The 2.1 Å structure of protein F9 and its comparison to L1, two components of the conserved poxvirus entry-fusion complex

Diesterbeck, Ulrike S.; Gittis, Apostolos G.; Garboczi, David N.; Moss, Bernard

doi:10.1038/s41598-018-34244-7

Title: The 2.1 Å structure of protein F9 and its comparison to L1, two components of the conserved poxvirus entry-fusion complex

Journal Article · Wed Nov 14 00:00:00 EST 2018 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-018-34244-7· OSTI ID:1624434

Diesterbeck, Ulrike S. ^[1]; Gittis, Apostolos G. ^[2]; Garboczi, David N. ^[2];

^[1]

National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Diseases (NIAID)
National Inst. of Health (NIH), Rockville, MD (United States). National Inst. of Allergy and Infectious Diseases (NIAID)

The poxvirus F9 protein is a component of the vaccinia virus entry fusion complex (EFC) which consists of 11 proteins. The EFC forms a unique apparatus among viral fusion proteins and complexes. We solved the atomic structure of the F9 ectodomain at 2.10Å. A structural comparison to the ectodomain of the EFC protein L1 indicated a similar fold and organization, in which a bundle of fve α-helices is packed against two pairs of β-strands. However, instead of the L1 myristoylation site and hydrophobic cavity, F9 possesses a protruding loop between α-helices α3 and α4 starting at Gly90. Gly90 is conserved in all poxviruses except Salmon gill poxvirus (SGPV) and Diachasmimorpha longicaudata entomopoxvirus. Phylogenetic sequence analysis of all Poxviridae F9 and L1 orthologs revealed the SGPV genome to contain the most distantly related F9 and L1 sequences compared to the vaccinia proteins studied here. The structural diferences between F9 and L1 suggest functional adaptations during evolution from a common precursor that underlie the present requirement for each protein.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institute of Allergy and Infectious Diseases (NIAID); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1624434

Journal Information:: Scientific Reports, Vol. 8, Issue 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 15 works

Citation information provided by
Web of Science

References (62)

