FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / J Virol / N-Glycolylneuraminic Acid Binding of Avian and Equine H7 Inf...
Journal of virology2022; 96(5); e0212021; doi: 10.1128/jvi.02120-21

N-Glycolylneuraminic Acid Binding of Avian and Equine H7 Influenza A Viruses.

Abstract: Influenza A viruses (IAV) initiate infection by binding to glycans with terminal sialic acids on the cell surface. Hosts of IAV variably express two major forms of sialic acid, -acetylneuraminic acid (NeuAc) and -glycolylneuraminic acid (NeuGc). NeuGc is produced in most mammals, including horses and pigs, but is absent in humans, ferrets, and birds. The only known naturally occurring IAV that exclusively bind NeuGc are extinct highly pathogenic equine H7N7 viruses. We determined the crystal structure of a representative equine H7 hemagglutinin (HA) in complex with NeuGc and observed high similarity in the receptor-binding domain with an avian H7 HA. To determine the molecular basis for NeuAc and NeuGc specificity, we performed systematic mutational analyses, based on the structural insights, on two distant avian H7 HAs and an H15 HA. We found that the A135E mutation is key for binding α2,3-linked NeuGc but does not abolish NeuAc binding. The additional mutations S128T, I130V, T189A, and K193R converted the specificity from NeuAc to NeuGc. We investigated the residues at positions 128, 130, 135, 189, and 193 in a phylogenetic analysis of avian and equine H7 HAs. This analysis revealed a clear distinction between equine and avian residues. The highest variability was observed at key position 135, of which only the equine glutamic acid led to NeuGc binding. These results demonstrate that genetically distinct H7 and H15 HAs can be switched from NeuAc to NeuGc binding and vice versa after the introduction of several mutations, providing insights into the adaptation of H7 viruses to NeuGc receptors. Influenza A viruses cause millions of cases of severe illness and deaths annually. To initiate infection and replicate, the virus first needs to bind to a structure on the cell surface, like a key fitting in a lock. For influenza A viruses, these "keys" (receptors) on the cell surface are chains of sugar molecules (glycans). The terminal sugar on these glycans is often either -acetylneuraminic acid (NeuAc) or -glycolylneuraminic acid (NeuGc). Most influenza A viruses bind NeuAc, but a small minority bind NeuGc. NeuGc is present in species like horses, pigs, and mice but not in humans, ferrets, and birds. Here, we investigated the molecular determinants of NeuGc specificity and the origin of viruses that bind NeuGc.
Get Full Text
Publication Date: 2022-01-19 PubMed ID: 35044215PubMed Central: PMC8906439DOI: 10.1128/jvi.02120-21Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't
  • Research Support
  • U.S. Gov't
  • Non-P.H.S.

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 investigates how the Influenza A virus binds to chains of sugar molecules, particularly a type called N-glycolylneuraminic acid (NeuGc), to initiate infection in hosts. The study finds key mutations that allow the virus to bind with NeuGc, shedding light on the adaptation of Influenza A viruses to different hosts.

Introduction to Influenza A Virus

  • Influenza A Virus (IAV) causes severe illness and death each year across the globe.
  • To start an infection and replicate, the virus needs to connect to a structure on the cell surface—this mechanism is similar to a key fitting into a lock.

Understanding NeuAc and NeuGc Receptors

  • These “keys” or receptors on the cell surface are known as chains of sugar molecules (glycans). The terminal sugar on these glycans is either N-acetylneuraminic acid (NeuAc) or N-glycolylneuraminic acid (NeuGc).
  • While most IAVs bind to NeuAc, a small percentage binds to NeuGc.
  • NeuGc is found in different species such as horses, pigs, and mice, but it’s absent in humans, ferrets, and birds, creating distinctive avenues for the virus to infect different types of hosts.

Objectives of the Research

  • This study aims to investigate the molecular determinants of NeuGc specificity and the origin of viruses capable of binding to NeuGc.
  • By better understanding these mechanisms, researchers can further study the adaptation and evolution of the virus across species and develop new strategies for preventing and treating infections.

Findings of the Research

  • The researchers identified key mutations (A135E, S128T, I130V, T189A, and K193R) that switch the virus’s binding preference from NeuAc to NeuGc.
  • These results indicate that genetically distinct H7 and H15 influenza A viruses can change their binding specificity based on the introduction of certain mutations.
  • The highest variability was observed at the key position 135, where only the equine glutamic acid resulted in NeuGc binding. This reveals the significant role played by this specific amino acid in influencing the binding ability of the virus.
  • This knowledge provides valuable insight into how different influenza A strains adapt to recognize and bind with NeuGc receptors on host cells.

