Structural basis of rotavirus strain preference toward N-acetyl-or N-glycolylneuraminic acid-containing receptors

Journal of Virology

Volumn 86, Issue 24, 2012, Pages 13456-13466

  Yu, Xing ^a   Dang, Vi T ^b   Fleming, Fiona E ^b   von Itzstein, Mark ^a   Coulson, Barbara S ^b   Blanchard, Helen ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBOHYDRATE; N ACETYLNEURAMINIC ACID; N GLYCOLOYLNEURAMINIC ACID; PROTEIN VP8; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; FLOW CYTOMETRY; ISOTHERMAL TITRATION CALORIMETRY; NEBRASKA CALF DIARRHEA VIRUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; ROTAVIRUS; SIMIAN ROTAVIRUS; SITE DIRECTED MUTAGENESIS; VIRUS STRAIN; X RAY DIFFRACTION;

BASE SEQUENCE; CALORIMETRY; CRYSTALLOGRAPHY, X-RAY; DNA PRIMERS; FLOW CYTOMETRY; MODELS, MOLECULAR; NEURAMINIC ACIDS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; RECEPTORS, VIRUS; ROTAVIRUS; SIALIC ACIDS;

ANIMALIA; BOVINE ROTAVIRUS; PORCINE ROTAVIRUS; RHESUS ROTAVIRUS; ROTAVIRUS;

EID: 84870681494     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06975-11     Document Type: Article

References (45)

