Human norovirus GII.4(MI001) P dimer binds fucosylated and sialylated carbohydrates

Glycobiology

Volumn 27, Issue 11, 2017, Pages 1027-1037

  Wegener, Henrik ^a   Mallagaray, Álvaro ^a   Schöne, Tobias ^a   Peters, Thomas ^a   Lockhauserbäumer, Julia ^b   Yan, Hao ^b   Uetrecht, Charlotte ^b,c   Hansman, Grant S ^d   Taube, Stefan ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

^b LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^c EUROPEAN XFEL GMBH   (Germany)

^d UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

gangliosides; HBGAs; histo blood group antigens; human noroviruses; sialic acids

Indexed keywords

3' SIALYLLACTOSE; BLOOD GROUP A ANTIGEN; BLOOD GROUP ABH ANTIGEN; BLOOD GROUP ANTIGEN; BLOOD GROUP B ANTIGEN; CARBOHYDRATE; FUCOSE; GANGLIOSIDE; GANGLIOSIDE GM3; HUMAN NOROVIRUS GII.4(MI001) P DIMER; SIALIC ACID; UNCLASSIFIED DRUG; VIRAL PROTEIN; CAPSID PROTEIN; LACTOSE; N ACETYLNEURAMINIC ACID; PROTEIN BINDING;

ARTICLE; DISSOCIATION CONSTANT; EPITOPE MAPPING; FUCOSYLATION; MASS SPECTROMETRY; NOROVIRUS; NOROVIRUS INFECTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DOMAIN; SIALYLATION; SPECTROSCOPY; STOICHIOMETRY; SURFACE PLASMON RESONANCE; ANIMAL; METABOLISM; MOUSE;

ANIMALS; BLOOD GROUP ANTIGENS; CAPSID PROTEINS; FUCOSE; G(M3) GANGLIOSIDE; LACTOSE; MICE; N-ACETYLNEURAMINIC ACID; NOROVIRUS; PROTEIN BINDING;

EID: 85035060645     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwx078     Document Type: Article

References (54)

