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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.

Hansman GS, Biertümpfel C, Georgiev I, McLellan JS, Chen L, Zhou T, Katayama K, Kwong PD
J Virol 85 6687-701 (2011)
Related entries: 3onu, 3ony, 3pa1, 3pa2, 3q38, 3q39, 3q3a, 3q6q, 3r6j, 3r6k

Cited: 90 times
EuropePMC logo PMID: 21525337

Abstract

Noroviruses are the dominant cause of outbreaks of gastroenteritis worldwide, and interactions with human histo-blood group antigens (HBGAs) are thought to play a critical role in their entry mechanism. Structures of noroviruses from genogroups GI and GII in complex with HBGAs, however, reveal different modes of interaction. To gain insight into norovirus recognition of HBGAs, we determined crystal structures of norovirus protruding domains from two rarely detected GII genotypes, GII.10 and GII.12, alone and in complex with a panel of HBGAs, and analyzed structure-function implications related to conservation of the HBGA binding pocket. The GII.10- and GII.12-apo structures as well as the previously solved GII.4-apo structure resembled each other more closely than the GI.1-derived structure, and all three GII structures showed similar modes of HBGA recognition. The primary GII norovirus-HBGA interaction involved six hydrogen bonds between a terminal αfucose1-2 of the HBGAs and a dimeric capsid interface, which was composed of elements from two protruding subdomains. Norovirus interactions with other saccharide units of the HBGAs were variable and involved fewer hydrogen bonds. Sequence analysis revealed a site of GII norovirus sequence conservation to reside under the critical αfucose1-2 and to be one of the few patches of conserved residues on the outer virion-capsid surface. The site was smaller than that involved in full HBGA recognition, a consequence of variable recognition of peripheral saccharides. Despite this evasion tactic, the HBGA site of viral vulnerability may provide a viable target for small molecule- and antibody-mediated neutralization of GII norovirus.

Articles - 3q6r mentioned but not cited (2)

  1. 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. Hansman GS, Biertümpfel C, Georgiev I, McLellan JS, Chen L, Zhou T, Katayama K, Kwong PD. J Virol 85 6687-6701 (2011)
  2. Bioinformatics analysis of the epitope regions for norovirus capsid protein. Chen L, Wu D, Ji L, Wu X, Xu D, Cao Z, Han J. BMC Bioinformatics 14 Suppl 4 S5 (2013)


Reviews citing this publication (16)

  1. Histo-blood group antigens: a common niche for norovirus and rotavirus. Tan M, Jiang X. Expert Rev Mol Med 16 e5 (2014)
  2. Noroviruses and histo-blood groups: the impact of common host genetic polymorphisms on virus transmission and evolution. Ruvoën-Clouet N, Belliot G, Le Pendu J. Rev Med Virol 23 355-366 (2013)
  3. Human Milk Oligosaccharides as Promising Antivirals. Morozov V, Hansman G, Hanisch FG, Schroten H, Kunz C. Mol Nutr Food Res 62 e1700679 (2018)
  4. Norovirus P particle: a subviral nanoparticle for vaccine development against norovirus, rotavirus and influenza virus. Tan M, Jiang X. Nanomedicine (Lond) 7 889-897 (2012)
  5. Histo-blood group antigens as mediators of infections. Heggelund JE, Varrot A, Imberty A, Krengel U. Curr Opin Struct Biol 44 190-200 (2017)
