Alphavirus Particles Can Assemble with an Alternate Triangulation Number

Kaelber, Jason T.; Chmielewski, David; Chiu, Wah; Auguste, Albert J.

doi:10.3390/v14122650

Alphavirus Particles Can Assemble with an Alternate Triangulation Number

Journal Article · Sat Nov 26 23:00:00 EST 2022 · Viruses

DOI:https://doi.org/10.3390/v14122650· OSTI ID:1991614

^[1]; Chmielewski, David ^[2]; Chiu, Wah ^[3]; ^[4]

Rutgers Univ., Piscataway, NJ (United States); SLAC
Stanford Univ., CA (United States)
Stanford Univ., CA (United States); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States)

Alphaviruses are spherical, enveloped RNA viruses primarily transmitted by mosquitoes, and cause significant arthritogenic and neurotropic disease in humans and livestock. Previous reports have shown that—in contrast to prototypical icosahedral viruses—alphaviruses incorporate frequent defects, and these may serve important functions in the viral life cycle. We confirm the genus-wide pleomorphism in live viral particles and extend our understanding of alphavirus assembly through the discovery of an alternate architecture of Eastern equine encephalitis virus (EEEV) particles. The alternate T = 3 icosahedral architecture differs in triangulation number from the classic T = 4 icosahedral organization that typifies alphaviruses, but the alternate architecture maintains the quasi-equivalence relationship of asymmetric units. The fusion spike glycoproteins are more loosely apposed in the T = 3 form with corresponding changes in the underlying capsid protein lattice. This alternate architecture could potentially be exploited in engineering alphavirus-based particles for delivery of alphaviral or other RNA.

View Accepted Manuscript (DOE)

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Institutes of Health (NIH); Robert Welch Foundation; USDA

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1991614

Journal Information:: Viruses, Journal Name: Viruses Journal Issue: 12 Vol. 14; ISSN 1999-4915

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (33)

