MHC class II proteins mediate sialic acid independent entry of human and avian H2N2 influenza A viruses.

التفاصيل البيبلوغرافية
العنوان:	MHC class II proteins mediate sialic acid independent entry of human and avian H2N2 influenza A viruses.
المؤلفون:	Karakus U; Institute of Medical Virology, University of Zurich, Zurich, Switzerland.; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA., Sempere Borau M; Institute of Medical Virology, University of Zurich, Zurich, Switzerland., Martínez-Barragán P; Institute of Medical Virology, University of Zurich, Zurich, Switzerland., von Kempis J; Institute of Medical Virology, University of Zurich, Zurich, Switzerland., Yildiz S; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA., Arroyo-Fernández LM; Institute of Medical Virology, University of Zurich, Zurich, Switzerland., Pohl MO; Institute of Medical Virology, University of Zurich, Zurich, Switzerland., Steiger JA; Institute of Medical Virology, University of Zurich, Zurich, Switzerland., Glas I; Institute of Medical Virology, University of Zurich, Zurich, Switzerland., Hunziker A; Institute of Medical Virology, University of Zurich, Zurich, Switzerland., García-Sastre A; Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Department of Medicine, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; The Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; Department of Pathology, Molecular and Cell-Based Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA.; The Icahn Genomics Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA., Stertz S; Institute of Medical Virology, University of Zurich, Zurich, Switzerland. stertz.silke@virology.uzh.ch.
المصدر:	Nature microbiology [Nat Microbiol] 2024 Jul 15. Date of Electronic Publication: 2024 Jul 15.
Publication Model:	Ahead of Print
نوع المنشور:	Journal Article
اللغة:	English
بيانات الدورية:	Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101674869 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2058-5276 (Electronic) Linking ISSN: 20585276 NLM ISO Abbreviation: Nat Microbiol Subsets: MEDLINE
أسماء مطبوعة:	Original Publication: [London] : Nature Publishing Group, [2016]-
مستخلص:	Influenza A viruses (IAV) pose substantial burden on human and animal health. Avian, swine and human IAV bind sialic acid on host glycans as receptor, whereas some bat IAV require MHC class II complexes for cell entry. It is unknown how this difference evolved and whether dual receptor specificity is possible. Here we show that human H2N2 IAV and related avian H2N2 possess dual receptor specificity in cell lines and primary human airway cultures. Using sialylation-deficient cells, we reveal that entry via MHC class II is independent of sialic acid. We find that MHC class II from humans, pigs, ducks, swans and chickens but not bats can mediate H2 IAV entry and that this is conserved in Eurasian avian H2. Our results demonstrate that IAV can possess dual receptor specificity for sialic acid and MHC class II, and suggest a role for MHC class II-dependent entry in zoonotic IAV infections. (© 2024. The Author(s), under exclusive licence to Springer Nature Limited.)
References:	Long, J. S., Mistry, B., Haslam, S. M. & Barclay, W. S. Host and viral determinants of influenza A virus species specificity. Nat. Rev. Microbiol. 17, 67–81 (2019). (PMID: 3048753610.1038/s41579-018-0115-z) Schrauwen, E. J. & Fouchier, R. A. Host adaptation and transmission of influenza A viruses in mammals. Emerg. Microbes Infect. 3, e9 (2014). (PMID: 26038511394412310.1038/emi.2014.9) Imai, M. & Kawaoka, Y. The role of receptor binding specificity in interspecies transmission of influenza viruses. Curr. Opin. Virol. 2, 160–167 (2012). (PMID: 22445963560575210.1016/j.coviro.2012.03.003) Gamblin, S. J. et al. Hemagglutinin structure and activities. Cold Spring Harb. Perspect. Med. https://doi.org/10.1101/cshperspect.a038638 (2021). Gottschalk, A. On the mechanism underlying initiation of influenza virus infection. Ergeb. Mikrobiol. Immunitatsforsch. Exp. Ther. 32, 1–22 (1959). (PMID: 13652926) Rogers, G. N. & Paulson, J. C. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 127, 361–373 (1983). (PMID: 686837010.1016/0042-6822(83)90150-2) Carroll, S. M. & Paulson, J. C. Differential infection of receptor-modified host cells by receptor-specific influenza viruses. Virus Res. 3, 165–179 (1985). (PMID: 406088610.1016/0168-1702(85)90006-1) Stevens, J. et al. