Mechanistic basis for potent neutralization of Sin Nombre hantavirus by a human monoclonal antibody.
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
received:
22
07
2022
accepted:
17
05
2023
medline:
7
7
2023
pubmed:
16
6
2023
entrez:
15
6
2023
Statut:
ppublish
Résumé
Rodent-borne hantaviruses are prevalent worldwide and upon spillover to human populations, cause severe disease for which no specific treatment is available. A potent antibody response is key for recovery from hantavirus infection. Here we study a highly neutralizing human monoclonal antibody, termed SNV-42, which was derived from a memory B cell isolated from an individual with previous Sin Nombre virus (SNV) infection. Crystallographic analysis demonstrates that SNV-42 targets the Gn subcomponent of the tetrameric (Gn-Gc)
Identifiants
pubmed: 37322112
doi: 10.1038/s41564-023-01413-y
pii: 10.1038/s41564-023-01413-y
pmc: PMC10322703
doi:
Substances chimiques
Antibodies, Monoclonal
0
Antibodies, Neutralizing
0
Glycoproteins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1293-1303Subventions
Organisme : NIGMS NIH HHS
ID : T32 GM008320
Pays : United States
Organisme : Medical Research Council
ID : MR/S007555/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/V031635/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 203141/Z/16/Z
Pays : United Kingdom
Informations de copyright
© 2023. The Author(s).
Références
Nichol, S. T. et al. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 262, 914–917 (1993).
pubmed: 8235615
doi: 10.1126/science.8235615
Jonsson, C. B., Figueiredo, L. T. & Vapalahti, O. A global perspective on hantavirus ecology, epidemiology, and disease. Clin. Microbiol. Rev. 23, 412–441 (2010).
pubmed: 20375360
pmcid: 2863364
doi: 10.1128/CMR.00062-09
Hjelle, B. & Torres-Pérez, F. Hantaviruses in the Americas and their role as emerging pathogens. Viruses 2, 2559–2586 (2010).
pubmed: 21994631
pmcid: 3185593
doi: 10.3390/v2122559
Martinez, V. P. et al. Person-to-person transmission of Andes virus. Emerg. Infect. Dis. 11, 1848–1853 (2005).
pubmed: 16485469
pmcid: 3367635
doi: 10.3201/eid1112.050501
Serris, A. et al. The hantavirus surface glycoprotein lattice and its fusion control mechanism. Cell 183, 442–456.e16 (2020).
pubmed: 32937107
pmcid: 7572791
doi: 10.1016/j.cell.2020.08.023
Rissanen, I. et al. Structural transitions of the conserved and metastable hantaviral glycoprotein envelope. J. Virol. 91, e00378-17 (2017).
pubmed: 28835498
pmcid: 5640846
doi: 10.1128/JVI.00378-17
Li, S. et al. A molecular-level account of the antigenic hantaviral surface. Cell Rep. 15, 959–967 (2016).
pubmed: 27117403
pmcid: 4858563
doi: 10.1016/j.celrep.2016.03.082
Guardado-Calvo, P. & Rey, F. A. The surface glycoproteins of hantaviruses. Curr. Opin. Virol. 50, 87–94 (2021).
pubmed: 34418649
doi: 10.1016/j.coviro.2021.07.009
Guardado-Calvo, P. & Rey, F. A. The viral class II membrane fusion machinery: divergent evolution from an ancestral heterodimer. Viruses 13, 2368 (2021).
pubmed: 34960636
pmcid: 8706100
doi: 10.3390/v13122368
Hulswit, R. J. G., Paesen, G. C., Bowden, T. A. & Shi, X. Recent advances in bunyavirus glycoprotein research: precursor processing, receptor binding and structure. Viruses 13, 353 (2021).
pubmed: 33672327
pmcid: 7926653
doi: 10.3390/v13020353
Jangra, R. K. et al. Protocadherin-1 is essential for cell entry by New World hantaviruses. Nature 563, 559–563 (2018).
pubmed: 30464266
pmcid: 6556216
doi: 10.1038/s41586-018-0702-1
Engdahl, T. B. & Crowe, J. E. Jr. Humoral immunity to hantavirus infection. mSphere 5, e00482-20 (2020).
pubmed: 32669473
pmcid: 7364217
doi: 10.1128/mSphere.00482-20
Rissanen, I. et al. Molecular rationale for antibody-mediated targeting of the hantavirus fusion glycoprotein. eLife 9, 2308 (2020).
doi: 10.7554/eLife.58242
Rissanen, I. et al. Structural basis for a neutralizing antibody response elicited by a recombinant Hantaan virus Gn immunogen. mBio 12, e0253120 (2021).