  6. Human Norovirus Interactions with Histo-Blood Group Antigens and Human Milk Oligosaccharides. Schroten H, Hanisch FG, Hansman GS. J Virol 90 5855-5859 (2016)
  7. Antiviral targets of human noroviruses. Prasad BV, Shanker S, Muhaxhiri Z, Deng L, Choi JM, Estes MK, Song Y, Palzkill T, Atmar RL. Curr Opin Virol 18 117-125 (2016)
  8. Structural basis of glycan interaction in gastroenteric viral pathogens. Venkataram Prasad BV, Shanker S, Hu L, Choi JM, Crawford SE, Ramani S, Czako R, Atmar RL, Estes MK. Curr Opin Virol 7 119-127 (2014)
  9. The Dynamic Capsid Structures of the Noroviruses. Smith HQ, Smith TJ. Viruses 11 E235 (2019)
  10. Anti-norovirus therapeutics: a patent review (2010-2015). Galasiti Kankanamalage AC, Weerawarna PM, Kim Y, Chang KO, Groutas WC. Expert Opin Ther Pat 26 297-308 (2016)
  11. Glycan Recognition in Human Norovirus Infections. Tenge VR, Hu L, Prasad BVV, Larson G, Atmar RL, Estes MK, Ramani S. Viruses 13 2066 (2021)
  12. Applications of omics approaches to the development of microbiological risk assessment using RNA virus dose-response models as a case study. Gale P, Hill A, Kelly L, Bassett J, McClure P, Le Marc Y, Soumpasis I. J Appl Microbiol 117 1537-1548 (2014)
  13. The Double Face of Mucin-Type O-Glycans in Lectin-Mediated Infection and Immunity. Morozov V, Borkowski J, Hanisch FG. Molecules 23 E1151 (2018)
  14. C-terminal domains of bacterial proteases: structure, function and the biotechnological applications. Huang J, Wu C, Liu D, Yang X, Wu R, Zhang J, Ma C, He H. J Appl Microbiol 122 12-22 (2017)
  15. The bulky and the sweet: How neutralizing antibodies and glycan receptors compete for virus binding. Dietrich MH, Harprecht C, Stehle T. Protein Sci 26 2342-2354 (2017)
  16. [Genetic susceptibility to norovirus infection]. Ruvoën N, Le Pendu J. Pathol Biol (Paris) 61 28-35 (2013)

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  1. Contribution of intra- and interhost dynamics to norovirus evolution. Bull RA, Eden JS, Luciani F, McElroy K, Rawlinson WD, White PA. J Virol 86 3219-3229 (2012)
  2. Norovirus immunity and the great escape. Debbink K, Lindesmith LC, Donaldson EF, Baric RS. PLoS Pathog 8 e1002921 (2012)
  3. Association between norovirus and rotavirus infection and histo-blood group antigen types in Vietnamese children. Van Trang N, Vu HT, Le NT, Huang P, Jiang X, Anh DD. J Clin Microbiol 52 1366-1374 (2014)
  4. Human noroviruses' fondness for histo-blood group antigens. Singh BK, Leuthold MM, Hansman GS. J Virol 89 2024-2040 (2015)
  5. Structural Basis for Norovirus Inhibition by Human Milk Oligosaccharides. Weichert S, Koromyslova A, Singh BK, Hansman S, Jennewein S, Schroten H, Hansman GS. J Virol 90 4843-4848 (2016)
  6. Human norovirus inhibition by a human milk oligosaccharide. Koromyslova A, Tripathi S, Morozov V, Schroten H, Hansman GS. Virology 508 81-89 (2017)
  7. Structural basis for broad detection of genogroup II noroviruses by a monoclonal antibody that binds to a site occluded in the viral particle. Hansman GS, Taylor DW, McLellan JS, Smith TJ, Georgiev I, Tame JR, Park SY, Yamazaki M, Gondaira F, Miki M, Katayama K, Murata K, Kwong PD. J Virol 86 3635-3646 (2012)
