Functional and structural basis of human parainfluenza virus type 3 neutralization with human monoclonal antibodies.


Journal

Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869

Informations de publication

Date de publication:
10 Jun 2024
Historique:
received: 02 08 2023
accepted: 02 05 2024
medline: 11 6 2024
pubmed: 11 6 2024
entrez: 10 6 2024
Statut: aheadofprint

Résumé

Human parainfluenza virus type 3 (hPIV3) is a respiratory pathogen that can cause severe disease in older people and infants. Currently, vaccines against hPIV3 are in clinical trials but none have been approved yet. The haemagglutinin-neuraminidase (HN) and fusion (F) surface glycoproteins of hPIV3 are major antigenic determinants. Here we describe naturally occurring potently neutralizing human antibodies directed against both surface glycoproteins of hPIV3. We isolated seven neutralizing HN-reactive antibodies and a pre-fusion conformation F-reactive antibody from human memory B cells. One HN-binding monoclonal antibody (mAb), designated PIV3-23, exhibited functional attributes including haemagglutination and neuraminidase inhibition. We also delineated the structural basis of neutralization for two HN and one F mAbs. MAbs that neutralized hPIV3 in vitro protected against infection and disease in vivo in a cotton rat model of hPIV3 infection, suggesting correlates of protection for hPIV3 and the potential clinical utility of these mAbs.

Identifiants

pubmed: 38858594
doi: 10.1038/s41564-024-01722-w
pii: 10.1038/s41564-024-01722-w
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : R01 AI13752
Organisme : NIAID NIH HHS
ID : R01 AI114736
Pays : United States
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : R01 AI13752
Organisme : NIGMS NIH HHS
ID : U24 GM129541
Pays : United States