1. Arai M, Ferreon JC, Wright PE. 2012. Quantitative analysis of multisite protein-ligand interactions by NMR: binding of intrinsically disordered p53 transactivation subdomains with the TAZ2 domain of CBP. J Am Chem Soc. 134:3792-3803.
2. Bu W, Mamedova A, Tan M, Xia M, Jiang X, Hegde RS. 2008. Structural basis for the receptor binding specificity of Norwalk virus. J Virol. 82:5340-5347.
3. Bustamante M, Standl M, Bassat Q, Vilor-Tejedor N, Medina-Gomez C, Bonilla C, Ahluwalia TS, Bacelis J, Bradfield JP, Tiesler CM et al. 2016. A genome-wide association meta-analysis of diarrhoeal disease in young children identifies FUT2 locus and provides plausible biological pathways. Hum Mol Genet. 25:4127-4142.
4. Cao S, Lou Z, Tan M, Chen Y, Liu Y, Zhang Z, Zhang XC, Jiang X, Li X, Rao Z. 2007. Structural basis for the recognition of blood group trisaccharides by norovirus. J Virol. 81:5949-5957.
5. Chen Y, Tan M, Xia M, Hao N, Zhang XC, Huang P, Jiang X, Li X, Rao Z. 2011. Crystallography of a lewis-binding norovirus, elucidation of strainspecificity to the polymorphic human histo-blood group antigens. PLoS Pathog. 7:e1002152.
6. Choi J-M, Hutson AM, Estes MK, Prasad BV. 2008. Atomic resolution structural characterization of recognition of histo-blood group antigens by Norwalk virus. Proc Natl Acad Sci USA. 105:9175-9180.
7. Debbink K, Lindesmith LC, Donaldson EF, Costantini V, Beltramello M, Corti D, Swanstrom J, Lanzavecchia A, Vinjé J, Baric RS. 2013. Emergence of new pandemic GII. 4 Sydney norovirus strain correlates with escape from herd immunity. J Infect Dis. 208:1877-1887.
8. Donaldson EF, Lindesmith LC, Lobue AD, Baric RS. 2008. Norovirus pathogenesis: mechanisms of persistence and immune evasion in human populations. Immunol Rev. 225:190-211.
9. Ettayebi K, Crawford SE, Murakami K, Broughman JR, Karandikar U, Tenge VR, Neill FH, Blutt SE, Zeng XL, Qu L et al. 2016. Replication of human noroviruses in stem cell-derived human enteroids. Science. 353:1387-1393.
10. Fiege B, Rademacher C, Cartmell J, Kitov PI, Parra F, Peters T. 2012. Molecular details of the recognition of blood group antigens by a human norovirus as determined by STD NMR spectroscopy. Angew Chem Int Ed Engl. 51:928-932.
11. Frenck R, Bernstein DI, Xia M, Huang P, Zhong W, Parker S, Dickey M, McNeal M, Jiang X. 2012. Predicting susceptibility to norovirus GII. 4 by use of a challenge model involving humans. J Infect Dis. 206:1386-1393.
12. Han L, Kitov PI, Kitova EN, Tan M, Wang L, Xia M, Jiang X, Klassen JS. 2013. Affinities of recombinant norovirus P dimers for human blood group antigens. Glycobiology. 23:276-285.
13. Han L, Kitova EN, Tan M, Jiang X, Pluvinage B, Boraston AB, Klassen JS. 2015. Affinities of human histo-blood group antigens for norovirus capsid protein complexes. Glycobiology. 25:170-180.
14. Han L, Tan M, Xia M, Kitova EN, Jiang X, Klassen JS. 2014. Gangliosides are ligands for human noroviruses. J Am Chem Soc. 136:12631-12637.
15. Hansman GS, Biertumpfel C, Georgiev I, McLellan JS, Chen L, Zhou T, Katayama K, Kwong PD. 2011. Crystal structures of GII. 10 and GII. 12 norovirus protruding domains in complex with histo-blood group antigens reveal details for a potential site of vulnerability. J Virol. 85:6687-6701.
16. van den Heuvel RH, van Duijn E, Mazon H, Synowsky SA, Lorenzen K, Versluis C, Brouns SJ, Langridge D, van der Oost J, Hoyes J et al. 2006. Improving the performance of a quadrupole time-of-flight instrument for macromolecular mass spectrometry. Anal Chem. 78:7473-7483.
17. Huang P, Farkas T, Marionneau S, Zhong W, Ruvoën-Clouet N, Morrow AL, Altaye M, Pickering LK, Newburg DS, LePendu J et al. 2003. Noroviruses bind to human ABO, Lewis, and secretor histo-blood group antigens: identification of 4 distinct strain-specific patterns. J InfectDis. 188:19-31.
18. Huang P, Farkas T, Zhong W, Tan M, Thornton S, Morrow AL, Jiang X. 2005. Norovirus and histo-blood group antigens: demonstration of a wide spectrum of strain specificities and classification of two major binding groups among multiple binding patterns. J Virol. 79:6714-6722.
19. Hutson AM, Atmar RL, Graham DY, Estes MK. 2002. Norwalk virus infection and disease is associated with ABO histo-blood group type. J Infect Dis. 185:1335-1337.
20. Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR, Grau KR, Gonzalez-Hernandez MB, Iovine NM, Wobus CE, Vinjé J et al. 2014. Enteric bacteria promote human and mouse norovirus infection of B cells. Science. 346:755-759.
21. Kim D-S, Hosmillo M, Alfajaro MM, Kim J-Y, Park J-G, Son K-Y, Ryu E-H, Sorgeloos F, Kwon H-J, Park S-J et al. 2014. Both 2, 3-and 2, 6-linked sialic acids on O-linked glycoproteins act as functional receptors for porcine sapovirus. PLoS Pathog. 10:e1004172.
22. Knipe DM, Howley PM. 2013. Fields Virology. Philadelphia, PA: Lippincott Williams Wilkins.
23. Koromyslova AD, Leuthold MM, Bowler MW, Hansman GS. 2015. The sweet quartet: binding of fucose to the norovirus capsid. Virology. 483:203-208.
24. Le Guyader FS, Krol J, Ambert-Balay K, Ruvoën-Clouet N, Desaubliaux B, Parnaudeau S, Le Saux J-C, Ponge A, Pothier P, Atmar RL et al. 2010. Comprehensive analysis of a norovirus-associated gastroenteritis outbreak, from the environment to the consumer. J Clin Microbiol. 48:915-920.