  8. Murine noroviruses bind glycolipid and glycoprotein attachment receptors in a strain-dependent manner. Taube S, Perry JW, McGreevy E, Yetming K, Perkins C, Henderson K, Wobus CE. J Virol 86 5584-5593 (2012)
  9. Sera Antibody Repertoire Analyses Reveal Mechanisms of Broad and Pandemic Strain Neutralizing Responses after Human Norovirus Vaccination. Lindesmith LC, McDaniel JR, Changela A, Verardi R, Kerr SA, Costantini V, Brewer-Jensen PD, Mallory ML, Voss WN, Boutz DR, Blazeck JJ, Ippolito GC, Vinje J, Kwong PD, Georgiou G, Baric RS. Immunity 50 1530-1541.e8 (2019)
  10. Structural basis for norovirus inhibition and fucose mimicry by citrate. Hansman GS, Shahzad-Ul-Hussan S, McLellan JS, Chuang GY, Georgiev I, Shimoike T, Katayama K, Bewley CA, Kwong PD. J Virol 86 284-292 (2012)
  11. The importance of intergenic recombination in norovirus GII.3 evolution. Mahar JE, Bok K, Green KY, Kirkwood CD. J Virol 87 3687-3698 (2013)
  12. Structural basis for the recognition of Lewis antigens by genogroup I norovirus. Kubota T, Kumagai A, Ito H, Furukawa S, Someya Y, Takeda N, Ishii K, Wakita T, Narimatsu H, Shirato H. J Virol 86 11138-11150 (2012)
  13. Gangliosides are ligands for human noroviruses. Han L, Tan M, Xia M, Kitova EN, Jiang X, Klassen JS. J Am Chem Soc 136 12631-12637 (2014)
  14. A Unique Human Norovirus Lineage with a Distinct HBGA Binding Interface. Liu W, Chen Y, Jiang X, Xia M, Yang Y, Tan M, Li X, Rao Z. PLoS Pathog 11 e1005025 (2015)
  15. Human Norovirus Neutralized by a Monoclonal Antibody Targeting the Histo-Blood Group Antigen Pocket. Koromyslova AD, Morozov VA, Hefele L, Hansman GS. J Virol 93 e02174-18 (2019)
  16. Nanobody binding to a conserved epitope promotes norovirus particle disassembly. Koromyslova AD, Hansman GS. J Virol 89 2718-2730 (2015)
  17. Structural Basis for Human Norovirus Capsid Binding to Bile Acids. Kilic T, Koromyslova A, Hansman GS. J Virol 93 e01581-18 (2019)
  18. A novel norovirus GII.17 lineage contributed to adult gastroenteritis in Shanghai, China, during the winter of 2014–2015. Chen H, Qian F, Xu J, Chan M, Shen Z, Zai S, Shan M, Cai J, Zhang W, He J, Liu Y, Zhang J, Yuan Z, Zhu Z, Hu Y. Emerg Microbes Infect 4 e67 (2015)
  19. Structural basis for norovirus neutralization by an HBGA blocking human IgA antibody. Shanker S, Czakó R, Sapparapu G, Alvarado G, Viskovska M, Sankaran B, Atmar RL, Crowe JE, Estes MK, Prasad BV. Proc Natl Acad Sci U S A 113 E5830-E5837 (2016)
  20. Inhibition of histo-blood group antigen binding as a novel strategy to block norovirus infections. Zhang XF, Tan M, Chhabra M, Dai YC, Meller J, Jiang X. PLoS One 8 e69379 (2013)
  21. Structural Constraints on Human Norovirus Binding to Histo-Blood Group Antigens. Singh BK, Leuthold MM, Hansman GS. mSphere 1 e00049-16 (2016)
  22. Structure, stability and dynamics of norovirus P domain derived protein complexes studied by native mass spectrometry. Bereszczak JZ, Barbu IM, Tan M, Xia M, Jiang X, van Duijn E, Heck AJ. J Struct Biol 177 273-282 (2012)
  23. Molecular details of the recognition of blood group antigens by a human norovirus as determined by STD NMR spectroscopy. Fiege B, Rademacher C, Cartmell J, Kitov PI, Parra F, Peters T. Angew Chem Int Ed Engl 51 928-932 (2012)
