin, Virginie Cellular Microbiology, Vol. 15, Issue 2 https://doi.org/10.1111/cmi.12041	journal	November 2012
ESCRT-III and Vps4: a dynamic multipurpose tool for membrane budding and scission Alonso Y. Adell, Manuel; Migliano, Simona M.; Teis, David The FEBS Journal, Vol. 283, Issue 18 https://doi.org/10.1111/febs.13688	journal	March 2016
Spin Labeled Cysteines as Sensors for Protein-Lipid Interaction and Conformation in Rhodopsin Farahbakhsh, Zohreh T.; Altenbach, Christian; Hubbell, Wayne L. Photochemistry and Photobiology, Vol. 56, Issue 6 https://doi.org/10.1111/j.1751-1097.1992.tb09725.x	journal	December 1992
BAR Domains as Sensors of Membrane Curvature: The Amphiphysin BAR Structure Peter, B. J. Science, Vol. 303, Issue 5657 https://doi.org/10.1126/science.1092586	journal	January 2004
An atomic model of HIV-1 capsid-SP1 reveals structures regulating assembly and maturation Schur, Florian K. M.; Obr, Martin; Hagen, Wim J. H. Science, Vol. 353, Issue 6298 https://doi.org/10.1126/science.aaf9620	journal	July 2016
Phosphorylation of the UL31 Protein of Herpes Simplex Virus 1 by the US3-Encoded Kinase Regulates Localization of the Nuclear Envelopment Complex and Egress of Nucleocapsids Mou, F.; Wills, E.; Baines, J. D. Journal of Virology, Vol. 83, Issue 10 https://doi.org/10.1128/JVI.00090-09	journal	March 2009
Herpes Simplex Virus Type 1 Cytoplasmic Envelopment Requires Functional Vps4 Crump, Colin M.; Yates, Catherine; Minson, Tony Journal of Virology, Vol. 81, Issue 14 https://doi.org/10.1128/JVI.00222-07	journal	July 2007
Structural Determinants for Nuclear Envelope Localization and Function of Pseudorabies Virus pUL34 Schuster, Franziska; Klupp, Barbara G.; Granzow, Harald Journal of Virology, Vol. 86, Issue 7 https://doi.org/10.1128/JVI.00251-12	journal	April 2012
Herpes Simplex Virus 1 pUL34 Plays a Critical Role in Cell-to-Cell Spread of Virus in Addition to Its Role in Virus Replication Haugo, Alison C.; Szpara, Moriah L.; Parsons, Lance Journal of Virology, Vol. 85, Issue 14 https://doi.org/10.1128/JVI.00262-11	journal	July 2011
Roles of the Interhexamer Contact Site for Hexagonal Lattice Formation of the Herpes Simplex Virus 1 Nuclear Egress Complex in Viral Primary Envelopment and Replication Arii, Jun; Takeshima, Kosuke; Maruzuru, Yuhei Journal of Virology, Vol. 93, Issue 14 https://doi.org/10.1128/JVI.00498-19	journal	May 2019
Function of the Nonconserved N-Terminal Domain of Pseudorabies Virus pUL31 in Nuclear Egress Klupp, Barbara G.; Hellberg, Teresa; Rönfeldt, Sebastian Journal of Virology, Vol. 92, Issue 15 https://doi.org/10.1128/JVI.00566-18	journal	August 2018
Membrane Requirement for Folding of the Herpes Simplex Virus 1 gB Cytodomain Suggests a Unique Mechanism of Fusion Regulation Silverman, J. L.; Greene, N. G.; King, D. S. Journal of Virology, Vol. 86, Issue 15 https://doi.org/10.1128/JVI.00932-12	journal	May 2012
Analysis of a Charge Cluster Mutation of Herpes Simplex Virus Type 1 UL34 and Its Extragenic Suppressor Suggests a Novel Interaction between pUL34 and pUL31 That Is Necessary for Membrane Curvature around Capsids Roller, R. J.; Bjerke, S. L.; Haugo, A. C. Journal of Virology, Vol. 84, Issue 8 https://doi.org/10.1128/JVI.01638-09	journal	January 2010
Mechanism of Nuclear Lamina Disruption and the Role of pUS3 in Herpes Simplex Virus 1 Nuclear Egress Masoud Bahnamiri, Masoudeh; Roller, Richard J. Journal of Virology, Vol. 95, Issue 10 https://doi.org/10.1128/JVI.02432-20	journal	April 2021
Deletion of Epstein-Barr Virus BFLF2 Leads to Impaired Viral DNA Packaging and Primary Egress as Well as to the Production of Defective Viral Particles Granato, Marisa; Feederle, Regina; Farina, Antonella Journal of Virology, Vol. 82, Issue 8 https://doi.org/10.1128/JVI.02436-07	journal	April 2008
The Herpes Simplex Virus 2 UL21 Protein Is Essential for Virus Propagation Le Sage, Valerie; Jung, Masany; Alter, Jake D. Journal of Virology, Vol. 87, Issue 10 https://doi.org/10.1128/JVI.03489-12	journal	May 2013
