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Virology2021; 565; 13-21; doi: 10.1016/j.virol.2021.09.007

Exposing cryptic epitopes on the Venezuelan equine encephalitis virus E1 glycoprotein prior to treatment with alphavirus cross-reactive monoclonal antibody allows blockage of replication early in infection.

Abstract: Eastern equine encephalitis virus (EEEV), western equine encephalitis virus (WEEV) and Venezuelan equine encephalitis virus (VEEV) can cause fatal encephalitis in humans and equids. Some MAbs to the E1 glycoprotein are known to be cross-reactive, weakly neutralizing in vitro but can protect from disease in animal models. We investigated the mechanism of neutralization of VEEV infection by the broadly cross-reactive E1-specific MAb 1A4B-6. 1A4B-6 protected 3-week-old Swiss Webster mice prophylactically from lethal VEEV challenge. Likewise, 1A4B-6 inhibited virus growth in vitro at a pre-attachment step after virions were incubated at 37 °C and inhibited virus-mediated cell fusion. Amino acid residue N100 in the fusion loop of E1 protein was identified as critical for binding. The potential to elicit broadly cross-reactive MAbs with limited virus neutralizing activity in vitro but that can inhibit virus entry and protect animals from infection merits further exploration for vaccine and therapeutic developmental research.
Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.
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Publication Date: 2021-09-28 PubMed ID: 34626907PubMed Central: PMC8765347DOI: 10.1016/j.virol.2021.09.007Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research investigated the ability of the E1-specific MAb 1A4B-6 antibody to block the replication of the Venezuelan equine encephalitis virus (VEEV) at an early stage of infection. It suggests that the antibody, which can bind to the virus’s E1 glycoprotein, can offer protection from disease in animals, despite having limited in vitro neutralizing activity.

Understanding the Research

  • This study aimed to understand the function and effectiveness of MAb 1A4B-6, an antibody that reacts to the E1 glycoprotein on the VEEV. The immune system’s ability to recognize and neutralize any foreign material, such as bacteria, viruses, or tumor cells, is often due to antibodies, which bind specifically to these pathogens.
  • The VEEV, along with the Eastern equine encephalitis virus (EEEV) and the Western equine encephalitis virus (WEEV), can lead to fatal encephalitis in both humans and equids (a family of animals that includes horses and related species).
  • Previous research indicated that some monoclonal antibodies (MAbs) known to react to the E1 glycoprotein exhibited limited effectiveness in neutralizing the virus in vitro (laboratory conditions outside a living organism). However, these antibodies were able to protect animals from the disease in laboratory tests, showing some therapeutic potential.

Research Methodology and Outcomes

  • In this research, the scientists investigated how MAb 1A4B-6 combats VEEV infection. They discovered that the antibody could protect against lethal VEEV challenge prophylactically in 3-week-old Swiss Webster mice, suggesting a preventive use.
  • MAb 1A4B-6 was also able to impede the growth of the virus at a stage before it attached to host cells. The investigation revealed that this was accomplished after the virus particles, referred to as virions, were incubated at a certain temperature (37 °C).
  • The researchers also found that MAb 1A4B-6 could inhibit the fusion of the VEEV with host cells, a crucial step for the virus to replicate and spread within the host.
  • Through their investigation, the researchers identified the N100 amino acid residue found in the fusion loop of the E1 protein as an essential binding site for MAb, providing a potential target for future vaccine or therapeutic developments.

Implications

  • The research suggested that despite their limited in vitro neutralizing activity, antibodies like MAb 1A4B-6 could potentially be used as a preventive measure against VEEV infection.
  • The identification of the N100 amino acid residue as a critical binding site for the antibody provides a specific target for future research aiming to develop vaccines and therapeutics against VEEV.
  • The ability of MAb 1A4B-6 to inhibit virus entry and protect animals from infection in the study highlights a pathway for further exploration and development in the domain of vaccine and therapeutic research.