  24. Tannic acid inhibited norovirus binding to HBGA receptors, a study of 50 Chinese medicinal herbs. Zhang XF, Dai YC, Zhong W, Tan M, Lv ZP, Zhou YC, Jiang X. Bioorg Med Chem 20 1616-1623 (2012)
  25. Characterization of the new GII.17 norovirus variant that emerged recently as the predominant strain in China. Jin M, Zhou YK, Xie HP, Fu JG, He YQ, Zhang S, Jing HB, Kong XY, Sun XM, Li HY, Zhang Q, Li K, Zhang YJ, Zhou DQ, Xing WJ, Liao QH, Liu N, Yu HJ, Jiang X, Tan M, Duan ZJ. J Gen Virol 97 2620-2632 (2016)
  26. Recombinant norovirus GII.g/GII.12 gastroenteritis in children. Giammanco GM, Rotolo V, Medici MC, Tummolo F, Bonura F, Chezzi C, Martella V, De Grazia S. Infect Genet Evol 12 169-174 (2012)
  27. Attachment of norovirus to histo blood group antigens: a cooperative multistep process. Mallagaray A, Lockhauserbäumer J, Hansman G, Uetrecht C, Peters T. Angew Chem Int Ed Engl 54 12014-12019 (2015)
  28. Structural Evolution of the Emerging 2014-2015 GII.17 Noroviruses. Singh BK, Koromyslova A, Hefele L, Gürth C, Hansman GS. J Virol 90 2710-2715 (2015)
  29. Atomic Structure of the Murine Norovirus Protruding Domain and Soluble CD300lf Receptor Complex. Kilic T, Koromyslova A, Malak V, Hansman GS. J Virol 92 e00413-18 (2018)
  30. A post-translational modification of human Norovirus capsid protein attenuates glycan binding. Mallagaray A, Creutznacher R, Dülfer J, Mayer PHO, Grimm LL, Orduña JM, Trabjerg E, Stehle T, Rand KD, Blaum BS, Uetrecht C, Peters T. Nat Commun 10 1320 (2019)
  31. Molecular epidemiology of noroviruses detected in Nepalese children with acute diarrhea between 2005 and 2011: increase and predominance of minor genotype GII.13. Hoa-Tran TN, Nakagomi T, Sano D, Sherchand JB, Pandey BD, Cunliffe NA, Nakagomi O. Infect Genet Evol 30 27-36 (2015)
  32. Comparison of human saliva and synthetic histo-blood group antigens usage as ligands in norovirus-like particle binding and blocking assays. Uusi-Kerttula H, Tamminen K, Malm M, Vesikari T, Blazevic V. Microbes Infect 16 472-480 (2014)
  33. Identification of human single-chain antibodies with broad reactivity for noroviruses. Huang W, Samanta M, Crawford SE, Estes MK, Neill FH, Atmar RL, Palzkill T. Protein Eng Des Sel 27 339-349 (2014)
  34. Treatment of norovirus particles with citrate. Koromyslova AD, White PA, Hansman GS. Virology 485 199-204 (2015)
  35. Human Norovirus Evolution in a Chronically Infected Host. Doerflinger SY, Weichert S, Koromyslova A, Chan M, Schwerk C, Adam R, Jennewein S, Hansman GS, Schroten H. mSphere 2 e00352-16 (2017)
  36. Two gastroenteritis outbreaks caused by GII Noroviruses: host susceptibility and HBGA phenotypes. Jin M, He Y, Li H, Huang P, Zhong W, Yang H, Zhang H, Tan M, Duan ZJ. PLoS One 8 e58605 (2013)
  37. Bioengineered Norovirus S60 Nanoparticles as a Multifunctional Vaccine Platform. Xia M, Huang P, Sun C, Han L, Vago FS, Li K, Zhong W, Jiang W, Klassen JS, Jiang X, Tan M. ACS Nano 12 10665-10682 (2018)
  38. Structural analysis of a rabbit hemorrhagic disease virus binding to histo-blood group antigens. Leuthold MM, Dalton KP, Hansman GS. J Virol 89 2378-2387 (2015)