pubmed: 34225492
doi: 10.1128/mBio.02531-20
Mittler, E. et al. Human antibody recognizing a quaternary epitope in the Puumala virus glycoprotein provides broad protection against orthohantaviruses. Sci. Transl. Med. 14, eabl5399 (2022).
pubmed: 35294259
pmcid: 9805701
doi: 10.1126/scitranslmed.abl5399
Engdahl, T. B. et al. Broad and potently neutralizing monoclonal antibodies isolated from human survivors of New World hantavirus infection. Cell Rep. 35, 109086 (2021).
pubmed: 33951434
pmcid: 8142553
doi: 10.1016/j.celrep.2021.109086
Mittler, E. et al. Hantavirus entry: perspectives and recent advances. Adv. Virus Res 104, 185–224 (2019).
pubmed: 31439149
pmcid: 6881143
doi: 10.1016/bs.aivir.2019.07.002
Bignon, E. A., Albornoz, A., Guardado-Calvo, P., Rey, F. A. & Tischler, N. D. Molecular organization and dynamics of the fusion protein Gc at the hantavirus surface. eLife 8, e46028 (2019).
pubmed: 31180319
pmcid: 6609335
doi: 10.7554/eLife.46028
Guardado-Calvo, P. et al. Mechanistic insight into bunyavirus-induced membrane fusion from structure-function analyses of the hantavirus envelope glycoprotein Gc. PLoS Pathog. 12, e1005813 (2016).
pubmed: 27783711
pmcid: 5082683
doi: 10.1371/journal.ppat.1005813
Willensky, S. et al. Crystal structure of glycoprotein C from a hantavirus in the post-fusion conformation. PLoS Pathog. 12, e1005948 (2016).
pubmed: 27783673
pmcid: 5081248
doi: 10.1371/journal.ppat.1005948
Bharadwaj, M., Nofchissey, R., Goade, D., Koster, F. & Hjelle, B. Humoral immune responses in the hantavirus cardiopulmonary syndrome. J. Infect. Dis. 182, 43–48 (2000).
pubmed: 10882580
doi: 10.1086/315657
Garrido, J. L. et al. Two recombinant human monoclonal antibodies that protect against lethal Andes hantavirus infection in vivo. Sci. Transl. Med. 10, eaat6420 (2018).
pubmed: 30463919
doi: 10.1126/scitranslmed.aat6420
Duehr, J. et al. Neutralizing monoclonal antibodies against the Gn and the Gc of the Andes virus glycoprotein spike complex protect from virus challenge in a preclinical hamster model. mBio 11, e00028-20 (2020).
pubmed: 32209676
pmcid: 7157512
doi: 10.1128/mBio.00028-20
Wang, M., Pennock, D. G., Spik, K. W. & Schmaljohn, C. S. Epitope mapping studies with neutralizing and non-neutralizing monoclonal antibodies to the G1 and G2 envelope glycoproteins of Hantaan virus. Virology 197, 757–766 (1993).
pubmed: 7504368
doi: 10.1006/viro.1993.1652
Kikuchi, M. et al. Characterization of neutralizing monoclonal antibody escape mutants of Hantaan virus 76118. Arch. Virol. 143, 73–83 (1998).
pubmed: 9505967
doi: 10.1007/s007050050269
Wu, Y. et al. Structures of phlebovirus glycoprotein Gn and identification of a neutralizing antibody epitope. Proc. Natl Acad. Sci. USA 114, E7564–E7573 (2017).
pubmed: 28827346
pmcid: 5594662
doi: 10.1073/pnas.1705176114
Halldorsson, S. et al. Shielding and activation of a viral membrane fusion protein. Nat. Commun. 9, 349 (2018).
pubmed: 29367607
pmcid: 5783950
doi: 10.1038/s41467-017-02789-2
Wang, Q. et al. Neutralization mechanism of human monoclonal antibodies against Rift Valley fever virus. Nat. Microbiol. 4, 1231–1241 (2019).
pubmed: 30936489
doi: 10.1038/s41564-019-0411-z
Chapman, N. S. et al. Potent neutralization of Rift Valley fever virus by human monoclonal antibodies through fusion inhibition. Proc. Natl Acad. Sci. USA 118, e2025642118 (2021).
pubmed: 33782133
pmcid: 8040655
doi: 10.1073/pnas.2025642118
Allen, E. R. et al. A protective monoclonal antibody targets a site of vulnerability on the surface of Rift Valley fever virus. Cell Rep. 25, 3750–3758 e4 (2018).
pubmed: 30590046
pmcid: 6315105
doi: 10.1016/j.celrep.2018.12.001
Pappas, L. et al. Rapid development of broadly influenza neutralizing antibodies through redundant mutations. Nature 516, 418–422 (2014).
pubmed: 25296253
doi: 10.1038/nature13764
Yuan, M. et al. Structural basis of a shared antibody response to SARS-CoV-2. Science 369, 1119–1123 (2020).