The Product of the Vaccinia Virus L5R Gene Is a Fourth Membrane Protein Encoded by All Poxviruses That Is Required for Cell Entry and Cell-Cell Fusion Townsley, Alan C.; Senkevich, Tatiana G.; Moss, Bernard Journal of Virology, Vol. 79, Issue 17 https://doi.org/10.1128/JVI.79.17.10988-10998.2005	journal	September 2005
Principles of protein-protein interactions. Jones, S.; Thornton, J. M. Proceedings of the National Academy of Sciences, Vol. 93, Issue 1 https://doi.org/10.1073/pnas.93.1.13	journal	January 1996
The 1.51-A structure of the poxvirus L1 protein, a target of potent neutralizing antibodies Su, H. -P.; Garman, S. C.; Allison, T. J. Proceedings of the National Academy of Sciences, Vol. 102, Issue 12 https://doi.org/10.1073/pnas.0501103102	journal	March 2005
A Myristylated Membrane Protein Encoded by the Vaccinia Virus L1R Open Reading Frame Is the Target of Potent Neutralizing Monoclonal Antibodies Wolffe, Elizabeth J.; Vijaya, S.; Moss, Bernard Virology, Vol. 211, Issue 1 https://doi.org/10.1006/viro.1995.1378	journal	August 1995
Dali server update Holm, Liisa; Laakso, Laura M. Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw357	journal	April 2016
Entry of the vaccinia virus intracellular mature virion and its interactions with glycosaminoglycans Carter, Gemma C.; Law, Mansun; Hollinshead, Michael Journal of General Virology, Vol. 86, Issue 5 https://doi.org/10.1099/vir.0.80831-0	journal	May 2005
A viral member of the ERV1/ALR protein family participates in a cytoplasmic pathway of disulfide bond formation Senkevich, T. G.; White, C. L.; Koonin, E. V. Proceedings of the National Academy of Sciences, Vol. 97, Issue 22 https://doi.org/10.1073/pnas.210397997	journal	October 2000
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Thompson, J. Nucleic Acids Research, Vol. 25, Issue 24 https://doi.org/10.1093/nar/25.24.4876	journal	December 1997
Vaccinia Virus A56/K2 Fusion Regulatory Protein Interacts with the A16 and G9 Subunits of the Entry Fusion Complex Wagenaar, Timothy R.; Ojeda, Suany; Moss, Bernard Journal of Virology, Vol. 82, Issue 11 https://doi.org/10.1128/JVI.00162-08	journal	March 2008
Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Krissinel, E.; Henrick, K. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904026460	journal	November 2004
The Membrane Fusion Step of Vaccinia Virus Entry Is Cooperatively Mediated by Multiple Viral Proteins and Host Cell Components Laliberte, Jason P.; Weisberg, Andrea S.; Moss, Bernard PLoS Pathogens, Vol. 7, Issue 12 https://doi.org/10.1371/journal.ppat.1002446	journal	December 2011
Improved methods for building protein models in electron density maps and the location of errors in these models Jones, T. A.; Zou, J. Y.; Cowan, S. W. Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 2, p. 110-119 https://doi.org/10.1107/S0108767390010224	journal	March 1991
The Structure of G4, the Poxvirus Disulfide Oxidoreductase Essential for Virus Maturation and Infectivity Su, H. -P.; Lin, D. Y. -w.; Garboczi, D. N. Journal of Virology, Vol. 80, Issue 15 https://doi.org/10.1128/JVI.00521-06	journal	July 2006
Ligand-induced and nonfusogenic dissolution of a viral membrane Law, M.; Carter, G. C.; Roberts, K. L. Proceedings of the National Academy of Sciences, Vol. 103, Issue 15 https://doi.org/10.1073/pnas.0601025103	journal	April 2006
Hydrodynamic Radii of Native and Denatured Proteins Measured by Pulse Field Gradient NMR Techniques ^† Wilkins, Deborah K.; Grimshaw, Shaun B.; Receveur, Véronique Biochemistry, Vol. 38, Issue 50 https://doi.org/10.1021/bi991765q	journal	December 1999
I-TASSER server for protein 3D structure prediction Zhang, Yang BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-40	journal	January 2008
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Vaccinia Virus F9 Virion Membrane Protein Is Required for Entry but Not Virus Assembly, in Contrast to the Related L1 Protein Brown, Erica; Senkevich, Tatiana G.; Moss, Bernard Journal of Virology, Vol. 80, Issue 19 https://doi.org/10.1128/JVI.01149-06	journal	October 2006
Entering a New Phase Dauter, Zbigniew; Dauter, Miroslawa Structure, Vol. 9, Issue 2 https://doi.org/10.1016/S0969-2126(01)00565-2	journal	February 2001
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform Katoh, K. Nucleic Acids Research, Vol. 30, Issue 14 https://doi.org/10.1093/nar/gkf436	journal	July 2002
A simple method for displaying the hydropathic character of a protein Kyte, Jack; Doolittle, Russell F. Journal of Molecular Biology, Vol. 157, Issue 1, p. 105-132 https://doi.org/10.1016/0022-2836(82)90515-0	journal	May 1982
Ten years of probabilistic estimates of biocrystal solvent content: new insights via nonparametric kernel density estimate Weichenberger, Christian X.; Rupp, Bernhard Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 6 https://doi.org/10.1107/S1399004714005550	journal	May 2014
Interaction between the G3 and L5 proteins of the vaccinia virus entry–fusion complex Wolfe, Cindy L.; Moss, Bernard Virology, Vol. 412, Issue 2 https://doi.org/10.1016/j.virol.2011.01.014	journal	April 2011
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Dendroscope 3: An Interactive Tool for Rooted Phylogenetic Trees and Networks Huson, Daniel H.; Scornavacca, Celine Systematic Biology, Vol. 61, Issue 6 https://doi.org/10.1093/sysbio/sys062	journal	September 2012
Why similar protein sequences encode similar three-dimensional structures? Kaczanowski, Szymon; Zielenkiewicz, Piotr Theoretical Chemistry Accounts, Vol. 125, Issue 3-6 https://doi.org/10.1007/s00214-009-0656-3	journal	October 2009
Expression and Purification of Soluble His6-Tagged TEV Protease Tropea, Joseph E.; Cherry, Scott; Waugh, David S. Methods in Molecular Biology https://doi.org/10.1007/978-1-59745-196-3_19	book	January 2009
Solvent content of protein crystals Matthews, B. W. Journal of Molecular Biology, Vol. 33, Issue 2 https://doi.org/10.1016/0022-2836(68)90205-2	journal	April 1968
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Poxvirus multiprotein entry-fusion complex Senkevich, T. G.; Ojeda, S.; Townsley, A. Proceedings of the National Academy of Sciences, Vol. 102, Issue 51 https://doi.org/10.1073/pnas.0509239102	journal	December 2005
Cross-Neutralizing and Protective Human Antibody Specificities to Poxvirus Infections Gilchuk, Iuliia; Gilchuk, Pavlo; Sapparapu, Gopal Cell, Vol. 167, Issue 3 https://doi.org/10.1016/j.cell.2016.09.049	journal	October 2016