  39. Human norovirus GII.4(MI001) P dimer binds fucosylated and sialylated carbohydrates. Wegener H, Mallagaray Á, Schöne T, Peters T, Lockhauserbäumer J, Yan H, Uetrecht C, Hansman GS, Taube S. Glycobiology 27 1027-1037 (2017)
  40. Identifying carbohydrate ligands of a norovirus P particle using a catch and release electrospray ionization mass spectrometry assay. Han L, Kitova EN, Tan M, Jiang X, Klassen JS. J Am Soc Mass Spectrom 25 111-119 (2014)
  41. Lewis histo-blood group α1,3/α1,4 fucose residues may both mediate binding to GII.4 noroviruses. Nasir W, Frank M, Koppisetty CA, Larson G, Nyholm PG. Glycobiology 22 1163-1172 (2012)
  42. Structural Adaptations of Norovirus GII.17/13/21 Lineage through Two Distinct Evolutionary Paths. Qian Y, Song M, Jiang X, Xia M, Meller J, Tan M, Chen Y, Li X, Rao Z. J Virol 93 e01655-18 (2019)
  43. Antigenic Relatedness of Norovirus GII.4 Variants Determined by Human Challenge Sera. Dai YC, Zhang XF, Xia M, Tan M, Quigley C, Lei W, Fang H, Zhong W, Lee B, Pang X, Nie J, Jiang X. PLoS One 10 e0124945 (2015)
  44. Pandemic GII.4 Sydney and Epidemic GII.17 Kawasaki308 Noroviruses Display Distinct Specificities for Histo-Blood Group Antigens Leading to Different Transmission Vector Dynamics in Pacific Oysters. Morozov V, Hanisch FG, Wegner KM, Schroten H. Front Microbiol 9 2826 (2018)
  45. Saturation transfer difference nuclear magnetic resonance titrations reveal complex multistep-binding of l-fucose to norovirus particles. Mallagaray A, Rademacher C, Parra F, Hansman G, Peters T. Glycobiology 27 80-86 (2017)
  46. Characterizing carbohydrate-protein interactions by nuclear magnetic resonance spectroscopy. Bewley CA, Shahzad-ul-Hussan S. Biopolymers 99 796-806 (2013)
  47. Crystal structures of GI.8 Boxer virus P dimers in complex with HBGAs, a novel evolutionary path selected by the Lewis epitope. Hao N, Chen Y, Xia M, Tan M, Liu W, Guan X, Jiang X, Li X, Rao Z. Protein Cell 6 101-116 (2015)
  48. Detection of Norovirus and Rotavirus Present in Suspended and Dissolved Forms in Drinking Water Sources. Miura T, Gima A, Akiba M. Food Environ Virol 11 9-19 (2019)
  49. The formation of P particle increased immunogenicity of norovirus P protein. Tan M, Jiang X. Immunology 136 28-29 (2012)
  50. Binding-Based RT-qPCR Assay to Assess Binding Patterns of Noroviruses to Shellfish. Langlet J, Kaas L, Greening G. Food Environ Virol (2015)
  51. Quantifying the binding stoichiometry and affinity of histo-blood group antigen oligosaccharides for human noroviruses. Han L, Zheng R, Richards MR, Tan M, Kitova EN, Jiang X, Klassen JS. Glycobiology 28 488-498 (2018)
  52. Structural analysis of a feline norovirus protruding domain. Singh BK, Glatt S, Ferrer JL, Koromyslova AD, Leuthold MM, Dunder J, Hansman GS. Virology 474 181-185 (2015)
  53. Glycan-Induced Protein Dynamics in Human Norovirus P Dimers Depend on Virus Strain and Deamidation Status. Dülfer J, Yan H, Brodmerkel MN, Creutznacher R, Mallagaray A, Peters T, Caleman C, Marklund EG, Uetrecht C. Molecules 26 2125 (2021)
  54. Identification and characterization of antibody-binding epitopes on the norovirus GII.3 capsid. Mahar JE, Donker NC, Bok K, Talbo GH, Green KY, Kirkwood CD. J Virol 88 1942-1952 (2014)