Cite This Article

APA
Calvert AE, Bennett SL, Hunt AR, Fong RH, Doranz BJ, Roehrig JT, Blair CD. (2021). Exposing cryptic epitopes on the Venezuelan equine encephalitis virus E1 glycoprotein prior to treatment with alphavirus cross-reactive monoclonal antibody allows blockage of replication early in infection. Virology, 565, 13-21. https://doi.org/10.1016/j.virol.2021.09.007

Publication

Virology
ISSN: 1096-0341
NlmUniqueID: 0110674
Country: United States
Language: English
Volume: 565
Pages: 13-21
PII: S0042-6822(21)00198-7

Researcher Affiliations

Calvert, Amanda E
  • Arboviral Diseases Branch, Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, CO 80521, USA. Electronic address: zpz0@cdc.gov.
Bennett, Susan L
  • Center for Vector-borne Infectious Diseases, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523, USA.
Hunt, Ann R
  • Center for Vector-borne Infectious Diseases, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523, USA.
Fong, Rachel H
  • Integral Molecular, Philadelphia, PA 19104, USA.
Doranz, Benjamin J
  • Integral Molecular, Philadelphia, PA 19104, USA.
Roehrig, John T
  • Center for Vector-borne Infectious Diseases, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523, USA.
Blair, Carol D
  • Center for Vector-borne Infectious Diseases, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523, USA.

MeSH Terms

  • Alphavirus / immunology
  • Alphavirus Infections / immunology
  • Amino Acid Sequence
  • Animals
  • Antibodies, Monoclonal / immunology
  • Antibodies, Neutralizing / immunology
  • Antibodies, Viral / immunology
  • Cell Line
  • Chlorocebus aethiops
  • Cross Reactions
  • Encephalitis Virus, Venezuelan Equine / immunology
  • Encephalitis Virus, Venezuelan Equine / metabolism
  • Encephalomyelitis, Venezuelan Equine / immunology
  • Encephalomyelitis, Venezuelan Equine / therapy
  • Encephalomyelitis, Venezuelan Equine / virology
  • Glycoproteins / immunology
  • Immunotherapy
  • Mice
  • Protein Binding
  • Vero Cells
  • Viral Envelope Proteins / immunology
  • Viral Envelope Proteins / metabolism
  • Virion / immunology
  • Virion / metabolism
  • Virus Replication / drug effects

Grant Funding

  • HHSN272201400058C / NIAID NIH HHS

Conflict of Interest Statement

Declaration of competing interest. The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: B.J.D. and R.H.F. are shareholders of Integral Molecular.

