Coxsackievirus A16 utilizes cell surface heparan sulfate glycosaminoglycans as its attachment receptor

References

• Mao Q, Wang Y, Yao Xet al.Coxsackievirus A16: epidemiology, diagnosis, and vaccine. Hum Vaccin Immunother 2014;10: 360–367.
   PubMed Web of Science ®Google Scholar
• Wang CY, Lu FL, Wu MHet al.Fatal coxsackievirus A16 infection. Pediatr Infect Dis J 2004;23: 275–276.
   PubMed Web of Science ®Google Scholar
• Wright Jr HT, Landing BH, Lennette EHet al.Fatal infection in an infant associated with Coxsackie virus group A, type 16. N Engl J Med 1963;268: 1041–1044.
   PubMed Web of Science ®Google Scholar
• Goldberg MF, McAdams AJ.Myocarditis possibly due to Coxsackie group A, type 16, virus. J Pediatr 1963;62: 762–765.
   PubMed Web of Science ®Google Scholar
• Xu W, Liu CF, Yan Let al.Distribution of enteroviruses in hospitalized children with hand, foot and mouth disease and relationship between pathogens and nervous system complications. Virol J 2012;9: 8.
   PubMed Web of Science ®Google Scholar
• Liu Q, Yan K, Feng Yet al.A virus-like particle vaccine for coxsackievirus A16 potently elicits neutralizing antibodies that protect mice against lethal challenge. Vaccine 2012;30: 6642–6648.
   PubMed Web of Science ®Google Scholar
• Cai Y, Liu Q, Huang Xet al.Active immunization with a Coxsackievirus A16 experimental inactivated vaccine induces neutralizing antibodies and protects mice against lethal infection. Vaccine 2013;31: 2215–2221.
   PubMed Web of Science ®Google Scholar
• Zhao H, Li HY, Han JFet al.Virus-like particles produced in Saccharomyces cerevisiae elicit protective immunity against Coxsackievirus A16 in mice. Appl Microbiol Biotechnol 2013;97: 10445–10452.
   PubMed Web of Science ®Google Scholar
• Li J, Chang J, Liu Xet al.Protection from lethal challenge in a neonatal mouse model by circulating recombinant form coxsackievirus A16 vaccine candidates. J Gen Virol 2014;95 (Pt 5): 1083–1093.
   PubMed Web of Science ®Google Scholar
• Yang E, Cheng C, Zhang Yet al.Comparative study of the immunogenicity in mice and monkeys of an inactivated CA16 vaccine made from a human diploid cell line. Hum Vaccin Immunother 2014;10: 1266–1273.
   PubMed Web of Science ®Google Scholar
• Poyry T, Hyypia T, Horsnell Cet al.Molecular analysis of coxsackievirus A16 reveals a new genetic group of enteroviruses. Virology 1994;202: 982–987.
   PubMed Web of Science ®Google Scholar
• Lauber C, Gorbalenya AE.Toward genetics-based virus taxonomy: comparative analysis of a genetics-based classification and the taxonomy of picornaviruses. J Virol 2012;86: 3905–3915.
   PubMed Web of Science ®Google Scholar
• Liu F, Liu Q, Cai Yet al.Construction and characterization of an infectious clone of coxsackievirus A16. Virol J 2011;8: 534.
   PubMed Web of Science ®Google Scholar
• Ren J, Wang X, Zhu Let al.Structures of coxsackievirus A16 capsids with native antigenicity: implications for particle expansion, receptor binding, and immunogenicity. J Virol 2015;89: 10500–10511.
   PubMed Web of Science ®Google Scholar
• Ren JS, Wang XX, Hu ZYet al.Picornavirus uncoating intermediate captured in atomic detail. Nat Commun 2013;4: 1929.
   PubMed Web of Science ®Google Scholar
• Yamayoshi S, Yamashita Y, Li Jet al.Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat Med 2009;15: 798–801.
   PubMed Web of Science ®Google Scholar
• Yamayoshi S, Iizuka S, Yamashita Tet al.Human SCARB2-dependent infection by coxsackievirus A7, A14, and A16 and enterovirus 71. J Virol 2012;86: 5686–5696.
   PubMed Web of Science ®Google Scholar
• Nishimura Y, Shimojima M, Tano Yet al.Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat Med 2009;15: 794–797.