Electrostatic properties of cowpea chlorotic mottle virus and cucumber mosaic virus capsids Konecny, Robert; Trylska, Joanna; Tama, Florence Biopolymers, Vol. 82, Issue 2 https://doi.org/10.1002/bip.20409	journal	January 2006
Epitopes on the major capsid protein of simian virus 40 Babé, L. M.; Brew, K.; Matsuura, S. E. Journal of Biological Chemistry, Vol. 264, Issue 5 https://doi.org/10.1016/S0021-9258(19)81665-4	journal	February 1989
Phosphatidylserine Vesicles Enable Efficient En Bloc Transmission of Enteroviruses Chen, Ying-Han; Du, WenLi; Hagemeijer, Marne C. Cell, Vol. 160, Issue 4 https://doi.org/10.1016/j.cell.2015.01.032	journal	February 2015
Cryo-EM Structures of Eastern Equine Encephalitis Virus Reveal Mechanisms of Virus Disassembly and Antibody Neutralization Hasan, S. Saif; Sun, Chengqun; Kim, Arthur S. Cell Reports, Vol. 25, Issue 11 https://doi.org/10.1016/j.celrep.2018.11.067	journal	December 2018
EMAN2: An extensible image processing suite for electron microscopy Tang, Guang; Peng, Liwei; Baldwin, Philip R. Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.05.009	journal	January 2007
Averaging tens to hundreds of icosahedral particle images to resolve protein secondary structure elements using a Multi-path Simulated Annealing optimization algorithm Liu, Xiangan; Jiang, Wen; Jakana, Joanita Journal of Structural Biology, Vol. 160, Issue 1 https://doi.org/10.1016/j.jsb.2007.06.009	journal	October 2007
A tiling approach to virus capsid assembly explaining a structural puzzle in virology Twarock, R. Journal of Theoretical Biology, Vol. 226, Issue 4 https://doi.org/10.1016/j.jtbi.2003.10.006	journal	February 2004
Nucleic acid packaging in viruses Speir, Jeffrey A.; Johnson, John E. Current Opinion in Structural Biology, Vol. 22, Issue 1 https://doi.org/10.1016/j.sbi.2011.11.002	journal	February 2012
A high capacity Alphavirus heterologous gene delivery system Nanda, Kavita; Vancini, Ricardo; Ribeiro, Mariana Virology, Vol. 390, Issue 2 https://doi.org/10.1016/j.virol.2009.05.026	journal	August 2009
An alphavirus temperature-sensitive capsid mutant reveals stages of nucleocapsid assembly Zheng, Yan; Kielian, Margaret Virology, Vol. 484 https://doi.org/10.1016/j.virol.2015.05.011	journal	October 2015
High resolution single particle refinement in EMAN2.1 Bell, James M.; Chen, Muyuan; Baldwin, Philip R. Methods, Vol. 100 https://doi.org/10.1016/j.ymeth.2016.02.018	journal	May 2016
Visualizing and Correcting Dynamic Specimen Processes in TEM Using a Direct Detection Device Bammes, B. E.; Chen, D. -H.; Jin, L. Microscopy and Microanalysis, Vol. 19, Issue S2 https://doi.org/10.1017/S1431927613008593	journal	August 2013
Self-Assembly of an Alphavirus Core-like Particle Is Distinguished by Strong Intersubunit Association Energy and Structural Defects Wang, Joseph Che-Yen; Chen, Chao; Rayaprolu, Vamseedhar ACS Nano, Vol. 9, Issue 9 https://doi.org/10.1021/acsnano.5b02632	journal	August 2015
4.4 Å cryo-EM structure of an enveloped alphavirus Venezuelan equine encephalitis virus: 4.4 Å cryo-EM structure of an enveloped alphavirus Zhang, Rui; Hryc, Corey F.; Cong, Yao The EMBO Journal, Vol. 30, Issue 18 https://doi.org/10.1038/emboj.2011.261	journal	August 2011
Intrinsic antiviral immunity Yan, Nan; Chen, Zhijian J. Nature Immunology, Vol. 13, Issue 3 https://doi.org/10.1038/ni.2229	journal	February 2012
Intrinsic immunity: a front-line defense against viral attack Bieniasz, Paul D. Nature Immunology, Vol. 5, Issue 11 https://doi.org/10.1038/ni1125	journal	October 2004
cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination Punjani, Ali; Rubinstein, John L.; Fleet, David J. Nature Methods, Vol. 14, Issue 3 https://doi.org/10.1038/nmeth.4169	journal	February 2017
Defective viral genomes are key drivers of the virus–host interaction Vignuzzi, Marco; López, Carolina B. Nature Microbiology, Vol. 4, Issue 7 https://doi.org/10.1038/s41564-019-0465-y	journal	June 2019
Chikungunya virus assembly and budding visualized in situ using cryogenic electron tomography Chmielewski, David; Schmid, Michael F.; Simmons, Graham Nature Microbiology, Vol. 7, Issue 8 https://doi.org/10.1038/s41564-022-01164-2	journal	June 2022