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Chanock, R. M. et al. Newly recognized myxoviruses from children with respiratory disease. N. Engl. J. Med. 258, 207–213 (1958).
pubmed: 13504446 doi: 10.1056/NEJM195801302580502
Shah, D. P., Shah, P. K., Azzi, J. M. & Chemaly, R. F. Parainfluenza virus infections in hematopoietic cell transplant recipients and hematologic malignancy patients: a systematic review. Cancer Lett. 370, 358–364 (2016).
pubmed: 26582658 doi: 10.1016/j.canlet.2015.11.014
Fontana, L. & Strasfeld, L. Respiratory virus infections of the stem cell transplant recipient and the hematologic malignancy patient. Infect. Dis. Clin. North Am. 33, 523–544 (2019).
pubmed: 30940462 pmcid: 7126949 doi: 10.1016/j.idc.2019.02.004
Moscona, A. & Peluso, R. W. Fusion properties of cells persistently infected with human parainfluenza virus type 3: participation of hemagglutinin-neuraminidase in membrane fusion. J. Virol. 65, 2773–2777 (1991).
pubmed: 1851852 pmcid: 240891 doi: 10.1128/jvi.65.6.2773-2777.1991
Porotto, M. et al. Regulation of paramyxovirus fusion activation: the hemagglutinin-neuraminidase protein stabilizes the fusion protein in a pretriggered state. J. Virol. 86, 12838–12848 (2012).
pubmed: 22993149 pmcid: 3497673 doi: 10.1128/JVI.01965-12
Farzan, S. F. et al. Premature activation of the paramyxovirus fusion protein before target cell attachment with corruption of the viral fusion machinery. J. Biol. Chem. 286, 37945–37954 (2011).
pubmed: 21799008 pmcid: 3207398 doi: 10.1074/jbc.M111.256248
Bose, S., Jardetzky, T. S. & Lamb, R. A. Timing is everything: fine-tuned molecular machines orchestrate paramyxovirus entry. Virology 479, 518–531 (2015).
pubmed: 25771804 doi: 10.1016/j.virol.2015.02.037
Porotto, M., Murrell, M., Greengard, O. & Moscona, A. Triggering of human parainfluenza virus 3 fusion protein (F) by the hemagglutinin-neuraminidase (HN) protein: an HN mutation diminishes the rate of F activation and fusion. J. Virol. 77, 3647–3654 (2003).
pubmed: 12610140 pmcid: 149538 doi: 10.1128/JVI.77.6.3647-3654.2003
Marcink, T. C. et al. Subnanometer structure of an enveloped virus fusion complex on viral surface reveals new entry mechanisms. Sci. Adv. 9, eade2727 (2023).
pubmed: 36763666 pmcid: 9917000 doi: 10.1126/sciadv.ade2727
Porotto, M., Murrell, M., Greengard, O., Doctor, L. & Moscona, A. Influence of the human parainfluenza virus 3 attachment protein’s neuraminidase activity on its capacity to activate the fusion protein. J. Virol. 79, 2383–2392 (2005).
pubmed: 15681439 pmcid: 546598 doi: 10.1128/JVI.79.4.2383-2392.2005
Huberman, K., Peluso, R. W. & Moscona, A. Hemagglutinin-neuraminidase of human parainfluenza-3: role of the neuraminidase in the viral life cycle. Virology 214, 294–300 (1995).
pubmed: 8525632 doi: 10.1006/viro.1995.9925
Porotto, M., Fornabaio, M., Kellogg, G. E. & Moscona, A. A second receptor binding site on human parainfluenza virus type 3 hemagglutinin-neuraminidase contributes to activation of the fusion mechanism. J. Virol. 81, 3216–3228 (2007).
pubmed: 17229690 pmcid: 1866072 doi: 10.1128/JVI.02617-06
Xu, R. et al. Interaction between the hemagglutinin-neuraminidase and fusion glycoproteins of human parainfluenza virus type III regulates viral growth. mBio 4, e00803-13 (2013).
pubmed: 24149514 pmcid: 3812707 doi: 10.1128/mBio.00803-13
Greninger, A. L. et al. Human parainfluenza virus evolution during lung infection of immunocompromised individuals promotes viral persistence. J. Clin. Invest. https://doi.org/10.1172/JCI150506 (2021).
Iketani, S. et al. Viral entry properties required for fitness in humans are lost through rapid genomic change during viral isolation. mBio 9, e00898-18 (2018).
pubmed: 29970463 pmcid: 6030562 doi: 10.1128/mBio.00898-18
Porotto, M., Palmer, S. G., Palermo, L. M. & Moscona, A. Mechanism of fusion triggering by human parainfluenza virus type III. J. Biol. Chem. 287, 778–793 (2012).
pubmed: 22110138 doi: 10.1074/jbc.M111.298059
Palmer, S. G. et al. Adaptation of human parainfluenza virus to airway epithelium reveals fusion properties required for growth in host tissue. mBio 3, e00137-12 (2012).
pubmed: 22669629 pmcid: 3374391 doi: 10.1128/mBio.00137-12
