Symmetry-related clustering of positive charges is a common mechanism for heparan sulfate binding in enteroviruses

Journal of Virology

Volumn 86, Issue 20, 2012, Pages 11163-11170

  McLeish, Nigel J ^a,c   Williams, Çiǧdem H ^a   Kaloudas, Dimitrios ^a   Roivainen, Merja M ^b   Stanway, Glyn ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^c UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; HEPARIN; PROTEIN VP1; PROTEOHEPARAN SULFATE; THREONINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING KINETICS; CONTROLLED STUDY; COXSACKIE VIRUS A; COXSACKIE VIRUS A9; ENTEROVIRUS; ENTEROVIRUS INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; SYMMETRY RELATED CLUSTERING; VIRUS ATTACHMENT; VIRUS MORPHOLOGY; VIRUS STRAIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANTIGENS, NEOPLASM; BINDING SITES; CAPSID PROTEINS; CELL LINE; CERCOPITHECUS AETHIOPS; ENTEROVIRUS B, HUMAN; ENTEROVIRUS INFECTIONS; HEPARAN SULFATE PROTEOGLYCANS; INTEGRINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RECEPTORS, VIRUS; SEQUENCE ANALYSIS, RNA; STATIC ELECTRICITY; VIRAL PROTEINS;

COXSACKIEVIRUS; ENTEROVIRUS; HUMAN ENTEROVIRUS B; MIRIDAE; PICORNAVIRIDAE;

EID: 84869022974     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00640-12     Document Type: Article