Eilat virus, a unique alphavirus with host range restricted to insects by RNA replication Nasar, F.; Palacios, G.; Gorchakov, R. V. Proceedings of the National Academy of Sciences, Vol. 109, Issue 36 https://doi.org/10.1073/pnas.1204787109	journal	August 2012
RNA-controlled polymorphism in the in vivo assembly of 180-subunit and 120-subunit virions from a single capsid protein Krol, Michael A.; Olson, Norman H.; Tate, John Proceedings of the National Academy of Sciences, Vol. 96, Issue 24 https://doi.org/10.1073/pnas.96.24.13650	journal	November 1999
Membrane proteins organize a symmetrical virus Forsell, Kerstin; Xing, Li; Kozlovska, Tatyana The EMBO Journal, Vol. 19, Issue 19 https://doi.org/10.1093/emboj/19.19.5081	journal	October 2000
Physical Principles in the Construction of Regular Viruses Caspar, D. L. D.; Klug, A. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 27, Issue 0 https://doi.org/10.1101/SQB.1962.027.001.005	journal	January 1962
Structure of the AAVhu.37 capsid by cryoelectron microscopy Kaelber, Jason T.; Yost, Samantha A.; Webber, Keith A. Acta Crystallographica Section F Structural Biology Communications, Vol. 76, Issue 2 https://doi.org/10.1107/S2053230X20000308	journal	February 2020
Novel insect-specific Eilat virus-based chimeric vaccine candidates provide durable, mono- and multi-valent, single dose protection against lethal alphavirus challenge Erasmus, Jesse H.; Seymour, Robert L.; Kaelber, Jason T. Journal of Virology https://doi.org/10.1128/JVI.01274-17	journal	November 2017
In Vitro Assembly of Alphavirus Cores by Using Nucleocapsid Protein Expressed in Escherichia coli Tellinghuisen, Timothy L.; Hamburger, Agnes E.; Fisher, Bonnie R. Journal of Virology, Vol. 73, Issue 7 https://doi.org/10.1128/JVI.73.7.5309-5319.1999	journal	July 1999
Evolutionary Relationships and Systematics of the Alphaviruses Powers, Ann M.; Brault, Aaron C.; Shirako, Yukio Journal of Virology, Vol. 75, Issue 21 https://doi.org/10.1128/JVI.75.21.10118-10131.2001	journal	November 2001
Aura Virus Structure Suggests that the T=4 Organization Is a Fundamental Property of Viral Structural Proteins Zhang, Wei; Fisher, Bonnie R.; Olson, Norman H. Journal of Virology, Vol. 76, Issue 14 https://doi.org/10.1128/JVI.76.14.7239-7246.2002	journal	July 2002
Aura alphavirus subgenomic RNA is packaged into virions of two sizes Rümenapf, T.; Brown, D. T.; Strauss, E. G. Journal of Virology, Vol. 69, Issue 3 https://doi.org/10.1128/jvi.69.3.1741-1746.1995	journal	March 1995
The alphaviruses: gene expression, replication, and evolution Strauss, J. H.; Strauss, E. G. Microbiological Reviews, Vol. 58, Issue 3 https://doi.org/10.1128/mr.58.3.491-562.1994	journal	September 1994
Mechanisms of Virus Assembly Perlmutter, Jason D.; Hagan, Michael F. Annual Review of Physical Chemistry, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-physchem-040214-121637	journal	April 2015
The Social Life of Viruses Sanjuán, Rafael Annual Review of Virology, Vol. 8, Issue 1 https://doi.org/10.1146/annurev-virology-091919-071712	journal	September 2021
Utilization of an Eilat Virus-Based Chimera for Serological Detection of Chikungunya Infection Erasmus, Jesse H.; Needham, James; Raychaudhuri, Syamal PLOS Neglected Tropical Diseases, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pntd.0004119	journal	October 2015

Similar Records

Vaccine Advances against Venezuelan, Eastern, and Western Equine Encephalitis Viruses

Journal Article · Wed Jun 03 00:00:00 EDT 2020 · Vaccines · OSTI ID:1648092

Both RIG-I and MDA5 detect alphavirus replication in concentration-dependent mode

Journal Article · Thu Jan 14 23:00:00 EST 2016 · Virology · OSTI ID:22581664

Structure of a Venezuelan equine encephalitis virus assembly intermediate isolated from infected cells

Journal Article · Mon Oct 25 00:00:00 EDT 2010 · Virology · OSTI ID:21460281

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Togaviridae
alphavirus
cryo-electron microscopy
quasi-equivalence
triangulation number
virus assembly

Alphavirus Particles Can Assemble with an Alternate Triangulation Number

Citation Formats

References (33)

Similar Records

Related Subjects