References

This article includes 53 references
  1. Aguilar PV, Estrada-Franco JG, Navarro-Lopez R, Ferro C, Haddow AD, Weaver SC. Endemic Venezuelan equine encephalitis in the Americas: hidden under the dengue umbrella.. Future Virol 2011;6(6):721-740.
    pmc: PMC3134406pubmed: 21765860doi: 10.2217/FVL.11.5google scholar: lookup
  2. Bergren NA, Haller S, Rossi SL, Seymour RL, Huang J, Miller AL, Bowen RA, Hartman DA, Brault AC, Weaver SC. "Submergence" of Western equine encephalitis virus: Evidence of positive selection argues against genetic drift and fitness reductions.. PLoS Pathog 2020 Feb;16(2):e1008102.
    pmc: PMC7029877pubmed: 32027727doi: 10.1371/journal.ppat.1008102google scholar: lookup
  3. Boere WA, Benaissa-Trouw BJ, Harmsen M, Kraaijeveld CA, Snippe H. Neutralizing and non-neutralizing monoclonal antibodies to the E2 glycoprotein of Semliki Forest virus can protect mice from lethal encephalitis.. J Gen Virol 1983 Jun;64 (Pt 6):1405-8.
    pubmed: 6854274doi: 10.1099/0022-1317-64-6-1405google scholar: lookup
  4. Bogan AA, Thorn KS. Anatomy of hot spots in protein interfaces.. J Mol Biol 1998 Jul 3;280(1):1-9.
    pubmed: 9653027doi: 10.1006/jmbi.1998.1843google scholar: lookup
  5. Burke CW, Froude JW, Miethe S, Hülseweh B, Hust M, Glass PJ. Human-Like Neutralizing Antibodies Protect Mice from Aerosol Exposure with Western Equine Encephalitis Virus.. Viruses 2018 Mar 24;10(4).
    pmc: PMC5923441pubmed: 29587363doi: 10.3390/v10040147google scholar: lookup
  6. Burke CW, Froude JW, Rossi F, White CE, Moyer CL, Ennis J, Pitt ML, Streatfield S, Jones RM, Musiychuk K, Kervinen J, Zeitlin L, Yusibov V, Glass PJ. Therapeutic monoclonal antibody treatment protects nonhuman primates from severe Venezuelan equine encephalitis virus disease after aerosol exposure.. PLoS Pathog 2019 Dec;15(12):e1008157.
    pmc: PMC6907853pubmed: 31790515doi: 10.1371/journal.ppat.1008157google scholar: lookup
  7. Calisher CH. Medically important arboviruses of the United States and Canada.. Clin Microbiol Rev 1994 Jan;7(1):89-116.
    pmc: PMC358307pubmed: 8118792doi: 10.1128/CMR.7.1.89google scholar: lookup
  8. Carrera JP, Pittí Y, Molares-Martínez JC, Casal E, Pereyra-Elias R, Saenz L, Guerrero I, Galué J, Rodriguez-Alvarez F, Jackman C, Pascale JM, Armien B, Weaver SC, Donnelly CA, Vittor AY. Clinical and Serological Findings of Madariaga and Venezuelan Equine Encephalitis Viral Infections: A Follow-up Study 5 Years After an Outbreak in Panama.. Open Forum Infect Dis 2020 Sep;7(9):ofaa359.
    pmc: PMC7518370pubmed: 33005697doi: 10.1093/ofid/ofaa359google scholar: lookup
  9. Engelberts PJ, Badoil C, Beurskens FJ, Boulay-Moine D, Grivel K, Parren PW, Moulard M. A quantitative flow cytometric assay for determining binding characteristics of chimeric, humanized and human antibodies in whole blood: proof of principle with rituximab and ofatumumab.. J Immunol Methods 2013 Feb 28;388(1-2):8-17.
    pubmed: 23183273doi: 10.1016/j.jim.2012.11.007google scholar: lookup
  10. Flynn DC, Meyer WJ, Mackenzie JM Jr, Johnston RE. A conformational change in Sindbis virus glycoproteins E1 and E2 is detected at the plasma membrane as a consequence of early virus-cell interaction.. J Virol 1990 Aug;64(8):3643-53.
    pmc: PMC249657pubmed: 1695253doi: 10.1128/JVI.64.8.3643-3653.1990google scholar: lookup
  11. Fong RH, Banik SS, Mattia K, Barnes T, Tucker D, Liss N, Lu K, Selvarajah S, Srinivasan S, Mabila M, Miller A, Muench MO, Michault A, Rucker JB, Paes C, Simmons G, Kahle KM, Doranz BJ. Exposure of epitope residues on the outer face of the chikungunya virus envelope trimer determines antibody neutralizing efficacy.. J Virol 2014 Dec;88(24):14364-79.
    pmc: PMC4249124pubmed: 25275138doi: 10.1128/JVI.01943-14google scholar: lookup
  12. Fox JM, Long F, Edeling MA, Lin H, van Duijl-Richter MKS, Fong RH, Kahle KM, Smit JM, Jin J, Simmons G, Doranz BJ, Crowe JE Jr, Fremont DH, Rossmann MG, Diamond MS. Broadly Neutralizing Alphavirus Antibodies Bind an Epitope on E2 and Inhibit Entry and Egress.. Cell 2015 Nov 19;163(5):1095-1107.
    pmc: PMC4659373pubmed: 26553503doi: 10.1016/j.cell.2015.10.050google scholar: lookup