References (50)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Bernard KA, Klimstra WB, Johnston RE. 2000. Mutations in the E2 glycoprotein of Venezuelan equine encephalitis virus confer heparan sulfate interaction, low morbidity, and rapid clearance from blood of mice. Virology 276:93-103.
3. Byrnes AP, Griffin DE. 2000. Large-plaque mutants of Sindbis virus show reduced binding to heparan sulfate, heightened viremia, and slower clearance from the circulation. J. Virol. 74:644-651.
4. Cardin AD, Weintraub HJ. 1989. Molecular modeling of proteinglycosaminoglycan interactions. Arteriosclerosis 9:21-32.
5. Chang KH, Auvinen P, Hyypiä T, Stanway G. 1989. The nucleotide sequence of coxsackievirus A9; implications for receptor binding and enterovirus classification. J. Gen. Virol. 70:3269-3280.
6. Chang KH, Day C, Walker J, Hyypiä T, Stanway G. 1992. The nucleotide sequences of wild-type coxsackievirus A9 strains imply that an RGD motif in VP1 is functionally significant. J. Gen. Virol. 73:621-626.
7. Chung SK, et al. 2005. Internalization and trafficking mechanisms of coxsackievirus B3 in HeLa cells. Virology 333:31-40.
8. Dasgupta J, et al. 2011. Structural basis of oligosaccharide receptor recognition by human papillomavirus. J. Biol. Chem. 286:2617-2624.
9. Eisenhut M, et al. 2000. Fatal coxsackie A9 virus infection during an outbreak in a neonatal unit. J. Infect. 40:297-298.
10. Fry EE, et al. 1999. The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex. EMBO J. 18:543-554.
11. Fry EE, et al. 2005. Structure of foot-and-mouth disease virus serotype A10 61 alone and complexed with oligosaccharide receptor: receptor conservation in the face of antigenic variation. J. Gen. Virol. 86:1909-1920.
12. Goodfellow IG, Sioofy AB, Powell RM, Evans DJ. 2001. Echoviruses bind heparan sulfate at the cell surface. J. Virol. 75:4918-4921.
13. Grist NR, Reid D. 1988. General pathogenicity and epidemiology, p 221-239. In Berdinelli M, Friedman H (ed), Coxsackieviruses: a general update. Plenum Press, New York, NY.
14. Heikkilä O, Susi P, Stanway G, Hyypiä T. 2009. Integrin alphaVbeta6 is a high-affinity receptor for coxsackievirus A9. J. Gen. Virol. 90:197-204.
15. Heikkilä O, et al. 2010. Internalization of coxsackievirus A9 is mediated by _2-microglobulin, dynamin, and Arf6 but not by caveolin-1 or clathrin. J. Virol. 84:3666-3681.
16. Hendry E, et al. 1999. The crystal structure of coxsackievirus A9: new insights into the uncoating mechanisms of enteroviruses. Structure 7:1527-1538.
17. Hughes PJ, Horsnell C, Hyypiä T, Stanway G. 1995. The coxsackievirus A9 RGD motif is not essential for virus viability. J. Virol. 69:8035-8040.
18. Hulst MM, van Gennip HG, Moormann RJ. 2000. Passage of classical swine fever virus in cultured swine kidney cells selects virus variants that bind to heparan sulfate due to a single amino acid change in envelope protein E(rns). J. Virol. 74:9553-9561.
19. Israelsson S, et al. 2010. Studies of echovirus 5 interactions with the cell surface: heparan sulfate mediates attachment to the host cell. Virus Res. 151:170-176.
20. Jackson T, et al. 2004. Integrin _v_8 functions as a receptor for foot-andmouth disease virus: role of the _-chain cytodomain in integrin-mediated infection. J. Virol. 78:4533-4540.
21. Jackson T, et al. 1996. Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate. J. Virol. 70:5282-5287.
22. Jackson T, Mould AP, Sheppard D, King AM. 2002. Integrin _v_1 is a receptor for foot-and-mouth disease virus. J. Virol. 76:935-941.
23. Jackson T, et al. 1997. Arginine-glycine-aspartic acid-specific binding by foot-and-mouth disease viruses to the purified integrin alpha (v) beta3 in vitro. J. Virol. 71:8357-8361.
24. Jackson T, Sheppard D, Denyer M, Blakemore W, King AM. 2000. The epithelial integrin _v_6 is a receptor for foot-and-mouth disease virus. J. Virol. 74:4949-4956.
25. Jinno-Oue A, Oue M, Ruscetti SK. 2001. A unique heparin-binding domain in the envelope protein of the neuropathogenic PVC-211 murine leukemia virus may contribute to its brain capillary endothelial cell tropism. J. Virol. 75:12439-12445.
26. Johns HL, Berryman S, Monaghan P, Belsham GJ, Jackson T. 2009. A dominant-negative mutant of rab5 inhibits infection of cells by foot-andmouth disease virus: implications for virus entry. J. Virol. 83:6247-6256.
27. Kern A, et al. 2003. Identification of a heparin-binding motif on adenoassociated virus type 2 capsids. J. Virol. 77:11072-11081.
28. Khan AG, Pichler J, Rosemann A, Blaas D. 2007. Human rhinovirus type 54 infection via heparan sulfate is less efficient and strictly dependent on low endosomal pH. J. Virol. 81:4625-4632.
29. Khan AG, et al. 2011. Entry of a heparan sulphate-binding HRV8 variant strictly depends on dynamin but not on clathrin, caveolin, and flotillin. Virology 412:55-67.
30. Knowles NJ, et al. 2011. Picornaviridae, p 855-880. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (ed), Virus taxonomy: classification and nomenclature of viruses: ninth report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego, CA.
31. Kureishy N, Faruque D, Porter CD. 2006. Primary attachment of murine leukaemia virus vector mediated by particle-associated heparan sulfate proteoglycan. Biochem. J. 400:421-430.
32. Lopata MA, Cleveland DW, Sollner-Webb B. 1984. High level transient expression of a chloramphenicol acetyl transferase gene by DEAE-dextran mediated DNA transfection coupled with a dimethyl sulfoxide or glycerol shock treatment. Nucleic Acids Res. 12:5707-5717.
33. Maree FF, Blignaut B, de Beer TA, Visser N, Rieder EA. 2010. Mapping of amino acid residues responsible for adhesion of cell culture-adapted foot-and-mouth disease SAT type viruses. Virus Res. 153:82-91.
34. Mulloy B, Forster MJ. 2000. Conformation and dynamics of heparin and heparan sulfate. Glycobiology 10:1147-1156.
35. Pearson WR, Lipman DJ. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. U. S. A. 85:2444-2448.
36. Pulli T, Koivunen E, Hyypiä T. 1997. Cell-surface interactions of echovirus. J. Biol. Chem. 272:21176-21180.
37. Reddi HV, Lipton HL. 2002. Heparan sulfate mediates infection of highneurovirulence Theiler's viruses. J. Virol. 76:8400-8407.
38. Roivainen M, et al. 1991. RGD-dependent entry of coxsackievirus A9 into host cells and its bypass after cleavage of VP1 protein by intestinal proteases. J. Virol. 65:4735-4740.
39. Sayle RA, Milner-White EJ. 1995. RASMOL: biomolecular graphics for all. Trends Biochem. Sci. 20:374.
40. Seitsonen J, et al. 2010. Interaction of alphaVbeta3 and alphaVbeta6 integrins with human parechovirus 1. J. Virol. 84:8509-8519.
41. Shah AH, Lipton HL. 2002. Low-neurovirulence Theiler's viruses use sialic acid moieties on N-linked oligosaccharide structures for attachment. Virology 304:443-450.
42. Smit JM, et al. 2002. Adaptation of alphaviruses to heparan sulfate: interaction of Sindbis and Semliki Forest viruses with liposomes containing lipid-conjugated heparin. J. Virol. 76:10128-10137.
43. Takemoto KK, Liebhaber H. 1961. Virus-polysaccharide interactions. I. An agar polysaccharide determining plaque morphology of EMC virus. Virology 14:456-462.
44. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
45. Triantafilou K, Fradelizi D, Wilson K, Triantafilou M. 2002. GRP78, a coreceptor for coxsackievirus A9, interacts with major histocompatibility complex class I molecules which mediate virus internalization. J. Virol. 76:633-643.
46. Tuve S, et al. 2008. Role of cellular heparan sulfate proteoglycans in infection of human adenovirus serotype 3 and 35. PLoS Pathog. 4:e1000189. doi:10.1371/journal.ppat.1000189.
47. Vlasak M, Goesler I, Blaas D. 2005. Human rhinovirus type 89 variants use heparan sulfate proteoglycan for cell attachment. J. Virol. 79:5963-5970.
48. Williams ÇH, et al. 2004. Integrin _v_6 is an RGD-dependent receptor for coxsackievirus A9. J. Virol. 78:6967-6973.
49. Zautner AE, Jahn B, Hammerschmidt E, Wutzler P, Schmidtke M. 2006. N- and 6-O-sulfated heparan sulfates mediate internalization of coxsackievirus B3 variant PD into CHO-K1 cells. J. Virol. 80:6629-6636.
50. Zhang Z, et al. 2010. Heparin sulphate D-glucosaminyl 3-O-sulfotransferase 3B1 plays a role in HBV replication. Virology 406:280-285.