Mishin, V. P. et al. N-linked glycan at residue 523 of human parainfluenza virus type 3 hemagglutinin-neuraminidase masks a second receptor-binding site. J. Virol. 84, 3094–3100 (2010).
pubmed: 20053750 pmcid: 2826034 doi: 10.1128/JVI.02331-09
Lawrence, M. C. et al. Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J. Mol. Biol. 335, 1343–1357 (2004).
pubmed: 14729348 doi: 10.1016/j.jmb.2003.11.032
Streltsov, V. A., Pilling, P., Barrett, S. & McKimm-Breschkin, J. L. Catalytic mechanism and novel receptor binding sites of human parainfluenza virus type 3 hemagglutinin-neuraminidase (hPIV3 HN). Antiviral Res. 123, 216–223 (2015).
pubmed: 26364554 doi: 10.1016/j.antiviral.2015.08.014
Dirr, L., El-Deeb, I. M., Chavas, L. M. G., Guillon, P. & Itzstein, M. V. The impact of the butterfly effect on human parainfluenza virus haemagglutinin-neuraminidase inhibitor design. Sci. Rep. 7, 4507 (2017).
pubmed: 28674426 pmcid: 5495814 doi: 10.1038/s41598-017-04656-y
Pascolutti, M. et al. Structural insights into human parainfluenza virus 3 hemagglutinin-neuraminidase using unsaturated 3-substituted sialic acids as probes. ACS Chem. Biol. 13, 1544–1550 (2018).
pubmed: 29693380 doi: 10.1021/acschembio.8b00150
Dirr, L. et al. The catalytic mechanism of human parainfluenza virus type 3 haemagglutinin-neuraminidase revealed. Angew. Chem. Int. Ed. 54, 2936–2940 (2015).
doi: 10.1002/anie.201412243
Yin, H. S., Paterson, R. G., Wen, X., Lamb, R. A. & Jardetzky, T. S. Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc. Natl Acad. Sci. USA 102, 9288–9293 (2005).
pubmed: 15964978 pmcid: 1151655 doi: 10.1073/pnas.0503989102
Stewart-Jones, G. B. E. et al. Structure-based design of a quadrivalent fusion glycoprotein vaccine for human parainfluenza virus types 1-4. Proc. Natl Acad. Sci. USA 115, 12265–12270 (2018).
pubmed: 30420505 pmcid: 6275507 doi: 10.1073/pnas.1811980115
Habibi, M. S. et al. Impaired antibody-mediated protection and defective IgA B-cell memory in experimental infection of adults with respiratory syncytial virus. Am. J. Respir. Crit. Care Med. 191, 1040–1049 (2015).
pubmed: 25730467 pmcid: 4435460 doi: 10.1164/rccm.201412-2256OC
Ngwuta, J. O. et al. Prefusion F-specific antibodies determine the magnitude of RSV neutralizing activity in human sera. Sci. Transl. Med. 7, 309ra162 (2015).
pubmed: 26468324 pmcid: 4672383 doi: 10.1126/scitranslmed.aac4241
Gilman, M. S. et al. Rapid profiling of RSV antibody repertoires from the memory B cells of naturally infected adult donors. Sci. Immunol. 1, eaaj1879 (2016).
pubmed: 28111638 pmcid: 5244814 doi: 10.1126/sciimmunol.aaj1879
van Wyke Coelingh, K. L. & Tierney, E. L. Identification of amino acids recognized by syncytium-inhibiting and neutralizing monoclonal antibodies to the human parainfluenza type 3 virus fusion protein. J. Virol. 63, 3755–3760 (1989).
doi: 10.1128/jvi.63.9.3755-3760.1989
van Wyke Coelingh, K. L., Winter, C. & Murphy, B. R. Antigenic variation in the hemagglutinin-neuraminidase protein of human parainfluenza type 3 virus. Virology 143, 569–582 (1985).
pubmed: 2414910 doi: 10.1016/0042-6822(85)90395-2
van Wyke Coelingh, K. L., Winter, C. C., Jorgensen, E. D. & Murphy, B. R. Antigenic and structural properties of the hemagglutinin-neuraminidase glycoprotein of human parainfluenza virus type-3: sequence analysis of variants selected with monoclonal antibodies which inhibit infectivity, hemagglutination, and neuraminidase activities. J. Virol. 61, 1473–1477 (1987).
pubmed: 2437318 pmcid: 254125 doi: 10.1128/jvi.61.5.1473-1477.1987
Henrickson, K. J. & Portner, A. Antibody response in children to antigen sites on human PIV-3 HN: correlation with known epitopes mapped by monoclonal antibodies. Vaccine 8, 75–80 (1990).
pubmed: 1690489 doi: 10.1016/0264-410X(90)90182-L
van Wyke Coelingh, K. L. & Tierney, E. L. Antigenic and functional organization of human parainfluenza virus type 3 fusion glycoprotein. J. Virol. 63, 375–382 (1989).
pubmed: 2462062 pmcid: 247693 doi: 10.1128/jvi.63.1.375-382.1989
van Wyke Coelingh, K. L. & Winter, C. C. Naturally occurring human parainfluenza type 3 viruses exhibit divergence in amino acid sequence of their fusion protein neutralization epitopes and cleavage sites. J. Virol. 64, 1329–1334 (1990).
doi: 10.1128/jvi.64.3.1329-1334.1990