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J. Mol. Biol. 355, 1143–1155 (2006). (PMID: 1634353310.1016/j.jmb.2005.11.002) Gambaryan, A. S. et al. Specification of receptor-binding phenotypes of influenza virus isolates from different hosts using synthetic sialylglycopolymers: non-egg-adapted human H1 and H3 influenza A and influenza B viruses share a common high binding affinity for 6’-sialyl(N-acetyllactosamine). Virology 232, 345–350 (1997). (PMID: 919184810.1006/viro.1997.8572) Matrosovich, M. N. et al. Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 233, 224–234 (1997). (PMID: 920123210.1006/viro.1997.8580) Zhu, X. et al. Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc. Natl Acad. Sci. USA 110, 1458–1463 (2013). (PMID: 23297216355707310.1073/pnas.1218509110) Sun, X. et al. Bat-derived influenza hemagglutinin H17 does not bind canonical avian or human receptors and most likely uses a unique entry mechanism. Cell Rep. 3, 769–778 (2013). (PMID: 2343451010.1016/j.celrep.2013.01.025) Tong, S. et al. New world bats harbor diverse influenza A viruses. PLoS Pathog. 9, e1003657 (2013). (PMID: 24130481379499610.1371/journal.ppat.1003657) Tong, S. et al. A distinct lineage of influenza A virus from bats. Proc. Natl Acad. Sci. USA 109, 4269–4274 (2012). (PMID: 22371588330667510.1073/pnas.1116200109) Karakus, U. et al. MHC class II proteins mediate cross-species entry of bat influenza viruses. Nature 567, 109–112 (2019). (PMID: 3078743910.1038/s41586-019-0955-3) Ciminski, K., Pfaff, F., Beer, M. & Schwemmle, M. Bats reveal the true power of influenza A virus adaptability. PLoS Pathog. 16, e1008384 (2020). (PMID: 32298389716194610.1371/journal.ppat.1008384) Connor, R. J., Kawaoka, Y., Webster, R. G. & Paulson, J. C. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205, 17–23 (1994). (PMID: 797521210.1006/viro.1994.1615) Han, J. et al. Genome-wide CRISPR/Cas9 screen identifies host factors essential for influenza virus replication. Cell Rep. 23, 596–607 (2018). (PMID: 29642015593957710.1016/j.celrep.2018.03.045) Murakami, S. et al. Enhanced growth of influenza vaccine seed viruses in Vero cells mediated by broadening the optimal pH range for virus membrane fusion. J. Virol. 86, 1405–1410 (2012). (PMID: 22090129326436810.1128/JVI.06009-11) Olajide, O. M. et al. Evolutionarily conserved amino acids in MHC-II mediate bat influenza A virus entry into human cells. PLoS Biol. 21, e3002182 (2023). (PMID: 374107981032506810.1371/journal.pbio.3002182) Jones, J. C. et al. Risk assessment of H2N2 influenza viruses from the avian reservoir. J. Virol. 88, 1175–1188 (2014). (PMID: 24227848391167010.1128/JVI.02526-13) Krause, J. C. et al. Human monoclonal antibodies to pandemic 1957 H2N2 and pandemic 1968 H3N2 influenza viruses. J. Virol. 86, 6334–6340 (2012). (PMID: 22457520337219910.1128/JVI.07158-11) Cline, T. D., Karlsson, E. A., Seufzer, B. J. & Schultz-Cherry, S. The hemagglutinin protein of highly pathogenic H5N1 influenza viruses overcomes an early block in the replication cycle to promote productive replication in macrophages. J. Virol. 87, 1411–1419 (2013). (PMID: 23152519355417110.1128/JVI.02682-12) Riser, B. L. & Maassab, H. F. Differential interaction of virulent and attenuated influenza virus strains with ferret alveolar macrophages: possible role in pathogenicity. J. Infect. Dis. 161, 699–705 (1990). (PMID: 218103210.1093/infdis/161.4.699) Forrester, M. A. et al. Similarities and differences in surface receptor expression by THP-1 monocytes and differentiated macrophages polarized using seven different conditioning regimens. Cell Immunol. 332, 58–76 (2018). (PMID: 30077333761163710.1016/j.cellimm.2018.07.008) Genin, M., Clement, F., Fattaccioli, A., Raes, M. & Michiels, C. M1 and M2 macrophages derived from THP-1 cells differentially modulate the response of cancer cells to etoposide. BMC Cancer 15, 577 (2015). (PMID: 26253167454581510.1186/s12885-015-1546-9) Karakus, U. et al. H19 influenza A virus exhibits species-specific MHC class II receptor usage. Cell Host Microbe https://doi.org/10.1016/j.chom.2024.05.018 (2024). Pappas, C. et al. Assessment of transmission, pathogenesis and adaptation of H2 subtype influenza viruses in ferrets. Virology 477, 61–71 (2015). (PMID: 2565981810.1016/j.virol.2015.01.002) Lenny, B. J. et al. Evaluation of multivalent H2 influenza pandemic vaccines in mice. Vaccine 35, 1455–1463 (2017). (PMID: 28189402533651610.1016/j.vaccine.2017.01.026) Martínez-Sobrido, L. & García-Sastre, A. Generation of recombinant influenza virus from plasmid DNA. J. Vis. Exp. https://doi.org/10.3791/2057 (2010). (PMID: 10.3791/2057207298043156010) Hai, R. et al. Influenza A(H7N9) virus gains neuraminidase inhibitor resistance without loss of in vivo virulence or transmissibility. Nat. Commun. 