Reconstitution of the Kaposi's Sarcoma-Associated Herpesvirus Nuclear Egress Complex and Formation of Nuclear Membrane Vesicles by Coexpression of ORF67 and ORF69 Gene Products Desai, P. J.; Pryce, E. N.; Henson, B. W. Journal of Virology, Vol. 86, Issue 1 https://doi.org/10.1128/JVI.05988-11	journal	October 2011
The product of the UL31 gene of herpes simplex virus 1 is a nuclear phosphoprotein which partitions with the nuclear matrix. Chang, Y. E.; Roizman, B. Journal of Virology, Vol. 67, Issue 11 https://doi.org/10.1128/JVI.67.11.6348-6356.1993	journal	January 1993
Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids Zhou, W.; Parent, L. J.; Wills, J. W. Journal of Virology, Vol. 68, Issue 4 https://doi.org/10.1128/JVI.68.4.2556-2569.1994	journal	April 1994
The null mutant of the U(L)31 gene of herpes simplex virus 1: construction and phenotype in infected cells Chang, Y. E.; Van Sant, C.; Krug, P. W. Journal of Virology, Vol. 71, Issue 11 https://doi.org/10.1128/JVI.71.11.8307-8315.1997	journal	November 1997
Herpes Simplex Virus Type 1 UL34 Gene Product Is Required for Viral Envelopment Roller, R. J.; Zhou, Y.; Schnetzer, R. Journal of Virology, Vol. 74, Issue 1 https://doi.org/10.1128/JVI.74.1.117-129.2000	journal	January 2000
Comprehensive Mutational Analysis of a Herpesvirus Gene in the Viral Genome Context Reveals a Region Essential for Virus Replication Bubeck, A.; Wagner, M.; Ruzsics, Z. Journal of Virology, Vol. 78, Issue 15 https://doi.org/10.1128/JVI.78.15.8026-8035.2004	journal	July 2004
Identification of Proteins Phosphorylated Directly by the Us3 Protein Kinase Encoded by Herpes Simplex Virus 1 Kato, Akihisa; Yamamoto, Mayuko; Ohno, Takashi Journal of Virology, Vol. 79, Issue 14 https://doi.org/10.1128/JVI.79.14.9325-9331.2005	journal	July 2005
BFRF1 of Epstein-Barr Virus Is Essential for Efficient Primary Viral Envelopment and Egress Farina, Antonella; Feederle, Regina; Raffa, Salvatore Journal of Virology, Vol. 79, Issue 6 https://doi.org/10.1128/JVI.79.6.3703-3712.2005	journal	March 2005
Functional Domains of Murine Cytomegalovirus Nuclear Egress Protein M53/p38 Lötzerich, Mark; Ruzsics, Zsolt; Koszinowski, Ulrich H. Journal of Virology, Vol. 80, Issue 1 https://doi.org/10.1128/JVI.80.1.73-84.2006	journal	January 2006
Primary Envelopment of Pseudorabies Virus at the Nuclear Membrane Requires the UL34 Gene Product Klupp, Barbara G.; Granzow, Harald; Mettenleiter, Thomas C. Journal of Virology, Vol. 74, Issue 21 https://doi.org/10.1128/jvi.74.21.10063-10073.2000	journal	November 2000
The Interacting UL31 and UL34 Gene Products of Pseudorabies Virus Are Involved in Egress from the Host-Cell Nucleus and Represent Components of Primary Enveloped but Not Mature Virions Fuchs, W.; Klupp, B. G.; Granzow, H. Journal of Virology, Vol. 76, Issue 1 https://doi.org/10.1128/jvi.76.1.364-378.2002	journal	January 2002
Ultrastructural Localization of the Herpes Simplex Virus Type 1 UL31, UL34, and US3 Proteins Suggests Specific Roles in Primary Envelopment and Egress of Nucleocapsids Reynolds, A. E.; Wills, E. G.; Roller, R. J. Journal of Virology, Vol. 76, Issue 17 https://doi.org/10.1128/jvi.76.17.8939-8952.2002	journal	September 2002
Overlapping Motifs (PTAP and PPEY) within the Ebola Virus VP40 Protein Function Independently as Late Budding Domains: Involvement of Host Proteins TSG101 and VPS-4 Licata, J. M.; Simpson-Holley, M.; Wright, N. T. Journal of Virology, Vol. 77, Issue 3 https://doi.org/10.1128/jvi.77.3.1812-1819.2003	journal	February 2003
Herpes Simplex Virus Type 1 Primary Envelopment: UL34 Protein Modification and the US3-UL34 Catalytic Relationship Ryckman, Brent J.; Roller, Richard J. Journal of Virology, Vol. 78, Issue 1 https://doi.org/10.1128/jvi.78.1.399-412.2004	journal	January 2004
The Primary Enveloped Virion of Herpes Simplex Virus 1: Its Role in Nuclear Egress Newcomb, William W.; Fontana, Juan; Winkler, Dennis C. mBio, Vol. 8, Issue 3 https://doi.org/10.1128/mBio.00825-17	journal	July 2017