Boonyaratanakornkit, J. et al. Protective antibodies against human parainfluenza virus type 3 infection. MAbs 13, 1912884 (2021).
pubmed: 33876699 pmcid: 8078717 doi: 10.1080/19420862.2021.1912884
Caban, M. et al. Cross-protective antibodies against common endemic respiratory viruses. Nat. Commun. 14, 798 (2023).
pubmed: 36781872 pmcid: 9923667 doi: 10.1038/s41467-023-36459-3
Madhi, S. A. et al. Transmissibility, infectivity and immunogenicity of a live human parainfluenza type 3 virus vaccine (HP1V345) among susceptible infants and toddlers. Vaccine 24, 2432–2439 (2006).
pubmed: 16406170 doi: 10.1016/j.vaccine.2005.12.002
Bernstein, D. I., Falloon, J. & Yi, T. T. A randomized, double-blind, placebo-controlled, phase 1/2a study of the safety and immunogenicity of a live, attenuated human parainfluenza virus type 3 vaccine in healthy infants. Vaccine 29, 7042–7048 (2011).
pubmed: 21782874 doi: 10.1016/j.vaccine.2011.07.031
Karron, R. A. et al. Evaluation of a live attenuated bovine parainfluenza type 3 vaccine in two- to six-month-old infants. Pediatr. Infect. Dis. J. 15, 650–654 (1996).
pubmed: 8858666 doi: 10.1097/00006454-199608000-00003
Gomez, M. et al. Phase-I study MEDI-534, of a live, attenuated intranasal vaccine against respiratory syncytial virus and parainfluenza-3 virus in seropositive children. Pediatr. Infect. Dis. J. 28, 655–658 (2009).
pubmed: 19483659 doi: 10.1097/INF.0b013e318199c3b1
Greninger, A. L. A decade of RNA virus metagenomics is (not) enough. Virus Res. 244, 218–229 (2018).
pubmed: 29055712 doi: 10.1016/j.virusres.2017.10.014
Palermo, L. M. et al. Features of circulating parainfluenza virus required for growth in human airway. mBio 7, e00235 (2016).
pubmed: 26980833 pmcid: 4807361 doi: 10.1128/mBio.00235-16
Krammer, F. et al. NAction! How can neuraminidase-based immunity contribute to better influenza virus vaccines? mBio 9, e02332-17 (2018).
pubmed: 29615508 pmcid: 5885027 doi: 10.1128/mBio.02332-17
Monto, A. S. et al. Antibody to influenza virus neuraminidase: an independent correlate of protection. J. Infect. Dis. 212, 1191–1199 (2015).
pubmed: 25858957 doi: 10.1093/infdis/jiv195
Yin, H. S., Wen, X., Paterson, R. G., Lamb, R. A. & Jardetzky, T. S. Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439, 38–44 (2006).
pubmed: 16397490 pmcid: 7095149 doi: 10.1038/nature04322
White, J. M., Delos, S. E., Brecher, M. & Schornberg, K. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 43, 189–219 (2008).
pubmed: 18568847 pmcid: 2649671 doi: 10.1080/10409230802058320
Harrison, S. C. Viral membrane fusion. Nat. Struct. Mol. Biol. 15, 690–698 (2008).
pubmed: 18596815 pmcid: 2517140 doi: 10.1038/nsmb.1456
Wen, X. et al. Structure of the human metapneumovirus fusion protein with neutralizing antibody identifies a pneumovirus antigenic site. Nat. Struct. Mol. Biol. 19, 461–463 (2012).
pubmed: 22388735 pmcid: 3546531 doi: 10.1038/nsmb.2250
Jiang, J. J. et al. Functional analysis of amino acids at stalk/head interface of human parainfluenza virus type 3 hemagglutinin-neuraminidase protein in the membrane fusion process. Virus Genes 54, 333–342 (2018).
pubmed: 29516315 doi: 10.1007/s11262-018-1546-3
Li, L. et al. AbRSA: a robust tool for antibody numbering. Protein Sci. 28, 1524–1531 (2019).
pubmed: 31020723 pmcid: 6635766 doi: 10.1002/pro.3633
Pascolutti, M. et al. Structural insights into human parainfluenza virus 3 hemagglutinin-neuraminidase using unsaturated 3- N-substituted sialic acids as probes. ACS Chem. Biol. 13, 1544–1550 (2018).
pubmed: 29693380 doi: 10.1021/acschembio.8b00150
Taylor, G. Sialidases: structures, biological significance and therapeutic potential. Curr. Opin. Struct. Biol. 6, 830–837 (1996).
pubmed: 8994884 doi: 10.1016/S0959-440X(96)80014-5
Winger, M. & von Itzstein, M. Exposing the flexibility of human parainfluenza virus hemagglutinin-neuraminidase. J. Am. Chem. Soc. 134, 18447–18452 (2012).
pubmed: 23057491 doi: 10.1021/ja3084658
Bailly, B. et al. A dual drug regimen synergistically blocks human parainfluenza virus infection. Sci. Rep. 6, 24138 (2016).
pubmed: 27053240 pmcid: 4823791 doi: 10.1038/srep24138