  13. Guirakhoo F, Hunt AR, Lewis JG, Roehrig JT. Selection and partial characterization of dengue 2 virus mutants that induce fusion at elevated pH.. Virology 1993 May;194(1):219-23.
    pubmed: 8480420doi: 10.1006/viro.1993.1252google scholar: lookup
  14. Hart BL, Ketai L. Armies of pestilence: CNS infections as potential weapons of mass destruction.. AJNR Am J Neuroradiol 2015 Jun;36(6):1018-25.
    pmc: PMC8013034pubmed: 25477355doi: 10.3174/ajnr.A4177google scholar: lookup
  15. Holmes AC, Basore K, Fremont DH, Diamond MS. A molecular understanding of alphavirus entry.. PLoS Pathog 2020 Oct;16(10):e1008876.
    pmc: PMC7580943pubmed: 33091085doi: 10.1371/journal.ppat.1008876google scholar: lookup
  16. Hunt AR, Bowen RA, Frederickson S, Maruyama T, Roehrig JT, Blair CD. Treatment of mice with human monoclonal antibody 24h after lethal aerosol challenge with virulent Venezuelan equine encephalitis virus prevents disease but not infection.. Virology 2011 Jun 5;414(2):146-52.
    pmc: PMC3097527pubmed: 21489591doi: 10.1016/j.virol.2011.03.016google scholar: lookup
  17. Hunt AR, Frederickson S, Hinkel C, Bowdish KS, Roehrig JT. A humanized murine monoclonal antibody protects mice either before or after challenge with virulent Venezuelan equine encephalomyelitis virus.. J Gen Virol 2006 Sep;87(Pt 9):2467-2476.
    pubmed: 16894184doi: 10.1099/vir.0.81925-0google scholar: lookup
  18. Hunt AR, Roehrig JT. Biochemical and biological characteristics of epitopes on the E1 glycoprotein of western equine encephalitis virus.. Virology 1985 Apr 30;142(2):334-46.
    pubmed: 2414904doi: 10.1016/0042-6822(85)90342-3google scholar: lookup
  19. Hunt AR, Roehrig JT. Localization of a protective epitope on a Venezuelan equine encephalomyelitis (VEE) virus peptide that protects mice from both epizootic and enzootic VEE virus challenge and is immunogenic in horses.. Vaccine 1995 Feb;13(3):281-8.
    pubmed: 7543231doi: 10.1016/0264-410x(95)93315-zgoogle scholar: lookup
  20. Hunt AR, Short WA, Johnson AJ, Bolin RA, Roehrig JT. Synthetic peptides of the E2 glycoprotein of Venezuelan equine encephalomyelitis virus. II. Antibody to the amino terminus protects animals by limiting viral replication.. Virology 1991 Nov;185(1):281-90.
    pubmed: 1718085doi: 10.1016/0042-6822(91)90775-7google scholar: lookup
  21. Jose J, Snyder JE, Kuhn RJ. A structural and functional perspective of alphavirus replication and assembly.. Future Microbiol 2009 Sep;4(7):837-56.
    pmc: PMC2762864pubmed: 19722838doi: 10.2217/fmb.09.59google scholar: lookup
  22. Kim AS, Austin SK, Gardner CL, Zuiani A, Reed DS, Trobaugh DW, Sun C, Basore K, Williamson LE, Crowe JE Jr, Slifka MK, Fremont DH, Klimstra WB, Diamond MS. Protective antibodies against Eastern equine encephalitis virus bind to epitopes in domains A and B of the E2 glycoprotein.. Nat Microbiol 2019 Jan;4(1):187-197.
    pmc: PMC6294662pubmed: 30455470doi: 10.1038/s41564-018-0286-4google scholar: lookup
  23. Kim AS, Kafai NM, Winkler ES, Gilliland TC Jr, Cottle EL, Earnest JT, Jethva PN, Kaplonek P, Shah AP, Fong RH, Davidson E, Malonis RJ, Quiroz JA, Williamson LE, Vang L, Mack M, Crowe JE Jr, Doranz BJ, Lai JR, Alter G, Gross ML, Klimstra WB, Fremont DH, Diamond MS. Pan-protective anti-alphavirus human antibodies target a conserved E1 protein epitope.. Cell 2021 Aug 19;184(17):4414-4429.e19.
    pmc: PMC8382027pubmed: 34416146doi: 10.1016/j.cell.2021.07.006google scholar: lookup
  24. Lindsey NP, Martin SW, Staples JE, Fischer M. Notes from the Field: Multistate Outbreak of Eastern Equine Encephalitis Virus - United States, 2019.. MMWR Morb Mortal Wkly Rep 2020 Jan 17;69(2):50-51.
    pmc: PMC6973353pubmed: 31945032doi: 10.15585/mmwr.mm6902a4google scholar: lookup
  25. Lindsey NP, Staples JE, Fischer M. Eastern Equine Encephalitis Virus in the United States, 2003-2016.. Am J Trop Med Hyg 2018 May;98(5):1472-1477.
    pmc: PMC5953388pubmed: 29557336doi: 10.4269/ajtmh.17-0927google scholar: lookup
  26. Lo Conte L, Chothia C, Janin J. The atomic structure of protein-protein recognition sites.. J Mol Biol 1999 Feb 5;285(5):2177-98.