Cite This Article

APA
Spruit CM, Zhu X, Tomris I, Ríos-Carrasco M, Han AX, Broszeit F, van der Woude R, Bouwman KM, Luu MMT, Matsuno K, Sakoda Y, Russell CA, Wilson IA, Boons GJ, de Vries RP. (2022). N-Glycolylneuraminic Acid Binding of Avian and Equine H7 Influenza A Viruses. J Virol, 96(5), e0212021. https://doi.org/10.1128/jvi.02120-21

Publication

Journal of virology
ISSN: 1098-5514
NlmUniqueID: 0113724
Country: United States
Language: English
Volume: 96
Issue: 5
Pages: e0212021
PII: e02120-21

Researcher Affiliations

Spruit, Cindy M
  • Department of Chemical Biology & Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht Universitygrid.5477.1, Utrecht, the Netherlands.
Zhu, Xueyong
  • Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, California, USA.
Tomris, Ilhan
  • Department of Chemical Biology & Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht Universitygrid.5477.1, Utrecht, the Netherlands.
Ríos-Carrasco, María
  • Department of Chemical Biology & Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht Universitygrid.5477.1, Utrecht, the Netherlands.
Han, Alvin X
  • Department of Medical Microbiology, Amsterdam University Medical Center, Amsterdam, the Netherlands.
Broszeit, Frederik
  • Department of Chemical Biology & Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht Universitygrid.5477.1, Utrecht, the Netherlands.
van der Woude, Roosmarijn
  • Department of Chemical Biology & Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht Universitygrid.5477.1, Utrecht, the Netherlands.
Bouwman, Kim M
  • Department of Chemical Biology & Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht Universitygrid.5477.1, Utrecht, the Netherlands.
Luu, Michel M T
  • Department of Chemical Biology & Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht Universitygrid.5477.1, Utrecht, the Netherlands.
Matsuno, Keita
  • Division of Risk Analysis and Management, International Institute for Zoonosis Control, Hokkaido Universitygrid.39158.36, Sapporo, Japan.
  • International Collaboration Unit, International Institute for Zoonosis Control, Hokkaido Universitygrid.39158.36, Sapporo, Japan.
  • One Health Research Center, Hokkaido Universitygrid.39158.36, Sapporo, Japan.
Sakoda, Yoshihiro
  • International Collaboration Unit, International Institute for Zoonosis Control, Hokkaido Universitygrid.39158.36, Sapporo, Japan.
  • One Health Research Center, Hokkaido Universitygrid.39158.36, Sapporo, Japan.
  • Laboratory of Microbiology, Department of Disease Control, Faculty of Veterinary Medicine, Hokkaido Universitygrid.39158.36, Sapporo, Japan.
Russell, Colin A
  • Department of Medical Microbiology, Amsterdam University Medical Center, Amsterdam, the Netherlands.
Wilson, Ian A
  • Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, California, USA.
  • Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, California, USA.
Boons, Geert-Jan
  • Department of Chemical Biology & Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht Universitygrid.5477.1, Utrecht, the Netherlands.
  • Complex Carbohydrate Research Center, University of Georgia, Athens, Georgia, USA.
de Vries, Robert P
  • Department of Chemical Biology & Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht Universitygrid.5477.1, Utrecht, the Netherlands.

MeSH Terms

  • Animals
  • Hemagglutinin Glycoproteins, Influenza Virus / chemistry
  • Hemagglutinin Glycoproteins, Influenza Virus / genetics
  • Hemagglutinin Glycoproteins, Influenza Virus / metabolism
  • Horses
  • Humans
  • Influenza A Virus, H7N7 Subtype / chemistry
  • Influenza A Virus, H7N7 Subtype / metabolism
  • N-Acetylneuraminic Acid
  • Neuraminic Acids / chemistry
  • Neuraminic Acids / metabolism
  • Phylogeny
  • Polysaccharides / metabolism
  • Protein Binding