25. Lindesmith L, Moe C, LePendu J, Frelinger JA, Treanor J, Baric RS. 2005. Cellular and humoral immunity following Snow Mountain virus challenge. J Virol. 79:2900-2909.
26. Lindesmith L, Moe C, Marionneau S, Ruvoën N, Jiang X, Lindblad L, Stewart P, LePendu J, Baric R. 2003. Human susceptibility and resistance to Norwalk virus infection. Nat Med. 9:548-553.
27. Mallagaray A, Lockhauserbäumer J, Hansman G, Uetrecht C, Peters T. 2015. Attachment of norovirus to histo blood group antigens: a cooperative multistep process. Angew Chem Int Ed Engl. 54:12014-12019.
28. Mallagaray A, Rademacher C, Parra F, Hansman G, Peters T. 2017. Saturation transfer difference nuclear magnetic resonance titrations reveal complex multistep-binding of L-fucose to norovirus particles. Glycobiology. 27:80-86.
29. Mayer M, Meyer B. 1999. Characterization of Ligand Binding by Saturation Transfer Difference NMR Spectroscopy. Angew Chem Int Ed. 38: 1784-1788.
30. Mayer M, Meyer B. 2001. Group epitope mapping by saturation transfer difference NMR to identify segments of a ligand in direct contact with a protein receptor. J Am Chem Soc. 123:6108-6117.
31. Olofsson S, Bergström T. 2005. Glycoconjugate glycans as viral receptors. Ann Med. 37:154-172.
32. Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK. 1999. X-ray crystallographic structure of the Norwalk virus capsid. Science. 286:287-290.
33. Rademacher C, Krishna NR, Palcic M, Parra F, Peters T. 2008. NMR experiments reveal the molecular basis of receptor recognition by a calicivirus. J Am Chem Soc. 130:3669-3675.
34. Rydell GE, Nilsson J, Rodriguez-Diaz J, Ruvoën-Clouet N, Svensson L, Le Pendu J, Larson G. 2009. Human noroviruses recognize sialyl Lewis x neoglycoprotein. Glycobiology. 19:309-320.
35. Sabesan S, Bock K, Paulson JC. 1991. Conformational analysis of sialyloligosaccharides. Carbohydr Res. 218:27-54.
36. Schroten H, Hanisch FG, Hansman GS. 2016. Human norovirus interactions with histo-blood group antigens and human milk oligosaccharides. J Virol. 90:5855-5859.
37. Shanker S, Hu L, Ramani S, Atmar RL, Estes MK, Venkataram Prasad BV. 2017. Structural features of glycan recognition among viral pathogens. Curr Opin Struct Biol. 44:211-218.
38. Singh BK, Leuthold MM, Hansman GS. 2015. Human noroviruses' fondness for histo-blood group antigens. J Virol. 89:2024-2040.
39. Singh BK, Leuthold MM, Hansman GS. 2016. Structural constraints on human norovirus binding to histo-blood group antigens. mSphere. 1: e00049-00016.
40. Stencel-Baerenwald JE, Reiss K, Reiter DM, Stehle T, Dermody TS. 2014. The sweet spot: defining virus-sialic acid interactions. Nat Rev Microbiol. 12:739-749.
41. Stuart AD, Brown TDK. 2007. Alpha2, 6-linked sialic acid acts as a receptor for Feline calicivirus. J Gen Virol. 88:177-186.
42. Sun J, Kitova EN, Wang W, Klassen JS. 2006. Method for distinguishing specific from nonspecific protein-ligand complexes in nanoelectrospray ionization mass spectrometry. Anal Chem. 78:3010-3018.
43. Tahallah N, Pinkse M, Maier CS, Heck AJ. 2001. The effect of the source pressure on the abundance of ions of noncovalent protein assemblies in an electrospray ionization orthogonal time-of-flight instrument. Rapid Commun Mass Spectrom. 15:596-601.
44. Tamura M, Natori K, Kobayashi M, Miyamura T, Takeda N. 2004. Genogroup II noroviruses efficiently bind to heparan sulfate proteoglycan associated with the cellular membrane. J Virol. 78:3817-3826.
45. Tan M, Jiang X. 2010. Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathog. 6:e1000983.
46. Tan M, Jin M, Xie H, Duan Z, Jiang X, Fang Z. 2008. Outbreak studies of a GII-3 and a GII-4 norovirus revealed an association between HBGA phenotypes and viral infection. J Med Virol. 80:1296-1301.
47. Tan M, Wei C, Huang P, Fan Q, Quigley C, Xia M, Fang H, Zhang X, Zhong W, Klassen JS et al. 2015. Tulane virus recognizes sialic acids as cellular receptors. Sci Rep. 5:11784.
48. Tan M, Zhong W, Song D, Thornton S, Jiang X. 2004. E. coli-expressed recombinant norovirus capsid proteins maintain authentic antigenicity and receptor binding capability. J Med Virol. 74:641-649.
49. Taube S, Jiang M, Wobus CE. 2010. Glycosphingolipids as receptors for nonenveloped viruses. Viruses. 2:1011-1049.
50. Taube S, Kolawole AO, Höhne M, Wilkinson JE, Handley SA, Perry JW, Thackray LB, Akkina R, Wobus CE. 2013. A mouse model for human norovirus. mBio. 4:e00450,-00413-e00450-00413.
51. Taube S, Perry JW, McGreevy E, Yetming K, Perkins C, Henderson K, Wobus CE. 2012. Murine noroviruses bind glycolipid and glycoprotein attachment receptors in a strain-dependent manner. J Virol. 86:5584-5593.
52. Taube S, Perry JW, Yetming K, Patel SP, Auble H, Shu L, Nawar HF, Lee CH, Connell TD, Shayman JA et al. 2009. Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses. J Virol. 83:4092-4101.
53. Thorven M, Grahn A, Hedlund K-O, Johansson H, Wahlfrid C, Larson G, Svensson L. 2005. A homozygous nonsense mutation (428G->A) in the human secretor (FUT2) gene provides resistance to symptomatic norovirus (GGII) infections. J Virol. 79:15351-15355.
54. Vinjé J. 2015. Advances in Laboratory Methods for Detection and Typing of Norovirus. J Clin Microbiol. 53:373-381.