  55. First detection of neboviruses in yak (Bos grunniens) and identification of a novel neboviruses based on complete genome. Guo Z, He Q, Zhang B, Yue H, Tang C. Vet Microbiol 236 108388 (2019)
  56. In Depth Breadth Analyses of Human Blockade Responses to Norovirus and Response to Vaccination. Haynes J, Perry V, Benson E, Meeks A, Watts G, Watkins H, Braun R. Viruses 11 E392 (2019)
  57. Norovirus-glycan interactions - how strong are they really? Peters T, Creutznacher R, Maass T, Mallagaray A, Ogrissek P, Taube S, Thiede L, Uetrecht C. Biochem Soc Trans 50 347-359 (2022)
  58. Structural analysis of bovine norovirus protruding domain. Singh BK, Koromyslova A, Hansman GS. Virology 487 296-301 (2016)
  59. Computational analysis of carbohydrate recognition based on hybrid QM/MM modeling: a case study of norovirus capsid protein in complex with Lewis antigen. Ishida T. Phys Chem Chem Phys 20 4652-4665 (2018)
  60. Genetic analysis and homology modeling of capsid protein of norovirus GII.14. Chan-It W, Thongprachum A, Okitsu S, Mizuguchi M, Ushijima H. J Med Virol 86 329-334 (2014)
  61. Prevalence and complete genome of bovine norovirus with novel VP1 genotype in calves in China. Wang Y, Yue H, Tang C. Sci Rep 9 12023 (2019)
  62. Structural basis of host ligand specificity change of GII porcine noroviruses from their closely related GII human noroviruses. Yang Y, Xia M, Wang L, Arumugam S, Wang Y, Ou X, Wang C, Jiang X, Tan M, Chen Y, Li X. Emerg Microbes Infect 8 1642-1657 (2019)
  63. Letter An Improved One-Step Real-Time Reverse Transcription-PCR Assay for Detection of Norovirus. Glowacka I, Harste G, Witthuhn J, Heim A. J Clin Microbiol 54 497-499 (2016)
  64. In silico 3D structure analysis accelerates the solution of a real viral structure and antibodies docking mechanism. Miki M, Katayama K. Front Microbiol 3 387 (2012)
  65. Methods for ascertaining norovirus disease burdens. Allen DJ, Harris JP. Hum Vaccin Immunother 13 2630-2636 (2017)
  66. Natural extracts, honey, and propolis as human norovirus inhibitors. Ruoff K, Devant JM, Hansman G. Sci Rep 12 8116 (2022)
  67. The histo-blood group antigens of the host cell may determine the binding of different viruses such as SARS-CoV-2. Cuéllar-Cruz M. Future Microbiol 16 107-118 (2021)
  68. Direct Blockade of the Norovirus Histo-Blood Group Antigen Binding Pocket by Nanobodies. Kher G, Sabin C, Lun JH, Devant JM, Ruoff K, Koromyslova AD, von Itzstein M, Pancera M, Hansman GS. J Virol 97 e0183322 (2023)
  69. Immunogenicity and Blocking Efficacy of Norovirus GII.4 Recombinant P Protein Vaccine. Yu Z, Shao Q, Xu Z, Chen C, Li M, Jiang Y, Cheng D. Vaccines (Basel) 11 1053 (2023)
  70. Production of Human Norovirus Protruding Domains in E. coli for X-ray Crystallography. Leuthold MM, Koromyslova AD, Singh BK, Hansman GS. J Vis Exp (2016)
  71. Structural Basis for Rabbit Hemorrhagic Disease Virus Antibody Specificity. Leuthold MM, Kilic T, Devant JM, Landeta O, Parra F, Dalton KP, Hansman GS. J Virol 96 e0121722 (2022)
  72. Structural Insight into Terminal Galactose Recognition by Two Non-HBGA Binding GI.3 Noroviruses. Wang C, Kang H, Tan M, Cong J, Su D, Li X, Chen Y. J Virol 96 e0042022 (2022)


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