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 64 references
  1. Skehel JJ, Wiley DC. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin.. Annu Rev Biochem 2000;69:531-69.
    doi: 10.1146/annurev.biochem.69.1.531pubmed: 10966468google scholar: lookup
  2. Long JS, Mistry B, Haslam SM, Barclay WS. Host and viral determinants of influenza A virus species specificity.. Nat Rev Microbiol 2019 Jan;17(2):67-81.
    doi: 10.1038/s41579-018-0115-zpubmed: 30487536google scholar: lookup
  3. Ji Y, White YJ, Hadden JA, Grant OC, Woods RJ. New insights into influenza A specificity: an evolution of paradigms.. Curr Opin Struct Biol 2017 Jun;44:219-231.
    doi: 10.1016/j.sbi.2017.06.001pmc: PMC5715462pubmed: 28675835google scholar: lookup
  4. de Vries RP, Zhu X, McBride R, Rigter A, Hanson A, Zhong G, Hatta M, Xu R, Yu W, Kawaoka Y, de Haan CA, Wilson IA, Paulson JC. Hemagglutinin receptor specificity and structural analyses of respiratory droplet-transmissible H5N1 viruses.. J Virol 2014 Jan;88(1):768-73.
    doi: 10.1128/JVI.02690-13pmc: PMC3911709pubmed: 24173215google scholar: lookup
  5. de Vries RP, de Vries E, Moore KS, Rigter A, Rottier PJ, de Haan CA. Only two residues are responsible for the dramatic difference in receptor binding between swine and new pandemic H1 hemagglutinin.. J Biol Chem 2011 Feb 18;286(7):5868-75.
    doi: 10.1074/jbc.M110.193557pmc: PMC3037699pubmed: 21173148google scholar: lookup
  6. de Vries RP, Tzarum N, Peng W, Thompson AJ, Ambepitiya Wickramasinghe IN, de la Pena ATT, van Breemen MJ, Bouwman KM, Zhu X, McBride R, Yu W, Sanders RW, Verheije MH, Wilson IA, Paulson JC. A single mutation in Taiwanese H6N1 influenza hemagglutinin switches binding to human-type receptors.. EMBO Mol Med 2017 Sep;9(9):1314-1325.
    doi: 10.15252/emmm.201707726pmc: PMC5582370pubmed: 28694323google scholar: lookup
  7. Peri S, Kulkarni A, Feyertag F, Berninsone PM, Alvarez-Ponce D. Phylogenetic Distribution of CMP-Neu5Ac Hydroxylase (CMAH), the Enzyme Synthetizing the Proinflammatory Human Xenoantigen Neu5Gc.. Genome Biol Evol 2018 Jan 1;10(1):207-219.
    doi: 10.1093/gbe/evx251pmc: PMC5767959pubmed: 29206915google scholar: lookup
  8. Schauer R, Srinivasan GV, Coddeville B, Zanetta JP, Guérardel Y. Low incidence of N-glycolylneuraminic acid in birds and reptiles and its absence in the platypus.. Carbohydr Res 2009 Aug 17;344(12):1494-500.
    doi: 10.1016/j.carres.2009.05.020pubmed: 19541293google scholar: lookup
  9. Ng PS, Böhm R, Hartley-Tassell LE, Steen JA, Wang H, Lukowski SW, Hawthorne PL, Trezise AE, Coloe PJ, Grimmond SM, Haselhorst T, von Itzstein M, Paton AW, Paton JC, Jennings MP. Ferrets exclusively synthesize Neu5Ac and express naturally humanized influenza A virus receptors.. Nat Commun 2014 Dec 17;5:5750.
    doi: 10.1038/ncomms6750pmc: PMC4351649pubmed: 25517696google scholar: lookup
  10. Yasue S, Handa S, Miyagawa S, Inoue J, Hasegawa A, Yamakawa T. Difference in form of sialic acid in red blood cell glycolipids of different breeds of dogs.. J Biochem 1978 Apr;83(4):1101-7.
    doi: 10.1093/oxfordjournals.jbchem.a131999pubmed: 659384google scholar: lookup
  11. Spruit CM, Nemanichvili N, Okamatsu M, Takematsu H, Boons GJ, de Vries RP. N-Glycolylneuraminic Acid in Animal Models for Human Influenza A Virus.. Viruses 2021 May 1;13(5).
    doi: 10.3390/v13050815pmc: PMC8147317pubmed: 34062844google scholar: lookup
  12. Suzuki Y, Ito T, Suzuki T, Holland RE Jr, Chambers TM, Kiso M, Ishida H, Kawaoka Y. Sialic acid species as a determinant of the host range of influenza A viruses.. J Virol 2000 Dec;74(24):11825-31.
    doi: 10.1128/jvi.74.24.11825-11831.2000pmc: PMC112465pubmed: 11090182google scholar: lookup
  13. Suzuki T, Horiike G, Yamazaki Y, Kawabe K, Masuda H, Miyamoto D, Matsuda M, Nishimura SI, Yamagata T, Ito T, Kida H, Kawaoka Y, Suzuki Y. Swine influenza virus strains recognize sialylsugar chains containing the molecular species of sialic acid predominantly present in the swine tracheal epithelium.. FEBS Lett 1997 Mar 10;404(2-3):192-6.