Poxvirus membrane biogenesis Moss, Bernard Virology, Vol. 479-480 https://doi.org/10.1016/j.virol.2015.02.003	journal	May 2015
Version 1.2 of the Crystallography and NMR system Brunger, Axel T. Nature Protocols, Vol. 2, Issue 11 https://doi.org/10.1038/nprot.2007.406	journal	October 2007
Vaccinia Virus Uses Macropinocytosis and Apoptotic Mimicry to Enter Host Cells Mercer, J.; Helenius, A. Science, Vol. 320, Issue 5875 https://doi.org/10.1126/science.1155164	journal	April 2008
The exit of Vaccinia virus from infected cells Smith, Geoffrey L.; Law, Mansun Virus Research, Vol. 106, Issue 2 https://doi.org/10.1016/j.virusres.2004.08.015	journal	December 2004
meta-PPISP: a meta web server for protein-protein interaction site prediction Qin, S.; Zhou, H. -X. Bioinformatics, Vol. 23, Issue 24 https://doi.org/10.1093/bioinformatics/btm434	journal	September 2007
Matthews coefficient probabilities: Improved estimates for unit cell contents of proteins, DNA, and protein-nucleic acid complex crystals Kantardjieff, Katherine A.; Rupp, Bernhard Protein Science, Vol. 12, Issue 9 https://doi.org/10.1110/ps.0350503	journal	September 2003
Membrane fusion during poxvirus entry Moss, Bernard Seminars in Cell & Developmental Biology, Vol. 60 https://doi.org/10.1016/j.semcdb.2016.07.015	journal	December 2016
Structural basis for the binding of the neutralizing antibody, 7D11, to the poxvirus L1 protein Su, Hua-Poo; Golden, Joseph W.; Gittis, Apostolos G. Virology, Vol. 368, Issue 2 https://doi.org/10.1016/j.virol.2007.06.042	journal	November 2007
A27L Protein Mediates Vaccinia Virus Interaction with Cell Surface Heparan Sulfate Chung, Che-Sheng; Hsiao, Jye-Chian; Chang, Yuan-Shau Journal of Virology, Vol. 72, Issue 2 https://doi.org/10.1128/JVI.72.2.1577-1585.1998	journal	February 1998
Characterization of a Bacillus megaterium strain with metal bioremediation potential and in silico discovery of novel cadmium binding motifs in the regulator, CadC Kumari, Weerasingha Mudiyanselage Nilmini H.; Thiruchittampalam, Shalini; Weerasinghe, Mahinagoda Siril Samantha Applied Microbiology and Biotechnology, Vol. 105, Issue 6 https://doi.org/10.1007/s00253-021-11193-2	journal	March 2021
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Comparative analyses of the mitochondrial genomes of the cattle tick Rhipicephalus microplus clades A and B from China Deng, Yuan-Ping; Yi, Jia-Ning; Fu, Yi-Tian Parasitology Research, Vol. 121, Issue 6 https://doi.org/10.1007/s00436-022-07501-y	journal	April 2022
Structure of polymerized type V pilin reveals assembly mechanism involving protease-mediated strand exchange Shibata, Satoshi; Shoji, Mikio; Okada, Kodai Nature Microbiology, Vol. 5, Issue 6 https://doi.org/10.1038/s41564-020-0705-1	journal	April 2020
A Conserved Sequence within the H2 Subunit of the Vaccinia Virus Entry/Fusion Complex Is Important for Interaction with the A28 Subunit and Infectivity Nelson, Gretchen E.; Wagenaar, Timothy R.; Moss, Bernard Journal of Virology, Vol. 82, Issue 13 https://doi.org/10.1128/jvi.00434-08	journal	April 2008
The Envelope G3L Protein Is Essential for Entry of Vaccinia Virus into Host Cells Izmailyan, Ruzan A.; Huang, Cheng-Yen; Mohammad, Shamim Journal of Virology, Vol. 80, Issue 17 https://doi.org/10.1128/jvi.00624-06	journal	September 2006
Vaccinia Virus L1 Protein Is Required for Cell Entry and Membrane Fusion Bisht, Himani; Weisberg, Andrea S.; Moss, Bernard Journal of Virology, Vol. 82, Issue 17 https://doi.org/10.1128/jvi.00852-08	journal	July 2008
Vaccinia Virus G9 Protein Is an Essential Component of the Poxvirus Entry-Fusion Complex Ojeda, Suany; Domi, Arban; Moss, Bernard Journal of Virology, Vol. 80, Issue 19 https://doi.org/10.1128/jvi.00987-06	journal	October 2006
Vaccinia Virus Entry into Cells via a Low-pH-Dependent Endosomal Pathway Townsley, Alan C.; Weisberg, Andrea S.; Wagenaar, Timothy R. Journal of Virology, Vol. 80, Issue 18 https://doi.org/10.1128/jvi.01053-06	journal	September 2006
Salmon Gill Poxvirus, the Deepest Representative of the Chordopoxvirinae Gjessing, Mona C.; Yutin, Natalya; Tengs, Torstein Journal of Virology, Vol. 89, Issue 18 https://doi.org/10.1128/jvi.01174-15	journal	July 2015
Characterization of a Newly Identified 35-Amino-Acid Component of the Vaccinia Virus Entry/Fusion Complex Conserved in All Chordopoxviruses Satheshkumar, P. S.; Moss, Bernard Journal of Virology, Vol. 83, Issue 24 https://doi.org/10.1128/jvi.01744-09	journal	October 2009
The Myristate Moiety and Amino Terminus of Vaccinia Virus L1 Constitute a Bipartite Functional Region Needed for Entry Foo, C. H.; Whitbeck, J. C.; Ponce-de-Leon, M. Journal of Virology, Vol. 86, Issue 10 https://doi.org/10.1128/jvi.06703-11	journal	March 2012
Vaccinia Virus Envelope D8L Protein Binds to Cell Surface Chondroitin Sulfate and Mediates the Adsorption of Intracellular Mature Virions to Cells Hsiao, Jye-Chian; Chung, Che-Sheng; Chang, Wen Journal of Virology, Vol. 73, Issue 10 https://doi.org/10.1128/jvi.73.10.8750-8761.1999	journal	October 1999
Vaccinia Virus Envelope H3L Protein Binds to Cell Surface Heparan Sulfate and Is Important for Intracellular Mature Virion Morphogenesis and Virus Infection In Vitro and In Vivo Lin, C. -L.; Chung, C. -S.; Heine, H. G. Journal of Virology, Vol. 74, Issue 7 https://doi.org/10.1128/jvi.74.7.3353-3365.2000	journal	April 2000
Vaccinia Virus A28L Gene Encodes an Essential Protein Component of the Virion Membrane with Intramolecular Disulfide Bonds Formed by the Viral Cytoplasmic Redox Pathway Senkevich, Tatiana G.; Ward, Brian M.; Moss, Bernard Journal of Virology, Vol. 78, Issue 5 https://doi.org/10.1128/jvi.78.5.2348-2356.2004	journal	March 2004
Vaccinia Virus A21 Virion Membrane Protein Is Required for Cell Entry and Fusion Townsley, Alan C.; Senkevich, Tatiana G.; Moss, Bernard Journal of Virology, Vol. 79, Issue 15 https://doi.org/10.1128/jvi.79.15.9458-9469.2005	journal	August 2005
Vaccinia Virus H2 Protein Is an Essential Component of a Complex Involved in Virus Entry and Cell-Cell Fusion Senkevich, Tatiana G.; Moss, Bernard Journal of Virology, Vol. 79, Issue 8 https://doi.org/10.1128/jvi.79.8.4744-4754.2005	journal	April 2005
Entry of Vaccinia Virus and Cell-Cell Fusion Require a Highly Conserved Cysteine-Rich Membrane Protein Encoded by the A16L Gene Ojeda, Suany; Senkevich, Tatiana G.; Moss, Bernard Journal of Virology, Vol. 80, Issue 1 https://doi.org/10.1128/jvi.80.1.51-61.2006	journal	January 2006