   PubMed Web of Science ®Google Scholar
• Goodfellow IG, Sioofy AB, Powell RMet al.Echoviruses bind heparan sulfate at the cell surface. J Virol 2001;75: 4918–4921.
   PubMed Web of Science ®Google Scholar
• Khan AG, Pichler J, Rosemann Aet al.Human rhinovirus type 54 infection via heparan sulfate is less efficient and strictly dependent on low endosomal pH. J Virol 2007;81: 4625–4632.
   PubMed Web of Science ®Google Scholar
• Vlasak M, Goesler I, Blaas D.Human rhinovirus type 89 variants use heparan sulfate proteoglycan for cell attachment. J Virol 2005;79: 5963–5970.
   PubMed Web of Science ®Google Scholar
• Tan CW, Poh CL, Sam ICet al.Enterovirus 71 uses cell surface heparan sulfate glycosaminoglycan as an attachment receptor. J Virol 2013;87: 611–620.
   PubMed Web of Science ®Google Scholar
• Nishimura Y, McLaughlin NP, Pan Jet al.The suramin derivative NF449 interacts with the 5-fold vertex of the enterovirus A71 capsid to prevent virus attachment to PSGL-1 and heparan sulfate. PLoS Pathog 2015;11: e1005184.
   PubMed Web of Science ®Google Scholar
• McLeish NJ, Williams CH, Kaloudas Det al.Symmetry-related clustering of positive charges is a common mechanism for heparan sulfate binding in enteroviruses. J Virol 2012;86: 11163–11170.
   PubMed Web of Science ®Google Scholar
• Zautner AE, Jahn B, Hammerschmidt Eet al.N- and 6-O-sulfated heparan sulfates mediate internalization of coxsackievirus B3 variant PD into CHO-K1 cells. J Virol 2006;80: 6629–6636.
   PubMed Web of Science ®Google Scholar
• Jackson T, Ellard FM, Ghazaleh RAet al.Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate. J Virol 1996;70: 5282–5287.
   PubMed Web of Science ®Google Scholar
• Liu Q, Ku Z, Cai Yet al.Detection, characterization and quantitation of coxsackievirus A16 using polyclonal antibodies against recombinant capsid subunit proteins. J Virol Methods 2011;173: 115–120.
   PubMed Web of Science ®Google Scholar
• Reed LJ, Muench H.A simple method of estimating 50 percent endpoints. Am J Hyg 1938;27: 493–499.
   Google Scholar
• Ye X, Ku Z, Liu Qet al.Chimeric virus-like particle vaccines displaying conserved enterovirus 71 epitopes elicit protective neutralizing antibodies in mice through divergent mechanisms. J Virol 2014;88: 72–81.
   PubMed Web of Science ®Google Scholar
• Ku Z, Ye X, Huang Xet al.Neutralizing antibodies induced by recombinant virus-like particles of enterovirus 71 genotype C4 inhibit infection at pre- and post-attachment steps. PLoS One 2013;8: e57601.
   PubMed Web of Science ®Google Scholar
• Ku Z, Liu Q, Ye Xet al.A virus-like particle based bivalent vaccine confers dual protection against enterovirus 71 and coxsackievirus A16 infections in mice. Vaccine 2014;32: 4296–4303.
   PubMed Web of Science ®Google Scholar
• Guibinga GH, Miyanohara A, Esko JDet al.Cell surface heparan sulfate is a receptor for attachment of envelope protein-free retrovirus-like particles and VSV-G pseudotyped MLV-derived retrovirus vectors to target cells. Mol Ther 2002;5 (5 Pt 1): 538–546.
   PubMed Web of Science ®Google Scholar
• Eskelinen EL, Tanaka Y, Saftig P.At the acidic edge: emerging functions for lysosomal membrane proteins. Trends Cell Biol 2003;13: 137–145.
   PubMed Web of Science ®Google Scholar
• Ku Z, Ye X, Shi Jet al.Single neutralizing monoclonal antibodies targeting the VP1 GH loop of enterovirus 71 inhibit both virus attachment and internalization during viral entry. J Virol 2015;89: 12084–12095.
   PubMed Web of Science ®Google Scholar
• Tan CW, Sam IC, Lee VSet al.VP1 residues around the five-fold axis of enterovirus A71 mediate heparan sulfate interaction. Virology 2017;501: 79–87.
   PubMed Web of Science ®Google Scholar