Crystallography of a Lewis-Binding Norovirus, Elucidation of Strain-Specificity to the Polymorphic Human Histo-Blood Group Antigens
Noroviruses, an important cause of acute gastroenteritis in humans, recognize the histo-blood group antigens (HBGAs) as host susceptible factors in a strain-specific manner. The crystal structures of the HBGA-binding interfaces of two A/B/H-binding noroviruses, the prototype Norwalk virus (GI.1) and a predominant GII.4 strain (VA387), have been elucidated. In this study we determined the crystal structures of the P domain protein of the first Lewis-binding norovirus (VA207, GII.9) that has a distinct binding property from those of Norwalk virus and VA387. Co-crystallization of the VA207 P dimer with Ley or sialyl Lex tetrasaccharides showed that VA207 interacts with these antigens through a common site found on the VA387 P protein which is highly conserved among most GII noroviruses. However, the HBGA-binding site of VA207 targeted at the Lewis antigens through the α-1, 3 fucose (the Lewis epitope) as major and the β-N-acetyl glucosamine of the precursor as minor interacting sites. This completely differs from the binding mode of VA387 and Norwalk virus that target at the secretor epitopes. Binding pocket of VA207 is formed by seven amino acids, of which five residues build up the core structure that is essential for the basic binding function, while the other two are involved in strain-specificity. Our results elucidate for the first time the genetic and structural basis of strain-specificity by a direct comparison of two genetically related noroviruses in their interaction with different HBGAs. The results provide insight into the complex interaction between the diverse noroviruses and the polymorphic HBGAs and highlight the role of human HBGA as a critical factor in norovirus evolution.
Vyšlo v časopise:
Crystallography of a Lewis-Binding Norovirus, Elucidation of Strain-Specificity to the Polymorphic Human Histo-Blood Group Antigens. PLoS Pathog 7(7): e32767. doi:10.1371/journal.ppat.1002152
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002152
Souhrn
Noroviruses, an important cause of acute gastroenteritis in humans, recognize the histo-blood group antigens (HBGAs) as host susceptible factors in a strain-specific manner. The crystal structures of the HBGA-binding interfaces of two A/B/H-binding noroviruses, the prototype Norwalk virus (GI.1) and a predominant GII.4 strain (VA387), have been elucidated. In this study we determined the crystal structures of the P domain protein of the first Lewis-binding norovirus (VA207, GII.9) that has a distinct binding property from those of Norwalk virus and VA387. Co-crystallization of the VA207 P dimer with Ley or sialyl Lex tetrasaccharides showed that VA207 interacts with these antigens through a common site found on the VA387 P protein which is highly conserved among most GII noroviruses. However, the HBGA-binding site of VA207 targeted at the Lewis antigens through the α-1, 3 fucose (the Lewis epitope) as major and the β-N-acetyl glucosamine of the precursor as minor interacting sites. This completely differs from the binding mode of VA387 and Norwalk virus that target at the secretor epitopes. Binding pocket of VA207 is formed by seven amino acids, of which five residues build up the core structure that is essential for the basic binding function, while the other two are involved in strain-specificity. Our results elucidate for the first time the genetic and structural basis of strain-specificity by a direct comparison of two genetically related noroviruses in their interaction with different HBGAs. The results provide insight into the complex interaction between the diverse noroviruses and the polymorphic HBGAs and highlight the role of human HBGA as a critical factor in norovirus evolution.