    doi: 10.1016/s0014-5793(97)00127-0pubmed: 9119062google scholar: lookup
  14. Suzuki Y, Matsunaga M, Matsumoto M. N-Acetylneuraminyllactosylceramide, GM3-NeuAc, a new influenza A virus receptor which mediates the adsorption-fusion process of viral infection. Binding specificity of influenza virus A/Aichi/2/68 (H3N2) to membrane-associated GM3 with different molecular species of sialic acid.. J Biol Chem 1985 Feb 10;260(3):1362-5.
    pubmed: 3838173
  15. Barnard KN, Alford-Lawrence BK, Buchholz DW, Wasik BR, LaClair JR, Yu H, Honce R, Ruhl S, Pajic P, Daugherity EK, Chen X, Schultz-Cherry SL, Aguilar HC, Varki A, Parrish CR. Modified Sialic Acids on Mucus and Erythrocytes Inhibit Influenza A Virus Hemagglutinin and Neuraminidase Functions.. J Virol 2020 Apr 16;94(9).
    doi: 10.1128/JVI.01567-19pmc: PMC7163148pubmed: 32051275google scholar: lookup
  16. Varki A. Loss of N-glycolylneuraminic acid in humans: Mechanisms, consequences, and implications for hominid evolution.. Am J Phys Anthropol 2001;Suppl 33(Suppl):54-69.
    doi: 10.1002/ajpa.10018.abspmc: PMC7159735pubmed: 11786991google scholar: lookup
  17. Broszeit F, Tzarum N, Zhu X, Nemanichvili N, Eggink D, Leenders T, Li Z, Liu L, Wolfert MA, Papanikolaou A, Martínez-Romero C, Gagarinov IA, Yu W, García-Sastre A, Wennekes T, Okamatsu M, Verheije MH, Wilson IA, Boons GJ, de Vries RP. N-Glycolylneuraminic Acid as a Receptor for Influenza A Viruses.. Cell Rep 2019 Jun 11;27(11):3284-3294.e6.
    doi: 10.1016/j.celrep.2019.05.048pmc: PMC6750725pubmed: 31189111google scholar: lookup
  18. Gambaryan AS, Matrosovich TY, Philipp J, Munster VJ, Fouchier RA, Cattoli G, Capua I, Krauss SL, Webster RG, Banks J, Bovin NV, Klenk HD, Matrosovich MN. Receptor-binding profiles of H7 subtype influenza viruses in different host species.. J Virol 2012 Apr;86(8):4370-9.
    doi: 10.1128/JVI.06959-11pmc: PMC3318648pubmed: 22345462google scholar: lookup
  19. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses.. Microbiol Rev 1992 Mar;56(1):152-79.
    doi: 10.1128/mr.56.1.152-179.1992pmc: PMC372859pubmed: 1579108google scholar: lookup
  20. Webster RG. Are equine 1 influenza viruses still present in horses?. Equine Vet J 1993 Nov;25(6):537-8.
    doi: 10.1111/j.2042-3306.1993.tb03009.xpubmed: 8276003google scholar: lookup
  21. Liu S, Ji K, Chen J, Tai D, Jiang W, Hou G, Chen J, Li J, Huang B. Panorama phylogenetic diversity and distribution of Type A influenza virus.. PLoS One 2009;4(3):e5022.
    doi: 10.1371/journal.pone.0005022pmc: PMC2658884pubmed: 19325912google scholar: lookup
  22. Tzarum N, McBride R, Nycholat CM, Peng W, Paulson JC, Wilson IA. Unique Structural Features of Influenza Virus H15 Hemagglutinin.. J Virol 2017 Jun 15;91(12).
    doi: 10.1128/JVI.00046-17pmc: PMC5446636pubmed: 28404848google scholar: lookup
  23. Russell RJ, Gamblin SJ, Haire LF, Stevens DJ, Xiao B, Ha Y, Skehel JJ. H1 and H7 influenza haemagglutinin structures extend a structural classification of haemagglutinin subtypes.. Virology 2004 Aug 1;325(2):287-96.
    doi: 10.1016/j.virol.2004.04.040pubmed: 15246268google scholar: lookup
  24. de Vries RP, Peng W, Grant OC, Thompson AJ, Zhu X, Bouwman KM, de la Pena ATT, van Breemen MJ, Ambepitiya Wickramasinghe IN, de Haan CAM, Yu W, McBride R, Sanders RW, Woods RJ, Verheije MH, Wilson IA, Paulson JC. Three mutations switch H7N9 influenza to human-type receptor specificity.. PLoS Pathog 2017 Jun;13(6):e1006390.
    doi: 10.1371/journal.ppat.1006390pmc: PMC5472306pubmed: 28617868google scholar: lookup
  25. Tzarum N, de Vries RP, Peng W, Thompson AJ, Bouwman KM, McBride R, Yu W, Zhu X, Verheije MH, Paulson JC, Wilson IA. The 150-Loop Restricts the Host Specificity of Human H10N8 Influenza Virus.. Cell Rep 2017 Apr 11;19(2):235-245.
    doi: 10.1016/j.celrep.2017.03.054pmc: PMC5452617pubmed: 28402848google scholar: lookup