    pubmed: 9925793doi: 10.1006/jmbi.1998.2439google scholar: lookup
  27. Lok SM, Kostyuchenko V, Nybakken GE, Holdaway HA, Battisti AJ, Sukupolvi-Petty S, Sedlak D, Fremont DH, Chipman PR, Roehrig JT, Diamond MS, Kuhn RJ, Rossmann MG. Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins.. Nat Struct Mol Biol 2008 Mar;15(3):312-7.
    pubmed: 18264114doi: 10.1038/nsmb.1382google scholar: lookup
  28. Martinez MG, Kielian M. Intercellular Extensions Are Induced by the Alphavirus Structural Proteins and Mediate Virus Transmission.. PLoS Pathog 2016 Dec;12(12):e1006061.
    pmc: PMC5158078pubmed: 27977778doi: 10.1371/journal.ppat.1006061google scholar: lookup
  29. Mathews JH, Roehrig JT. Determination of the protective epitopes on the glycoproteins of Venezuelan equine encephalomyelitis virus by passive transfer of monoclonal antibodies.. J Immunol 1982 Dec;129(6):2763-7.
    pubmed: 6183343
  30. Meyer WJ, Gidwitz S, Ayers VK, Schoepp RJ, Johnston RE. Conformational alteration of Sindbis virion glycoproteins induced by heat, reducing agents, or low pH.. J Virol 1992 Jun;66(6):3504-13.
    pmc: PMC241131pubmed: 1374808doi: 10.1128/JVI.66.6.3504-3513.1992google scholar: lookup
  31. Pal P, Dowd KA, Brien JD, Edeling MA, Gorlatov S, Johnson S, Lee I, Akahata W, Nabel GJ, Richter MK, Smit JM, Fremont DH, Pierson TC, Heise MT, Diamond MS. Development of a highly protective combination monoclonal antibody therapy against Chikungunya virus.. PLoS Pathog 2013;9(4):e1003312.
    pmc: PMC3630103pubmed: 23637602doi: 10.1371/journal.ppat.1003312google scholar: lookup
  32. Parker MD, Buckley MJ, Melanson VR, Glass PJ, Norwood D, Hart MK. Antibody to the E3 glycoprotein protects mice against lethal venezuelan equine encephalitis virus infection.. J Virol 2010 Dec;84(24):12683-90.
    pmc: PMC3004303pubmed: 20926570doi: 10.1128/JVI.01345-10google scholar: lookup
  33. Pereboev AV, Razumov IA, Svyatchenko VA, Loktev VB. Glycoproteins E2 of the Venezuelan and eastern equine encephalomyelitis viruses contain multiple cross-reactive epitopes.. Arch Virol 1996;141(11):2191-205.
    pubmed: 8973533doi: 10.1007/BF01718225google scholar: lookup
  34. Phillpotts RJ. Venezuelan equine encephalitis virus complex-specific monoclonal antibody provides broad protection, in murine models, against airborne challenge with viruses from serogroups I, II and III.. Virus Res 2006 Sep;120(1-2):107-12.
    pubmed: 16621103doi: 10.1016/j.virusres.2006.02.003google scholar: lookup
  35. Porta J, Jose J, Roehrig JT, Blair CD, Kuhn RJ, Rossmann MG. Locking and blocking the viral landscape of an alphavirus with neutralizing antibodies.. J Virol 2014 Sep 1;88(17):9616-23.
    pmc: PMC4136364pubmed: 24920796doi: 10.1128/JVI.01286-14google scholar: lookup
  36. Powell LA, Fox JM, Kose N, Kim AS, Majedi M, Bombardi R, Carnahan RH, Slaughter JC, Morrison TE, Diamond MS, Crowe JE Jr. Human monoclonal antibodies against Ross River virus target epitopes within the E2 protein and protect against disease.. PLoS Pathog 2020 May;16(5):e1008517.
    pmc: PMC7252634pubmed: 32365139doi: 10.1371/journal.ppat.1008517google scholar: lookup
  37. Rico AB, Phillips AT, Schountz T, Jarvis DL, Tjalkens RB, Powers AM, Olson KE. Venezuelan and western equine encephalitis virus E1 liposome antigen nucleic acid complexes protect mice from lethal challenge with multiple alphaviruses.. Virology 2016 Dec;499:30-39.
    pmc: PMC5884135pubmed: 27632563doi: 10.1016/j.virol.2016.08.023google scholar: lookup
  38. Roehrig JT, Day JW, Kinney RM. Antigenic analysis of the surface glycoproteins of a Venezuelan equine encephalomyelitis virus (TC-83) using monoclonal antibodies.. Virology 1982 Apr 30;118(2):269-78.
    pubmed: 6178209doi: 10.1016/0042-6822(82)90346-4google scholar: lookup
  39. Roehrig JT, Hunt AR, Chang GJ, Sheik B, Bolin RA, Tsai TF, Trent DW. Identification of monoclonal antibodies capable of differentiating antigenic varieties of eastern equine encephalitis viruses.. Am J Trop Med Hyg 1990 Apr;42(4):394-8.
    pubmed: 2158755doi: 10.4269/ajtmh.1990.42.394google scholar: lookup