Yuan, P., Paterson, R. G., Leser, G. P., Lamb, R. A. & Jardetzky, T. S. Structure of the Ulster strain Newcastle disease virus hemagglutinin-neuraminidase reveals auto-inhibitory interactions associated with low virulence. PLoS Pathog. 8, e1002855 (2012).
pubmed: 22912577 pmcid: 3415446 doi: 10.1371/journal.ppat.1002855
Zaitsev, V. et al. Second sialic acid binding site in Newcastle disease virus hemagglutinin-neuraminidase: implications for fusion. J. Virol. 78, 3733–3741 (2004).
pubmed: 15016893 pmcid: 371092 doi: 10.1128/JVI.78.7.3733-3741.2004
Welch, S. R. et al. Inhibition of Nipah virus by defective interfering particles. J. Infect. Dis. 221, S460–S470 (2020).
pubmed: 32108876 doi: 10.1093/infdis/jiz564
Borisevich, V. et al. Escape from monoclonal antibody neutralization affects henipavirus fitness in vitro and in vivo. J. Infect. Dis. 213, 448–455 (2016).
pubmed: 26357909 doi: 10.1093/infdis/jiv449
Chou, T. C. Drug combination studies and their synergy quantification using the Chou–Talalay method. Cancer Res. 70, 440–446 (2010).
pubmed: 20068163 doi: 10.1158/0008-5472.CAN-09-1947
Ashton, J. C. Drug combination studies and their synergy quantification using the Chou–Talalay method—letter. Cancer Res. 75, 2400 (2015).
pubmed: 25977339 doi: 10.1158/0008-5472.CAN-14-3763
Gilchuk, P. et al. Analysis of a therapeutic antibody cocktail reveals determinants for cooperative and broad ebolavirus neutralization. Immunity 52, 388–403.e12 (2020).
pubmed: 32023489 pmcid: 7111202 doi: 10.1016/j.immuni.2020.01.001
Bernstein, D. I. et al. Phase 1 study of the safety and immunogenicity of a live, attenuated respiratory syncytial virus and parainfluenza virus type 3 vaccine in seronegative children. Pediatr. Infect. Dis. J. 31, 109–114 (2012).
pubmed: 21926667 doi: 10.1097/INF.0b013e31823386f1
Madhi, S. A. et al. Transmissibility, infectivity and immunogenicity of a live human parainfluenza type 3 virus vaccine (HP1V3cp45) among susceptible infants and toddlers. Vaccine 24, 2432–2439 (2006).
pubmed: 16406170 doi: 10.1016/j.vaccine.2005.12.002
Skiadopoulos, M. H. et al. Evaluation of the replication and immunogenicity of recombinant human parainfluenza virus type 3 vectors expressing up to three foreign glycoproteins. Virology 297, 136–152 (2002).
pubmed: 12083844 doi: 10.1006/viro.2002.1415
Karron, R. A. et al. A live human parainfluenza type 3 virus vaccine is attenuated and immunogenic in young infants. Pediatr. Infect. Dis. J. 22, 394–405 (2003).
pubmed: 12792378 doi: 10.1097/01.inf.0000066244.31769.83
Domachowske, J. et al. Safety of nirsevimab for RSV in infants with heart or lung disease or prematurity. N. Engl. J. Med. 386, 892–894 (2022).
pubmed: 35235733 doi: 10.1056/NEJMc2112186
Ginsburg, A. S. & Srikantiah, P. Respiratory syncytial virus: promising progress against a leading cause of pneumonia. Lancet Glob. Health 9, e1644–e1645 (2021).
pubmed: 34774184 pmcid: 8585487 doi: 10.1016/S2214-109X(21)00455-1
Fernandez, P. et al. A phase 2, randomized, double-blind safety and pharmacokinetic assessment of respiratory syncytial virus (RSV) prophylaxis with motavizumab and palivizumab administered in the same season. BMC Pediatr. 10, 38 (2010).
pubmed: 20525274 pmcid: 2898783 doi: 10.1186/1471-2431-10-38
Edupuganti, S. et al. Feasibility and successful enrollment in a proof-of-concept HIV prevention trial of VRC01, a broadly neutralizing HIV-1 monoclonal antibody. J. Acquir. Immune Defic. Syndr. 87, 671–679 (2021).
pubmed: 33587505 pmcid: 8397466 doi: 10.1097/QAI.0000000000002639
Mgodi, N. M. et al. A phase 2b study to evaluate the safety and efficacy of VRC01 broadly neutralizing monoclonal antibody in reducing acquisition of HIV-1 infection in women in sub-saharan Africa: baseline findings. J. Acquir. Immune Defic. Syndr. 87, 680–687 (2021).
pubmed: 33587510 pmcid: 8436719 doi: 10.1097/QAI.0000000000002649
Corey, L. et al. Two randomized trials of neutralizing antibodies to prevent HIV-1 acquisition. N. Engl. J. Med. 384, 1003–1014 (2021).
pubmed: 33730454 pmcid: 8189692 doi: 10.1056/NEJMoa2031738
Han, A. et al. Safety and efficacy of CR6261 in an influenza A H1N1 healthy human challenge model. Clin. Infect. Dis. 73, e4260–e4268 (2021).
pubmed: 33211860 doi: 10.1093/cid/ciaa1725
Ali, S. O. et al. Evaluation of MEDI8852, an anti-influenza A monoclonal antibody, in treating acute uncomplicated influenza. Antimicrob. Agents Chemother. https://doi.org/10.1128/AAC.00694-18 (2018).