  26. Peng W, Bouwman KM, McBride R, Grant OC, Woods RJ, Verheije MH, Paulson JC, de Vries RP. Enhanced Human-Type Receptor Binding by Ferret-Transmissible H5N1 with a K193T Mutation.. J Virol 2018 May 15;92(10).
    doi: 10.1128/JVI.02016-17pmc: PMC5923085pubmed: 29491160google scholar: lookup
  27. Medeiros R, Naffakh N, Manuguerra JC, van der Werf S. Binding of the hemagglutinin from human or equine influenza H3 viruses to the receptor is altered by substitutions at residue 193.. Arch Virol 2004 Aug;149(8):1663-71.
    doi: 10.1007/s00705-003-0287-2pubmed: 15290389google scholar: lookup
  28. Watanabe T, Kiso M, Fukuyama S, Nakajima N, Imai M, Yamada S, Murakami S, Yamayoshi S, Iwatsuki-Horimoto K, Sakoda Y, Takashita E, McBride R, Noda T, Hatta M, Imai H, Zhao D, Kishida N, Shirakura M, de Vries RP, Shichinohe S, Okamatsu M, Tamura T, Tomita Y, Fujimoto N, Goto K, Katsura H, Kawakami E, Ishikawa I, Watanabe S, Ito M, Sakai-Tagawa Y, Sugita Y, Uraki R, Yamaji R, Eisfeld AJ, Zhong G, Fan S, Ping J, Maher EA, Hanson A, Uchida Y, Saito T, Ozawa M, Neumann G, Kida H, Odagiri T, Paulson JC, Hasegawa H, Tashiro M, Kawaoka Y. Characterization of H7N9 influenza A viruses isolated from humans.. Nature 2013 Sep 26;501(7468):551-5.
    doi: 10.1038/nature12392pmc: PMC3891892pubmed: 23842494google scholar: lookup
  29. Masuda H, Suzuki T, Sugiyama Y, Horiike G, Murakami K, Miyamoto D, Jwa Hidari KI, Ito T, Kida H, Kiso M, Fukunaga K, Ohuchi M, Toyoda T, Ishihama A, Kawaoka Y, Suzuki Y. Substitution of amino acid residue in influenza A virus hemagglutinin affects recognition of sialyl-oligosaccharides containing N-glycolylneuraminic acid.. FEBS Lett 1999 Dec 24;464(1-2):71-4.
    doi: 10.1016/s0014-5793(99)01575-6pubmed: 10611486google scholar: lookup
  30. Wang M, Tscherne DM, McCullough C, Caffrey M, García-Sastre A, Rong L. Residue Y161 of influenza virus hemagglutinin is involved in viral recognition of sialylated complexes from different hosts.. J Virol 2012 Apr;86(8):4455-62.
    doi: 10.1128/JVI.07187-11pmc: PMC3318606pubmed: 22301136google scholar: lookup
  31. Wen F, Li L, Zhao N, Chiang MJ, Xie H, Cooley J, Webby R, Wang PG, Wan XF. A Y161F Hemagglutinin Substitution Increases Thermostability and Improves Yields of 2009 H1N1 Influenza A Virus in Cells.. J Virol 2018 Jan 15;92(2).
    doi: 10.1128/JVI.01621-17pmc: PMC5752953pubmed: 29118117google scholar: lookup
  32. Yang H, Carney PJ, Chang JC, Stevens J. Molecular characterization and three-dimensional structures of avian H8, H11, H14, H15 and swine H4 influenza virus hemagglutinins.. Heliyon 2020 Jun;6(6):e04068.
    doi: 10.1016/j.heliyon.2020.e04068pmc: PMC7281811pubmed: 32529072google scholar: lookup
  33. Jia N, Byrd-Leotis L, Matsumoto Y, Gao C, Wein AN, Lobby JL, Kohlmeier JE, Steinhauer DA, Cummings RD. The Human Lung Glycome Reveals Novel Glycan Ligands for Influenza A Virus.. Sci Rep 2020 Mar 24;10(1):5320.
    doi: 10.1038/s41598-020-62074-zpmc: PMC7093477pubmed: 32210305google scholar: lookup
  34. Sriwilaijaroen N, Nakakita SI, Kondo S, Yagi H, Kato K, Murata T, Hiramatsu H, Kawahara T, Watanabe Y, Kanai Y, Ono T, Hirabayashi J, Matsumoto K, Suzuki Y. N-glycan structures of human alveoli provide insight into influenza A virus infection and pathogenesis.. FEBS J 2018 May;285(9):1611-1634.
    doi: 10.1111/febs.14431pubmed: 29542865google scholar: lookup
  35. Byrd-Leotis L, Liu R, Bradley KC, Lasanajak Y, Cummings SF, Song X, Heimburg-Molinaro J, Galloway SE, Culhane MR, Smith DF, Steinhauer DA, Cummings RD. Shotgun glycomics of pig lung identifies natural endogenous receptors for influenza viruses.. Proc Natl Acad Sci U S A 2014 Jun 3;111(22):E2241-50.
    doi: 10.1073/pnas.1323162111pmc: PMC4050609pubmed: 24843157google scholar: lookup
  36. Hiono T, Okamatsu M, Nishihara S, Takase-Yoden S, Sakoda Y, Kida H. A chicken influenza virus recognizes fucosylated α2,3 sialoglycan receptors on the epithelial cells lining upper respiratory tracts of chickens.. Virology 2014 May;456-457:131-8.
    doi: 10.1016/j.virol.2014.03.004pubmed: 24889232google scholar: lookup