  40. Roehrig JT, Hunt AR, Kinney RM, Mathews JH. In vitro mechanisms of monoclonal antibody neutralization of alphaviruses.. Virology 1988 Jul;165(1):66-73.
    pubmed: 2455383doi: 10.1016/0042-6822(88)90659-9google scholar: lookup
  41. Rülker T, Voß L, Thullier P, O' Brien LM, Pelat T, Perkins SD, Langermann C, Schirrmann T, Dübel S, Marschall HJ, Hust M, Hülseweh B. Isolation and characterisation of a human-like antibody fragment (scFv) that inactivates VEEV in vitro and in vivo.. PLoS One 2012;7(5):e37242.
    pmc: PMC3364240pubmed: 22666347doi: 10.1371/journal.pone.0037242google scholar: lookup
  42. Rusnak JM, Kortepeter MG, Hawley RJ, Anderson AO, Boudreau E, Eitzen E. Risk of occupationally acquired illnesses from biological threat agents in unvaccinated laboratory workers.. Biosecur Bioterror 2004;2(4):281-93.
    pubmed: 15650438doi: 10.1089/bsp.2004.2.281google scholar: lookup
  43. Schmaljohn AL, Johnson ED, Dalrymple JM, Cole GA. Non-neutralizing monoclonal antibodies can prevent lethal alphavirus encephalitis.. Nature 1982 May 6;297(5861):70-2.
    pubmed: 6280072doi: 10.1038/297070a0google scholar: lookup
  44. Schmaljohn AL, Kokubun KM, Cole GA. Protective monoclonal antibodies define maturational and pH-dependent antigenic changes in Sindbis virus E1 glycoprotein.. Virology 1983 Oct 15;130(1):144-54.
    pubmed: 6195815doi: 10.1016/0042-6822(83)90124-1google scholar: lookup
  45. Sevvana M, Kuhn RJ. Mapping the diverse structural landscape of the flavivirus antibody repertoire.. Curr Opin Virol 2020 Dec;45:51-64.
    pmc: PMC7746604pubmed: 32801077doi: 10.1016/j.coviro.2020.07.006google scholar: lookup
  46. Sidwell RW, Smee DF. Viruses of the Bunya- and Togaviridae families: potential as bioterrorism agents and means of control.. Antiviral Res 2003 Jan;57(1-2):101-11.
    pubmed: 12615306doi: 10.1016/s0166-3542(02)00203-6google scholar: lookup
  47. Soonsawad P, Xing L, Milla E, Espinoza JM, Kawano M, Marko M, Hsieh C, Furukawa H, Kawasaki M, Weerachatyanukul W, Srivastava R, Barnett SW, Srivastava IK, Cheng RH. Structural evidence of glycoprotein assembly in cellular membrane compartments prior to Alphavirus budding.. J Virol 2010 Nov;84(21):11145-51.
    pmc: PMC2953181pubmed: 20739526doi: 10.1128/JVI.00036-10google scholar: lookup
  48. Stromberg ZR, Fischer W, Bradfute SB, Kubicek-Sutherland JZ, Hraber P. Vaccine Advances against Venezuelan, Eastern, and Western Equine Encephalitis Viruses.. Vaccines (Basel) 2020 Jun 3;8(2).
    pmc: PMC7350001pubmed: 32503232doi: 10.3390/vaccines8020273google scholar: lookup
  49. von Bonsdorff CH, Harrison SC. Hexagonal glycoprotein arrays from Sindbis virus membranes.. J Virol 1978 Nov;28(2):578-83.
    pmc: PMC354305pubmed: 722862doi: 10.1128/JVI.28.2.578-583.1978google scholar: lookup
  50. Williamson LE, Reeder KM, Bailey K, Tran MH, Roy V, Fouch ME, Kose N, Trivette A, Nargi RS, Winkler ES, Kim AS, Gainza C, Rodriguez J, Armstrong E, Sutton RE, Reidy J, Carnahan RH, McDonald WH, Schoeder CT, Klimstra WB, Davidson E, Doranz BJ, Alter G, Meiler J, Schey KL, Julander JG, Diamond MS, Crowe JE Jr. Therapeutic alphavirus cross-reactive E1 human antibodies inhibit viral egress.. Cell 2021 Aug 19;184(17):4430-4446.e22.
    pmc: PMC8418820pubmed: 34416147doi: 10.1016/j.cell.2021.07.033google scholar: lookup
  51. Wust CJ, Crombie R, Brown A. Passive protection across subgroups of alphaviruses by hyperimmune non-cross-neutralizing anti-Sindbis serum.. Proc Soc Exp Biol Med 1987 Jan;184(1):56-63.
    pubmed: 3025890doi: 10.3181/00379727-184-42446google scholar: lookup
  52. Zenger VE, Vogt R, Mandy F, Schwartz A, Marti GE. Quantitative flow cytometry: inter-laboratory variation.. Cytometry 1998 Oct 1;33(2):138-45.
    pubmed: 9773874doi: 10.1002/(sici)1097-0320(19981001)33:2<138::aid-cyto8>3.0.co;2-fgoogle scholar: lookup
  53. Zhou QF, Fox JM, Earnest JT, Ng TS, Kim AS, Fibriansah G, Kostyuchenko VA, Shi J, Shu B, Diamond MS, Lok SM. Structural basis of Chikungunya virus inhibition by monoclonal antibodies.. Proc Natl Acad Sci U S A 2020 Nov 3;117(44):27637-27645.
    pmc: PMC7959576pubmed: 33087569doi: 10.1073/pnas.2008051117google scholar: lookup