Johnson, S. et al. Development of a humanized monoclonal antibody (MEDI-493) with potent in vitro and in vivo activity against respiratory syncytial virus. J. Infect. Dis. 176, 1215–1224 (1997).
pubmed: 9359721 doi: 10.1086/514115
Guillon, P. et al. Structure-guided discovery of potent and dual-acting human parainfluenza virus haemagglutinin-neuraminidase inhibitors. Nat. Commun. 5, 5268 (2014).
pubmed: 25327774 doi: 10.1038/ncomms6268
Xu, R. et al. A recurring motif for antibody recognition of the receptor-binding site of influenza hemagglutinin. Nat. Struct. Mol. Biol. 20, 363–370 (2013).
pubmed: 23396351 pmcid: 3594569 doi: 10.1038/nsmb.2500
Hong, M. et al. Antibody recognition of the pandemic H1N1 Influenza virus hemagglutinin receptor binding site. J. Virol. 87, 12471–12480 (2013).
pubmed: 24027321 pmcid: 3807900 doi: 10.1128/JVI.01388-13
Palermo, L. M., Porotto, M., Greengard, O. & Moscona, A. Fusion promotion by a paramyxovirus hemagglutinin-neuraminidase protein: pH modulation of receptor avidity of binding sites I and II. J. Virol. 81, 9152–9161 (2007).
pubmed: 17567695 pmcid: 1951465 doi: 10.1128/JVI.00888-07
Chng, J. et al. Cleavage efficient 2A peptides for high level monoclonal antibody expression in CHO cells. MAbs 7, 403–412 (2015).
pubmed: 25621616 pmcid: 4622431 doi: 10.1080/19420862.2015.1008351
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
pubmed: 28250466 pmcid: 5494038 doi: 10.1038/nmeth.4193
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
pubmed: 28165473 doi: 10.1038/nmeth.4169
Sanchez-Garcia, R. et al. DeepEMhancer: a deep learning solution for cryo-EM volume post-processing. Commun. Biol. 4, 874 (2021).
pubmed: 34267316 pmcid: 8282847 doi: 10.1038/s42003-021-02399-1
Waterhouse, A. et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 46, W296–W303 (2018).
pubmed: 29788355 pmcid: 6030848 doi: 10.1093/nar/gky427
Teplyakov, A. et al. Structural diversity in a human antibody germline library. MAbs 8, 1045–1063 (2016).
pubmed: 27210805 pmcid: 4968113 doi: 10.1080/19420862.2016.1190060
Dejnirattisai, W. et al. The antigenic anatomy of SARS-CoV-2 receptor binding domain. Cell 184, 2183–2200.e22 (2021).
pubmed: 33756110 pmcid: 7891125 doi: 10.1016/j.cell.2021.02.032
Spurrier, B. et al. Structural analysis of human and macaque mAbs 2909 and 2.5B: implications for the configuration of the quaternary neutralizing epitope of HIV-1 gp120. Structure 19, 691–699 (2011).
pubmed: 21565703 pmcid: 3096878 doi: 10.1016/j.str.2011.02.012
Bonsignori, M. et al. Maturation pathway from germline to broad HIV-1 neutralizer of a CD4-mimic antibody. Cell 165, 449–463 (2016).
pubmed: 26949186 pmcid: 4826291 doi: 10.1016/j.cell.2016.02.022
Jiang, W. et al. Characterization of MW06, a human monoclonal antibody with cross-neutralization activity against both SARS-CoV-2 and SARS-CoV. MAbs 13, 1953683 (2021).
pubmed: 34313527 pmcid: 8317929 doi: 10.1080/19420862.2021.1953683
Pettersen, E. F. et al. UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
pubmed: 15264254 doi: 10.1002/jcc.20084
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).
pubmed: 20383002 pmcid: 2852313 doi: 10.1107/S0907444910007493
Liebschner, D. et al. Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix. Acta Crystallogr. D 75, 861–877 (2019).
doi: 10.1107/S2059798319011471
Schiffrin, B., Radford, S. E., Brockwell, D. J. & Calabrese, A. N. PyXlinkViewer: a flexible tool for visualization of protein chemical crosslinking data within the PyMOL molecular graphics system. Protein Sci. 29, 1851–1857 (2020).
pubmed: 32557917 pmcid: 7380677 doi: 10.1002/pro.3902
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
Greninger, A. L. et al. Rapid metagenomic next-generation sequencing during an investigation of hospital-acquired human parainfluenza virus 3 infections. J. Clin. Microbiol. 55, 177–182 (2017).
pubmed: 27795347 doi: 10.1128/JCM.01881-16
Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425 (1987).
pubmed: 3447015
Tamura, K., Stecher, G. & Kumar, S. MEGA11: molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38, 3022–3027 (2021).
pubmed: 33892491 pmcid: 8233496 doi: 10.1093/molbev/msab120