  37. Hua S, Jeong HN, Dimapasoc LM, Kang I, Han C, Choi JS, Lebrilla CB, An HJ. Isomer-specific LC/MS and LC/MS/MS profiling of the mouse serum N-glycome revealing a number of novel sialylated N-glycans.. Anal Chem 2013 May 7;85(9):4636-43.
    doi: 10.1021/ac400195hpmc: PMC5636693pubmed: 23534819google scholar: lookup
  38. Aich U, Beckley N, Shriver Z, Raman R, Viswanathan K, Hobbie S, Sasisekharan R. Glycomics-based analysis of chicken red blood cells provides insight into the selectivity of the viral agglutination assay.. FEBS J 2011 May;278(10):1699-712.
    doi: 10.1111/j.1742-4658.2011.08096.xpmc: PMC3740515pubmed: 21410647google scholar: lookup
  39. Gambaryan A, Tuzikov A, Pazynina G, Bovin N, Balish A, Klimov A. Evolution of the receptor binding phenotype of influenza A (H5) viruses.. Virology 2006 Jan 20;344(2):432-8.
    doi: 10.1016/j.virol.2005.08.035pubmed: 16226289google scholar: lookup
  40. Gambaryan AS, Tuzikov AB, Pazynina GV, Desheva JA, Bovin NV, Matrosovich MN, Klimov AI. 6-sulfo sialyl Lewis X is the common receptor determinant recognized by H5, H6, H7 and H9 influenza viruses of terrestrial poultry.. Virol J 2008 Jul 24;5:85.
    doi: 10.1186/1743-422X-5-85pmc: PMC2515299pubmed: 18652681google scholar: lookup
  41. Bateman AC, Karamanska R, Busch MG, Dell A, Olsen CW, Haslam SM. Glycan analysis and influenza A virus infection of primary swine respiratory epithelial cells: the importance of NeuAc{alpha}2-6 glycans.. J Biol Chem 2010 Oct 29;285(44):34016-26.
    doi: 10.1074/jbc.M110.115998pmc: PMC2962501pubmed: 20724471google scholar: lookup
  42. Stevens J, Chen LM, Carney PJ, Garten R, Foust A, Le J, Pokorny BA, Manojkumar R, Silverman J, Devis R, Rhea K, Xu X, Bucher DJ, Paulson JC, Cox NJ, Klimov A, Donis RO. Receptor specificity of influenza A H3N2 viruses isolated in mammalian cells and embryonated chicken eggs.. J Virol 2010 Aug;84(16):8287-99.
    doi: 10.1128/JVI.00058-10pmc: PMC2916524pubmed: 20519409google scholar: lookup
  43. Gambaryan A, Yamnikova S, Lvov D, Tuzikov A, Chinarev A, Pazynina G, Webster R, Matrosovich M, Bovin N. Receptor specificity of influenza viruses from birds and mammals: new data on involvement of the inner fragments of the carbohydrate chain.. Virology 2005 Apr 10;334(2):276-83.
    doi: 10.1016/j.virol.2005.02.003pubmed: 15780877google scholar: lookup
  44. Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, Paulson JC, Wilson IA. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities.. J Mol Biol 2006 Feb 3;355(5):1143-55.
    doi: 10.1016/j.jmb.2005.11.002pubmed: 16343533google scholar: lookup
  45. Hiono T, Okamatsu M, Igarashi M, McBride R, de Vries RP, Peng W, Paulson JC, Sakoda Y, Kida H. Amino acid residues at positions 222 and 227 of the hemagglutinin together with the neuraminidase determine binding of H5 avian influenza viruses to sialyl Lewis X.. Arch Virol 2016 Feb;161(2):307-16.
    doi: 10.1007/s00705-015-2660-3pmc: PMC5030063pubmed: 26542967google scholar: lookup
  46. Wen F, Blackmon S, Olivier AK, Li L, Guan M, Sun H, Wang PG, Wan XF. Mutation W222L at the Receptor Binding Site of Hemagglutinin Could Facilitate Viral Adaption from Equine Influenza A(H3N8) Virus to Dogs.. J Virol 2018 Sep 15;92(18).
    doi: 10.1128/JVI.01115-18pmc: PMC6146684pubmed: 29997206google scholar: lookup
  47. Murcia PR, Wood JL, Holmes EC. Genome-scale evolution and phylodynamics of equine H3N8 influenza A virus.. J Virol 2011 Jun;85(11):5312-22.
    doi: 10.1128/JVI.02619-10pmc: PMC3094979pubmed: 21430049google scholar: lookup
  48. Collins PJ, Vachieri SG, Haire LF, Ogrodowicz RW, Martin SR, Walker PA, Xiong X, Gamblin SJ, Skehel JJ. Recent evolution of equine influenza and the origin of canine influenza.. Proc Natl Acad Sci U S A 2014 Jul 29;111(30):11175-80.
    doi: 10.1073/pnas.1406606111pmc: PMC4121831pubmed: 25024224google scholar: lookup
  49. Worobey M, Han GZ, Rambaut A. A synchronized global sweep of the internal genes of modern avian influenza virus.. Nature 2014 Apr 10;508(7495):254-7.