Citations

This article has been cited 6 times.
  1. Kim AS, Diamond MS. A molecular understanding of alphavirus entry and antibody protection. Nat Rev Microbiol 2023 Jun;21(6):396-407.
    doi: 10.1038/s41579-022-00825-7pubmed: 36474012google scholar: lookup
  2. Geng Q, Navaratnarajah CK, Zhang W. Structural and Functional Hallmarks of Sindbis Virus Proteins: From Virion Architecture to Pathogenesis. Int J Mol Sci 2025 Aug 27;26(17).
    doi: 10.3390/ijms26178323pubmed: 40943245google scholar: lookup
  3. Miazgowicz KL, Maloney BE, Brindley MA, Cassaday M, Petch RJ, Bates P, Brault AC, Calvert AE. Chimeric Vesicular Stomatitis Virus Bearing Western Equine Encephalitis Virus Envelope Proteins E2-E1 Is a Suitable Surrogate for Western Equine Encephalitis Virus in a Plaque Reduction Neutralization Test. Viruses 2025 Jul 31;17(8).
    doi: 10.3390/v17081067pubmed: 40872781google scholar: lookup
  4. Callahan V, Sutton MS, Gardner CL, Prado-Smith J, Kenchegowda D, Dunagan MM, Gosavi M, Embong A, Green C, Kamphaugh H, Chen TY, Long D, Vogel JL, Kosik I, Yewdell JW, Kristie TM, Clancy CS, Burke CW, Roederer M, Fox JM. High binding potency overcomes the requirement of Fc effector functions for broadly reactive anti-alphavirus antibodies. Sci Transl Med 2025 Aug 20;17(812):eadt9853.
    doi: 10.1126/scitranslmed.adt9853pubmed: 40834099google scholar: lookup
  5. Callahan V, Sutton MS, Gardner CL, Kenchegowda D, Dunagan MM, Gosavi M, Green C, Chen TY, Prado-Smith J, Long D, Vogel JL, Kristie TM, Clancy CS, Burke CW, Roederer M, Fox JM. Requirement for Fc effector function is overcome by binding potency for broadly reactive anti-alphavirus antibodies. bioRxiv 2024 Nov 3;.
    doi: 10.1101/2024.11.03.619087pubmed: 39605662google scholar: lookup
  6. Sette A, Saphire EO. Inducing broad-based immunity against viruses with pandemic potential. Immunity 2022 May 10;55(5):738-748.
    doi: 10.1016/j.immuni.2022.04.010pubmed: 35545026google scholar: lookup
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