Auteurs

Naveenchandra Suryadevara (N)

Vanderbilt Vaccine Center, Vanderbilt University Medical Center, Nashville, TN, USA.

Ana Rita Otrelo-Cardoso (AR)

Department of Structural Biology, Stanford University School of Medicine, Stanford, CA, USA.

Nurgun Kose (N)

Vanderbilt Vaccine Center, Vanderbilt University Medical Center, Nashville, TN, USA.

Yao-Xiong Hu (YX)

Department of Structural Biology, Stanford University School of Medicine, Stanford, CA, USA.

Elad Binshtein (E)

Vanderbilt Vaccine Center, Vanderbilt University Medical Center, Nashville, TN, USA.

Rachael M Wolters (RM)

Vanderbilt Vaccine Center, Vanderbilt University Medical Center, Nashville, TN, USA.

Alexander L Greninger (AL)

Department of Laboratory Medicine and Pathology, University of Washington Medical Center, Seattle, WA, USA.

Laura S Handal (LS)

Vanderbilt Vaccine Center, Vanderbilt University Medical Center, Nashville, TN, USA.

Robert H Carnahan (RH)

Vanderbilt Vaccine Center, Vanderbilt University Medical Center, Nashville, TN, USA.
Department of Pediatrics, Vanderbilt University Medical Center, Nashville, TN, USA.

Anne Moscona (A)

Departments of Pediatrics, Microbiology and Immunology, and Physiology and Cellular Biophysics, and Center for Host-Pathogen Interaction, Columbia University Vagelos College of Physicians and Surgeons, New York, NY, USA.

Theodore S Jardetzky (TS)

Department of Structural Biology, Stanford University School of Medicine, Stanford, CA, USA. tjardetz@stanford.edu.

James E Crowe (JE)

Vanderbilt Vaccine Center, Vanderbilt University Medical Center, Nashville, TN, USA. james.crowe@vumc.org.
Department of Pediatrics, Vanderbilt University Medical Center, Nashville, TN, USA. james.crowe@vumc.org.
Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA. james.crowe@vumc.org.

Classifications MeSH