Cited By (1)

Species-Specific Conservation of Linear Antigenic Sites on Vaccinia Virus A27 Protein Homologs of Orthopoxviruses Ahsendorf, Henrike; Gan, Li; Eltom, Kamal Viruses, Vol. 11, Issue 6 https://doi.org/10.3390/v11060493	journal	May 2019

Figures / Tables (7)

Similar Records

Structural basis for antagonizing a host restriction factor by C7 family of poxvirus host-range proteins

Journal Article · Tue Nov 17 00:00:00 EST 2015 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1624434

Meng, Xiangzhi; Krumm, Brian; Li, Yongchao; +2 more

Structure-Function Analysis of Vaccinia Virus H7 Protein Reveals a Novel Phosphoinositide Binding Fold Essential for Poxvirus Replication

Journal Article · Wed Dec 03 00:00:00 EST 2014 · Journal of Virology · OSTI ID:1624434

Kolli, Swapna; Meng, Xiangzhi; Wu, Xiang; +4 more

The Structure of the Poxvirus A33 Protein Reveals a Dimer of Unique C-Type Lectin-Like Domains

Journal Article · Wed Nov 03 00:00:00 EDT 2010 · J. Virol. · OSTI ID:1624434

Su, Hua-Poo; Singh, Kavita; Gittis, Apostolos G; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Science & Technology - Other Topics
Pox Virus
Myristoylation Site
Entomopoxvirus
Vaccinia Virus (VACV)
Poxviridae