4, 2854 (2013). (PMID: 2432687510.1038/ncomms3854) Steel, J. et al. Live attenuated influenza viruses containing NS1 truncations as vaccine candidates against H5N1 highly pathogenic avian influenza. J. Virol. 83, 1742–1753 (2009). (PMID: 1907373110.1128/JVI.01920-08) Pugach, P. et al. HIV-1 clones resistant to a small molecule CCR5 inhibitor use the inhibitor-bound form of CCR5 for entry. Virology 361, 212–228 (2007). (PMID: 1716654010.1016/j.virol.2006.11.004) Tscherne, D. M., Manicassamy, B. & Garcia-Sastre, A. An enzymatic virus-like particle assay for sensitive detection of virus entry. J. Virol. Methods 163, 336–343 (2010). (PMID: 1987930010.1016/j.jviromet.2009.10.020) Whitt, M. A. Generation of VSV pseudotypes using recombinant DeltaG-VSV for studies on virus entry, identification of entry inhibitors, and immune responses to vaccines. J. Virol. Methods 169, 365–374 (2010). (PMID: 20709108295619210.1016/j.jviromet.2010.08.006) Madeira, F. et al. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 47, W636–W641 (2019). (PMID: 30976793660247910.1093/nar/gkz268) Khare, S. et al. GISAID’s role in pandemic response. China CDC Wkly 3, 1049–1051 (2021). (PMID: 34934514866840610.46234/ccdcw2021.255) de Castro, E. et al. ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 34, W362–W365 (2006). (PMID: 16845026153884710.1093/nar/gkl124) Prescott, R. A. et al. A comparative study of in vitro air-liquid interface culture models of the human airway epithelium evaluating cellular heterogeneity and gene expression at single cell resolution. Respir. Res. 24, 213 (2023). (PMID: 376352511046415310.1186/s12931-023-02514-2) Zepp, J. A. & Morrisey, E. E. Cellular crosstalk in the development and regeneration of the respiratory system. Nat. Rev. Mol. Cell Biol. 20, 551–566 (2019). (PMID: 31217577725449910.1038/s41580-019-0141-3) Travaglini, K. J. et al. A molecular cell atlas of the human lung from single-cell RNA sequencing. Nature 587, 619–625 (2020). (PMID: 33208946770469710.1038/s41586-020-2922-4) Bonser, L. R. et al. Flow-cytometric analysis and purification of airway epithelial-cell subsets. Am. J. Respir. Cell Mol. Biol. 64, 308–317 (2021). (PMID: 33196316790933510.1165/rcmb.2020-0149MA) Wyrzucki, A., Bianchi, M., Kohler, I., Steck, M. & Hangartner, L. Heterosubtypic antibodies to influenza A virus have limited activity against cell-bound virus but are not impaired by strain-specific serum antibodies. J. Virol. 89, 3136–3144 (2015). (PMID: 2555271810.1128/JVI.03069-14) Hurskainen, M. et al. Single cell transcriptomic analysis of murine lung development on hyperoxia-induced damage. Nat. Commun. 12, 1565 (2021). (PMID: 33692365794694710.1038/s41467-021-21865-2) Xu, R., McBride, R., Paulson, J. C., Basler, C. F. & Wilson, I. A. Structure, receptor binding, and antigenicity of influenza virus hemagglutinins from the 1957 H2N2 pandemic. J. Virol. 84, 1715–1721 (2010). (PMID: 2000727110.1128/JVI.02162-09)
معلومات مُعتمدة:	310030_204166 Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation); P500PB_206818 Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation); P400PB_199292 Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation); 18C190 Novartis Stiftung für Medizinisch-Biologische Forschung (Novartis Foundation for Medical-Biological Research); 75N93021C00014 United States AI NIAID NIH HHS; U19AI142733 U.S. Department of Health & Human Services \| NIH \| National Institute of Allergy and Infectious Diseases (NIAID); U19AI168631 U.S. Department of Health & Human Services \| NIH \| National Institute of Allergy and Infectious Diseases (NIAID)
تواريخ الأحداث:	Date Created: 20240715 Latest Revision: 20240715
رمز التحديث:	20240716
DOI:	10.1038/s41564-024-01771-1
PMID:	39009691
قاعدة البيانات:	MEDLINE

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تدمد:	2058-5276
DOI:	10.1038/s41564-024-01771-1