    doi: 10.1038/nature13016pmc: PMC4098125pubmed: 24531761google scholar: lookup
  50. Stevens J, Blixt O, Paulson JC, Wilson IA. Glycan microarray technologies: tools to survey host specificity of influenza viruses.. Nat Rev Microbiol 2006 Nov;4(11):857-64.
    doi: 10.1038/nrmicro1530pmc: PMC7097745pubmed: 17013397google scholar: lookup
  51. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode.. Methods Enzymol 1997;276:307-26.
    doi: 10.1016/S0076-6879(97)76066-Xpubmed: 27754618google scholar: lookup
  52. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, Read RJ. Likelihood-enhanced fast translation functions.. Acta Crystallogr D Biol Crystallogr 2005 Apr;61(Pt 4):458-64.
    doi: 10.1107/S0907444905001617pubmed: 15805601google scholar: lookup
  53. Murshudov GN, Skubák P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA. REFMAC5 for the refinement of macromolecular crystal structures.. Acta Crystallogr D Biol Crystallogr 2011 Apr;67(Pt 4):355-67.
    doi: 10.1107/S0907444911001314pmc: PMC3069751pubmed: 21460454google scholar: lookup
  54. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics.. Acta Crystallogr D Biol Crystallogr 2004 Dec;60(Pt 12 Pt 1):2126-32.
    doi: 10.1107/S0907444904019158pubmed: 15572765google scholar: lookup
  55. de Vries RP, de Vries E, Bosch BJ, de Groot RJ, Rottier PJ, de Haan CA. The influenza A virus hemagglutinin glycosylation state affects receptor-binding specificity.. Virology 2010 Jul 20;403(1):17-25.
    doi: 10.1016/j.virol.2010.03.047pubmed: 20441997google scholar: lookup
  56. Zeng Q, Langereis MA, van Vliet AL, Huizinga EG, de Groot RJ. Structure of coronavirus hemagglutinin-esterase offers insight into corona and influenza virus evolution.. Proc Natl Acad Sci U S A 2008 Jul 1;105(26):9065-9.
    doi: 10.1073/pnas.0800502105pmc: PMC2449365pubmed: 18550812google scholar: lookup
  57. Nemanichvili N, Tomris I, Turner HL, McBride R, Grant OC, van der Woude R, Aldosari MH, Pieters RJ, Woods RJ, Paulson JC, Boons GJ, Ward AB, Verheije MH, de Vries RP. Fluorescent Trimeric Hemagglutinins Reveal Multivalent Receptor Binding Properties.. J Mol Biol 2019 Feb 15;431(4):842-856.
    doi: 10.1016/j.jmb.2018.12.014pmc: PMC6397626pubmed: 30597163google scholar: lookup
  58. Shaner NC, Lin MZ, McKeown MR, Steinbach PA, Hazelwood KL, Davidson MW, Tsien RY. Improving the photostability of bright monomeric orange and red fluorescent proteins.. Nat Methods 2008 Jun;5(6):545-51.
    doi: 10.1038/nmeth.1209pmc: PMC2853173pubmed: 18454154google scholar: lookup
  59. Bouwman KM, Parsons LM, Berends AJ, de Vries RP, Cipollo JF, Verheije MH. Three Amino Acid Changes in Avian Coronavirus Spike Protein Allow Binding to Kidney Tissue.. J Virol 2020 Jan 6;94(2).
    doi: 10.1128/JVI.01363-19pmc: PMC6955270pubmed: 31694947google scholar: lookup
  60. Wickramasinghe IN, de Vries RP, Gröne A, de Haan CA, Verheije MH. Binding of avian coronavirus spike proteins to host factors reflects virus tropism and pathogenicity.. J Virol 2011 Sep;85(17):8903-12.
    doi: 10.1128/JVI.05112-11pmc: PMC3165808pubmed: 21697468google scholar: lookup
  61. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era.. Mol Biol Evol 2020 May 1;37(5):1530-1534.
    doi: 10.1093/molbev/msaa015pmc: PMC7182206pubmed: 32011700google scholar: lookup
  62. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates.. Nat Methods 2017 Jun;14(6):587-589.
    doi: 10.1038/nmeth.4285pmc: PMC5453245pubmed: 28481363google scholar: lookup
  63. Sagulenko P, Puller V, Neher RA. TreeTime: Maximum-likelihood phylodynamic analysis.. Virus Evol 2018 Jan;4(1):vex042.
    doi: 10.1093/ve/vex042pmc: PMC5758920pubmed: 29340210google scholar: lookup
  64. Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. MolProbity: all-atom structure validation for macromolecular crystallography.. Acta Crystallogr D Biol Crystallogr 2010 Jan;66(Pt 1):12-21.
    doi: 10.1107/S0907444909042073pmc: PMC2803126pubmed: 20057044google scholar: lookup