1. Blanchard H, Yu X, Coulson BS, von Itzstein M. 2007. Insight into hostcell carbohydrate-recognition by human and porcine rotavirus from crystalstructures of the virion spike associated carbohydrate-binding domain(VP8*). J. Mol. Biol. 367:1215-1226.
2. Byres E, et al. 2008. Incorporation of a non-human glycan mediateshuman susceptibility to a bacterial toxin. Nature 456:648-652.
3. CCP4. 1994. The CCP4 suite: programs for protein crystallography. ActaCrystallogr. D50:760-763.
4. Ciarlet M, et al. 2002. Initial interaction of rotavirus strains with Nacetylneuraminic(sialic) acid residues on thecell surface correlates withVP4 genotype, not species of origin. J. Virol. 76:4087-4095.
5. Coulson BS. 1993. Typing of human rotavirus VP4 by an enzyme immunoassayusing monoclonal antibodies. J. Clin. Microbiol. 31:1-8.
6. Crawrfaut ford SE, et al. 2001. Trypsin cleavage stabilizes the rotavirus VP4spike. J. Virol. 75:6052-6061.
7. DeLano WL. 2002. The PyMOL molecular graphics system. Schrödinger,LLC, Palo Alto, CA.
8. Delorme C, et al. 2001. Glycosphingolipid binding specificities of rotavirus:identification of a sialic acid-binding epitope. J. Virol. 75:2276-2287.
9. Dormitzer PR, et al. 2002. Specificity and affinity of sialic acid binding bythe rhesus rotavirus VP8* core. J. Virl. 76:10512-10517.
10. Dormitzer PR, Sun ZY, Wagner G, Harrison SC. 2002. The rhesusrotavirus VP4 sialic acid binding domain has a galectin fold with a novelcarbohydrate binding site. EMBO J. 21:885-897.
11. Emsley P, Cowtan K. 2004. Coot: model-building tools for moleculargraphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126.
12. Evans P. 2006. Scaling and assessment of data quality. Acta Crystallogr. DBiol. Crystallogr. 62:72-82.
13. Fiore L, Greenberg HB, Mackow ER. 1991. The VP8 fragment of VP4 isthe rhesus rotavirus hemagglutinin. Virology 181:553-563.
14. Graham KL, Takada Y, Coulson BS. 2006. Rotavirus spike protein VP5*binds α2β1 integrin on the cell surface and competes with virus for cellbinding and infectivity. J. Gen. Virol. 87:1275-1283.
15. Greenberg HB, Estes MK. 2009. Rotaviruses: from pathogenesis to vaccination.Gastroenterology 136:1939-1951.
16. Haselhorst T, et al. 2007. STD NMR spectroscopy and molecular modelinginvestigation of the binding of N-acetylneuraminic acid derivativesto rhesus rotavirus VP8* core. Glycobiology 17:68-81.
17. Haselhorst T, et al. 2011. Recognition of the GM3 ganglioside glycan byRhesus rotavirus particles. Angew. Chem. Inted Engl. 50:1055-1058.
18. Haselhorst T, et al. ll2009. Sialic acid dependence in rotavirus host cellinvasion. Nat. Chem. Biol. 5:91-93.
19. Hu L, et al. 2012. Cell attachment protein VP8* of a human rotavirusspecifically interacts with A-type histo-blood group antigen. Nature 485: 256-259
20. Huang JA, Nagesha HS, Holmes IH. 1993. Comparative sequence analysisof VP4s from five Australian porcine rotaviruses: implication of anapparent new P type. Virology 196:319-327.
21. Jolly CL, Beisner BM, Ozser E, Holmes IH. 2001. Non-lytic extractionand characterisation of receptors for multiplestrains of rotavirus. Arch.Virol. 146:1307-1323.
22. Kabsch W, Sander C. 1983. Dictionary of protein secondary structure:pattern recognition of hydrogen-bonded and geometrical features. Biopolymers22:2577-2637.
23. Kelm S, Schauer R. 1997. Sialic acids in molecular and cellular interactions.Int. Rev. Cytol. 175:137-240.
24. Kononov LO, et al. 1998. Synthesis of oligosaccharides related to HNK-1antigen. 2. Synthesis of 3-O-(3-O-sulfo-beta-D-glucuronopyranosyl)-lacto-N-neotetraose beta-propylglycoside. Bioorg. Khim. 24:608-622. In Russian.
25. Kraschnefski MJ, et al. 2009. Effects on sialic acid recognition of aminoacid mutations in the carbohydrate-bindincleft of the rotavirus spikeprotein. Glycobiology 19:194-200.
26. Laskowski RA. 1993. PROCHECK: a program to check the stereochemicalquality of protein structures. J. Appl. Crystallogr. 26:283-291.
27. Leslie AGW. 2006. The integration of macromolecular diffraction data.Acta Crystallogr. D62:48-57.
28. Matthijnssens J, et al. 2006. Full genomic analysis of human rotavirusstrain B4106 and lapine rotavirus strain 30/96 provides evidence for interspeciestransmission. J. Virol. 80:3801-3810.
29. Matthijnssens J, et al. 2006. G8 rotavirus strains isolated in the DemocraticRepublic of Congo belong to the DS-1-like genogroup. J. Clin. Microbiol.44:1801-1809.
30. Mendez E, Arias CF, Lopez S. 1993. Binding to sialic acids is not anessential step for the entry of animal rotaviruses to epithelial cells in culture.J. Virol. 67:5253-5259.
31. Midgley SE, et al. 2012. Diversity and zoonotic potential of rotaviruses inswine and cattle across Europe. Vet. Microbiol. 156:238-245.
32. Murshudov G, Vagin A, Dodson E. 1997. Refinement of macromolecularstructures by the maximum-likelihood method. ActaCrystallogr. D53:240-255.
33. Nagesha HS, Holmes IH. 1988. New porcine rotavirus serotype antigenicallyrelated to human rotavirus serotype 3. J. Clin. Microbiol. 26:171-174.
34. Nishikawa K, et al. 1988. Comparative analysis of the VP3 gene of divergentstrains of the rotaviruses simian SA11 and bovine Nebraska calf diarrheavirus. J. Virol. 62:4022-4026.
35. Olofsson S, Bergstrom T. 2005. Glycoconjugate glycans as viral receptors.Ann. Med. 37:154-172
36. Rolsma MD, Kuhlenschmidt TB, Gelberg HB, Kuhlenschmidt MS.1998. Structure and function of a ganglioside receptor for porcine rotavirus.J. Virol. 72:9079-9091.
37. Ruggeri FM, Greenberg HB. 1991. Antibodies to the trypsin cleavagepeptide VP8 neutralize rotavirus by inhibiting binding of virions to targetcells in culture. J. Virol. 65:2211-2219.
38. Scott SA, et al. 2005. Crystallization and preliminary X-ray diffractionanalysis of the sialic acid-binding domain (VP8*) of porcine rotavirusstrain CRW-8. Acta Crystallogr. F Struct. Biol. Crystallogr. Commun. 61:617-620.
39. Small C, Barro M, Brown TL, Patton JT. 2007. Genome heterogeneity ofSA11 rotavirus due to reassortment with "O" agent. Virology 359:415-424.
40. Tangvoranuntakul P, et al. 2003. Human uptake and incorporation of animmunogenic nonhuman dietary sialic acid. Pr. Natl. Acad. Sci. U. S. A.100:12045-12050.
41. Wallace AC, Laskowski RA, Thornton JM. 1995. LIGPLOT: a program togenerate schematic diagrams of protein-ligand interactions. Protein Eng.8:127-134
42. WHO. 2008. Rotavirus surveillance-worldwide, 2001-2008. MMWRMorb. Mortal. Wkly. Rep. 57:1255-1257.
43. Yolken RH, Willoughby R, Wee SB, Miskuff R, Vonderfecht S. 1987.Sialic acid glycoproteins inhibit in vitro and in vivo replication of rotaviruses.J. Clin. Invest. 79:148-154.
44. Yu X, et al. 2011. Novel structural insights into rotavirus recognition ofganglioside glycan receptors. J. Mol. Biol. 413:929-939.
45. Yu X, et al. 2008. Crystallization and preliminary X-ray diffraction analysisof the carbohydrate-recognizing domain(VP8*) of bovine rotavirusstrain NCDV. Acta Crystallogr. F Struct. Biol. Crystallogr. Commun. 64:509-511.