pubmed: 32661058
pmcid: 7402627
doi: 10.1126/science.abd2321
Dong, J. et al. Genetic and structural basis for SARS-CoV-2 variant neutralization by a two-antibody cocktail. Nat. Microbiol. 6, 1233–1244 (2021).
pubmed: 34548634
pmcid: 8543371
doi: 10.1038/s41564-021-00972-2
Robbiani, D. F. et al. Convergent antibody responses to SARS-CoV-2 in convalescent individuals. Nature 584, 437–442 (2020).
pubmed: 32555388
pmcid: 7442695
doi: 10.1038/s41586-020-2456-9
Byrne, P. O. & McLellan, J. S. Principles and practical applications of structure-based vaccine design. Curr. Opin. Immunol. 77, 102209 (2022).
pubmed: 35598506
pmcid: 9611442
doi: 10.1016/j.coi.2022.102209
Núñez, J. J. et al. Hantavirus infections among overnight visitors to Yosemite National Park, California, USA, 2012. Emerg. Infect. Dis. 20, 386–393 (2014).
pubmed: 24565589
pmcid: 3944872
doi: 10.3201/eid2003.131581
D’Souza, M. H. & Patel, T. R. Biodefense implications of New-World hantaviruses. Front. Bioeng. Biotechnol. 8, 925 (2020).
pubmed: 32850756
pmcid: 7426369
doi: 10.3389/fbioe.2020.00925
Martínez, V. P. et al. ‘Super-spreaders’ and person-to-person transmission of Andes virus in Argentina. N. Engl. J. Med. 383, 2230–2241 (2020).
pubmed: 33264545
doi: 10.1056/NEJMoa2009040
Aricescu, A. R., Lu, W. & Jones, E. Y. A time- and cost-efficient system for high-level protein production in mammalian cells. Acta Crystallogr. D 62, 1243–1250 (2006).
pubmed: 17001101
doi: 10.1107/S0907444906029799
Chang, V. T. et al. Glycoprotein structural genomics: solving the glycosylation problem. Structure 15, 267–273 (2007).
pubmed: 17355862
pmcid: 1885966
doi: 10.1016/j.str.2007.01.011
Walter, T. S. et al. A procedure for setting up high-throughput nanolitre crystallization experiments. Crystallization workflow for initial screening, automated storage, imaging and optimization. Acta Crystallogr. D 61, 651–657 (2005).
pubmed: 15930615
doi: 10.1107/S0907444905007808
Winter, G. xia2: an expert system for macromolecular crystallography data reduction. J. Appl. Crystallogr. 43, 186–190 (2010).
doi: 10.1107/S0021889809045701
McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
pubmed: 19461840
pmcid: 2483472
doi: 10.1107/S0021889807021206
Lopez-Sagaseta, J. et al. Crystal structure reveals vaccine elicited bactericidal human antibody targeting a conserved epitope on meningococcal fHbp. Nat. Commun. 9, 528 (2018).
pubmed: 29410413
pmcid: 5802752
doi: 10.1038/s41467-018-02827-7
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004).
pubmed: 15572765
doi: 10.1107/S0907444904019158
Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58, 1948–1954 (2002).
pubmed: 12393927
doi: 10.1107/S0907444902016657
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12–21 (2010).
pubmed: 20057044
doi: 10.1107/S0907444909042073
Pettersen, E. F. et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).
pubmed: 32881101
doi: 10.1002/pro.3943
Gilchuk, P. et al. Pan-ebolavirus protective therapy by two multifunctional human antibodies. Cell 184, 5593–5607.e18 (2021).
pubmed: 34715022
pmcid: 8716180
doi: 10.1016/j.cell.2021.09.035
Greaney, A. J. et al. Complete mapping of mutations to the SARS-CoV-2 spike receptor-binding domain that escape antibody recognition. Cell Host Microbe 29, 44–57.e9 (2021).
pubmed: 33259788
pmcid: 7676316
doi: 10.1016/j.chom.2020.11.007
Suryadevara, N. et al. Real-time cell analysis: a high-throughput approach for testing SARS-CoV-2 antibody neutralization and escape. STAR Protoc. 3, 101387 (2022).
pubmed: 35578733
pmcid: 9023333
doi: 10.1016/j.xpro.2022.101387
Hooper, J. W., Josleyn, M., Ballantyne, J. & Brocato, R. A novel Sin Nombre virus DNA vaccine and its inclusion in a candidate pan-hantavirus vaccine against hantavirus pulmonary syndrome (HPS) and hemorrhagic fever with renal syndrome (HFRS). Vaccine 31, 4314–4321 (2013).
pubmed: 23892100
pmcid: 4010434
doi: 10.1016/j.vaccine.2013.07.025