Bridges: a uniquely flexible HPC resource for new communities and data analytics Nystrom, Nicholas A.; Levine, Michael J.; Roskies, Ralph Z. Proceedings of the 2015 XSEDE Conference on Scientific Advancements Enabled by Enhanced Cyberinfrastructure - XSEDE '15 https://doi.org/10.1145/2792745.2792775	conference	January 2015
Structures, Functions, and Dynamics of ESCRT-III/Vps4 Membrane Remodeling and Fission Complexes McCullough, John; Frost, Adam; Sundquist, Wesley I. Annual Review of Cell and Developmental Biology, Vol. 34, Issue 1 https://doi.org/10.1146/annurev-cellbio-100616-060600	journal	October 2018
Curving Cells Inside and Out: Roles of BAR Domain Proteins in Membrane Shaping and Its Cellular Implications Simunovic, Mijo; Evergren, Emma; Callan-Jones, Andrew Annual Review of Cell and Developmental Biology, Vol. 35, Issue 1 https://doi.org/10.1146/annurev-cellbio-100617-060558	journal	October 2019
Viral Membrane Scission Rossman, Jeremy S.; Lamb, Robert A. Annual Review of Cell and Developmental Biology, Vol. 29, Issue 1 https://doi.org/10.1146/annurev-cellbio-101011-155838	journal	October 2013
Membrane curvature at a glance McMahon, H. T.; Boucrot, E. Journal of Cell Science, Vol. 128, Issue 6 https://doi.org/10.1242/jcs.114454	journal	March 2015
RosettaEPR: Rotamer Library for Spin Label Structure and Dynamics Alexander, Nathan S.; Stein, Richard A.; Koteiche, Hanane A. PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0072851	journal	September 2013
Accelerating Markov Chain Monte Carlo Simulation by Differential Evolution with Self-Adaptive Randomized Subspace Sampling Vrugt, J. A.; ter Braak, C. J. F.; Diks, C. G. H. International Journal of Nonlinear Sciences and Numerical Simulation, Vol. 10, Issue 3 https://doi.org/10.1515/IJNSNS.2009.10.3.273	journal	January 2009
Structural basis of membrane budding by the nuclear egress complex of herpesviruses Bigalke, Janna M.; Heldwein, Ekaterina E. The EMBO Journal, Vol. 34, Issue 23 https://doi.org/10.15252/embj.201592359	journal	October 2015
ESCRT s are everywhere Hurley, James H. The EMBO Journal, Vol. 34, Issue 19 https://doi.org/10.15252/embj.201592484	journal	August 2015
Unexpected features and mechanism of heterodimer formation of a herpesvirus nuclear egress complex Lye, Ming F.; Sharma, Mayuri; El Omari, Kamel The EMBO Journal, Vol. 34, Issue 23 https://doi.org/10.15252/embj.201592651	journal	October 2015
The Hydrophobic Insertion Mechanism of Membrane Curvature Generation by Proteins Campelo, Felix; McMahon, Harvey T.; Kozlov, Michael M. Biophysical Journal, Vol. 95, Issue 5 https://doi.org/10.1529/biophysj.108.133173	journal	September 2008
Nuclear Egress of Herpesviruses Draganova, Elizabeth B.; Thorsen, Michael K.; Heldwein, Ekaterina E. Current Issues in Molecular Biology https://doi.org/10.21775/cimb.041.125	journal	January 2021
Unique Structural Features of Membrane-Bound C-Terminal Domain Motifs Modulate Complexin Inhibitory Function Snead, David; Lai, Alex L.; Wragg, Rachel T. Frontiers in Molecular Neuroscience, Vol. 10 https://doi.org/10.3389/fnmol.2017.00154	journal	May 2017
Host and Viral Proteins Modulating Ebola and Marburg Virus Egress Gordon, Tamsin B.; Hayward, Joshua A.; Marsh, Glenn A. Viruses, Vol. 11, Issue 1 https://doi.org/10.3390/v11010025	journal	January 2019
Direct Antimicrobial Activity of IFN-β Kaplan, Amber; Lee, Michelle W.; Wolf, Andrea J. The Journal of Immunology, Vol. 198, Issue 10 https://doi.org/10.4049/jimmunol.1601226	journal	April 2017

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membrane curvature
membrane deformation
60 APPLIED LIFE SCIENCES
HSV-1
Microbiology
charge clusters
complex
electron spin resonance
electrostatics
herpes simplex virus
herpes viruses
membrane budding
membrane interactions
neutron reflectometry
nuclear egress
phosphorylation
small-angle X-ray scattering

Title: Highly Basic Clusters in the Herpes Simplex Virus 1 Nuclear Egress Complex Drive Membrane Budding by Inducing Lipid Ordering

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