Zdroje
1. GreenKChanockRKapikianA 2001 Human Calicivirus. KnipeDMHowleyPMGriffinDELambRAMartin MA etal Fields Virology 4th ed. Philadelphia:Lippincott Williams & Wilkins 841 874
2. TanMFarkasTJiangX 2009 Molecular Pathogenesis of Human Norovirus. YangDC RNA Virus: Host Gene Responses to Infection 1 ed. Singapore:World Scientific 575 600
3. TanMJiangX 2007 Norovirus-host interaction: implications for disease control and prevention. Expert Rev Mol Med 9 1 22
4. PrasadBVHardyMEDoklandTBellaJRossmannMG 1999 X-ray crystallographic structure of the Norwalk virus capsid. Science 286 287 290
5. Bertolotti-CiarletAWhiteLJChenRPrasadBVEstesMK 2002 Structural requirements for the assembly of Norwalk virus-like particles. J Virol 76 4044 4055
6. TanMHegdeRSJiangX 2004 The P domain of norovirus capsid protein forms dimer and binds to histo-blood group antigen receptors. J Virol 78 6233 6242
7. TanMFangPChachiyoTXiaMHuangP 2008 Noroviral P particle: Structure, function and applications in virus-host interaction. Virology 382 115 123
8. TanMJiangX 2005 The p domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors. J Virol 79 14017 14030
9. TanMMellerJJiangX 2006 C-terminal arginine cluster is essential for receptor binding of norovirus capsid protein. J Virol 80 7322 7331
10. TanMXiaMCaoSHuangPFarkasT 2008 Elucidation of strain-specific interaction of a GII-4 norovirus with HBGA receptors by site-directed mutagenesis study. Virology 379 324 334
11. TanMXiaMChenYBuWHegdeRS 2009 Conservation of carbohydrate binding interfaces: evidence of human HBGA selection in norovirus evolution. PLoS One 4 e5058
12. TanMHuangPXiaMFangPAZhongW 2011 Norovirus P particle, a novel platform for vaccine development and antibody production. J Virol 85 753 764
13. TanMFangPAXiaMChachiyoTJiangW 2011 Terminal modifications of norovirus P domain resulted in a new type of subviral particles, the small P particles. Virology 410 345 352
14. TanMJiangX 2005 Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol 13 285 293
15. TanMJiangX 2010 Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathog 6 e1000983
16. Le PenduJ 2004 Histo-blood group antigen and human milk oligosaccharides: genetic polymorphism and risk of infectious diseases. Adv Exp Med Biol 554 135 143
17. RavnVDabelsteenE 2000 Tissue distribution of histo-blood group antigens. Apmis 108 1 28
18. BuWMamedovaATanMXiaMJiangX 2008 Structural basis for the receptor binding specificity of Norwalk virus. J Virol 82 5340 5347
19. CaoSLouZTanMChenYLiuY 2007 Structural basis for the recognition of blood group trisaccharides by norovirus. J Virol 81 5949 5957
20. ChoiJMHutsonAMEstesMKPrasadBV 2008 Atomic resolution structural characterization of recognition of histo-blood group antigens by Norwalk virus. Proc Natl Acad Sci U S A 105 9175 9180
21. TanMHuangPMellerJZhongWFarkasT 2003 Mutations within the P2 Domain of Norovirus Capsid Affect Binding to Human Histo-Blood Group Antigens: Evidence for a Binding Pocket. J Virol 77 12562 12571
22. HuangPFarkasTMarionneauSZhongWRuvoen-ClouetN 2003 Noroviruses Bind to Human ABO, Lewis, and Secretor Histo-Blood Group Antigens: Identification of 4 Distinct Strain-Specific Patterns. J Infect Dis 188 19 31
23. HuangPFarkasTZhongWTanMThorntonS 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
24. OtwinowskiZMinorW 1997 Processing of X-ray diffraction data collected in oscillation mode. Method Enzymol 276 307 326
25. McCoyAJGrosse-KunstleveRWStoroniLCReadRJ 2005 Likelihood-enhanced fast translation functions. Acta Crystallogr D 61 458 464
26. EmsleyPCowtanK 2004 Coot: model-building tools for molecular graphics. Acta Crystallogr D 60 2126 2132
27. BrungerATAdamsPDCloreGMDeLanoWLGrosP 1998 Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D 54 905 921
28. MurshudovGNVaginAADodsonEJ 1997 Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 53 240 255
29. AdamsPDGrosse-KunstleveRWHungLWIoergerTRMcCoyAJ 2002 PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D 58 1948 1954
30. LaskowskiRAMacArthurMWMossDSThorntonJM 1993 PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26 283 291
31. ZhangXJMatthewsBW 1995 EDPDB: a multifunctional tool for protein structure analysis. J Appl Crystallogr 28 624 630
32. de RougemontARuvoen-ClouetNSimonBEstienneyMElie-CailleC 2011 Qualitative and Quantitative Analysis of the Binding of GII.4 Norovirus Variants onto Human Blood Group Antigens. J Virol 85 4057 4070
33. RydellGENilssonJRodriguez-DiazJRuvoen-ClouetNSvenssonL 2009 Human noroviruses recognize sialyl Lewis x neoglycoprotein. Glycobiology 19 309 320
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2011 Číslo 7
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Requires Glycerol for Maximum Fitness During The Tick Phase of the Enzootic Cycle
- Comparative Genomics Yields Insights into Niche Adaptation of Plant Vascular Wilt Pathogens
- The Role of IL-15 Deficiency in the Pathogenesis of Virus-Induced Asthma Exacerbations
- “Persisters”: Survival at the Cellular Level