Citations

This article has been cited 5 times.
  1. Abdelwhab EM, Mettenleiter TC. Zoonotic Animal Influenza Virus and Potential Mixing Vessel Hosts.. Viruses 2023 Apr 16;15(4).
    doi: 10.3390/v15040980pubmed: 37112960google scholar: lookup
  2. Tomris I, Unione L, Nguyen L, Zaree P, Bouwman KM, Liu L, Li Z, Fok JA, Ríos Carrasco M, van der Woude R, Kimpel ALM, Linthorst MW, Kilavuzoglu SE, Verpalen ECJM, Caniels TG, Sanders RW, Heesters BA, Pieters RJ, Jiménez-Barbero J, Klassen JS, Boons GJ, de Vries RP. SARS-CoV-2 Spike N-Terminal Domain Engages 9-O-Acetylated α2-8-Linked Sialic Acids.. ACS Chem Biol 2023 May 19;18(5):1180-1191.
    doi: 10.1021/acschembio.3c00066pubmed: 37104622google scholar: lookup
  3. Zhao C, Pu J. Influence of Host Sialic Acid Receptors Structure on the Host Specificity of Influenza Viruses.. Viruses 2022 Sep 28;14(10).
    doi: 10.3390/v14102141pubmed: 36298694google scholar: lookup
  4. Youk S, Leyson C, Killian ML, Torchetti MK, Lee DH, Suarez DL, Pantin-Jackwood MJ. Evolution of the North American Lineage H7 Avian Influenza Viruses in Association with H7 Virus's Introduction to Poultry.. J Virol 2022 Jul 27;96(14):e0027822.
    doi: 10.1128/jvi.00278-22pubmed: 35862690google scholar: lookup
  5. Nemanichvili N, Spruit CM, Berends AJ, Gröne A, Rijks JM, Verheije MH, de Vries RP. Wild and domestic animals variably display Neu5Ac and Neu5Gc sialic acids.. Glycobiology 2022 Aug 18;32(9):791-802.
    doi: 10.1093/glycob/cwac033pubmed: 35648131google scholar: lookup
Subscribe to our newsletter
Join 99,359 horse owners like you who receive our email updates on horse health and nutrition.