RESEARCH ARTICLE

Crystal structures of GI.8 Boxer virus P dimers in complex with HBGAs, a novel evolutionary path selected by the Lewis epitope

  • Ning Hao 1,2 ,
  • Yutao Chen 1 ,
  • Ming Xia 3 ,
  • Ming Tan 3,4 ,
  • Wu Liu 1 ,
  • Xiaotao Guan 1 ,
  • Xi Jiang , 3,4 ,
  • Xuemei Li , 1 ,
  • Zihe Rao 1
Expand
  • 1. National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
  • 2. University of Chinese Academy of Sciences, Beijing 100049, China
  • 3. Division of Infectious Diseases, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA
  • 4. University of Cincinnati College of Medicine, Cincinnati, OH 45267, USA

Received date: 14 Nov 2014

Accepted date: 20 Nov 2014

Published date: 05 Feb 2015

Copyright

2014 This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Abstract

Human noroviruses (huNoVs) recognize histo-blood group antigens (HBGAs) as attachment factors, in which genogroup (G) I and GII huNoVs use distinct binding interfaces. The genetic and evolutionary relationships of GII huNoVs under selection by the host HBGAs have been well elucidated via a number of structural studies; however, such relationships among GI NoVs remain less clear due to the fact that the structures of HBGA-binding interfaces of only three GI NoVs with similar binding profiles are known. In this study the crystal structures of the P dimers of a Lewis-binding strain, the GI.8 Boxer virus (BV) that does not bind the A and H antigens, in complex with the Lewis b (Leb) and Ley antigens, respectively, were determined and compared with those of the three previously known GI huNoVs, i.e. GI.1 Norwalk virus (NV), GI.2 FUV258 (FUV) and GI.7 TCH060 (TCH) that bind the A/H/Le antigens. The HBGA binding interface of BV is composed of a conserved central binding pocket (CBP) that interacts with the β-galactose of the precursor, and a well-developed Le epitope-binding site formed by five amino acids, including three consecutive residues from the long P-loop and one from the S-loop of the P1 subdomain, a feature that was not seen in the other GI NoVs. On the other hand, the H epitope/acetamido binding site observed in the other GI NoVs is greatly degenerated in BV. These data explain the evolutionary path of GI NoVs selected by the polymorphic human HBGAs. While the CBP is conserved, the regions surrounding the CBP are flexible, providing freedom for changes. The loss or degeneration of the H epitope/acetamido binding site and the reinforcement of the Le binding site of the GI.8 BV is a typical example of such change selected by the host Lewis epitope.

Cite this article

Ning Hao , Yutao Chen , Ming Xia , Ming Tan , Wu Liu , Xiaotao Guan , Xi Jiang , Xuemei Li , Zihe Rao . Crystal structures of GI.8 Boxer virus P dimers in complex with HBGAs, a novel evolutionary path selected by the Lewis epitope[J]. Protein & Cell, 2015 , 6(2) : 101 -116 . DOI: 10.1007/s13238-014-0126-0

1
Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr58: 1948-1954

DOI

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 Virol82: 5340-5347

DOI

3
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 Virol81: 5949-5957

DOI

4
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 strain-specificity to the polymorphic human histoblood group antigens. PLoS Pathog7: e1002152

DOI

5
Choi JM, 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 USA105: 9175-9180

DOI

6
de Rougemont A, Ruvoen-Clouet N, Simon B, Estienney M, Elie-Caille C, Aho S, Pothier P, Le Pendu J, Boireau W, Belliot G (2011) Qualitative and quantitative analysis of the binding of GII.4 norovirus variants onto human blood group antigens. J Virol85: 4057-4070

DOI

7
Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr60: 2126-2132

DOI

8
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 Dis206: 1386-1393

DOI

9
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 Virol85: 6687-6701

DOI

10
Huang P, Farkas T, Marionneau S, Zhong W, Ruvoen-Clouet N, Morrow AL, Altaye M, Pickering LK, Newburg DS, LePendu J, Jiang X (2003) Noroviruses bind to human ABO, Lewis, and secretor histo-blood group antigens: identification of 4 distinct strain-specific patterns. J Infect Dis188: 19-31

DOI

11
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 Virol79: 6714-6722

DOI

12
Hutson AM, Atmar RL, Graham DY, Estes MK (2002) Norwalk virus infection and disease is associated with ABO histo-blood group type. J Infect Dis185: 1335-1337

DOI

13
Kroneman A, Vega E, Vennema H, Vinje J, White PA, Hansman G, Green K, Martella V, Katayama K, Koopmans M (2013) Proposal for a unified norovirus nomenclature and genotyping. Arch Virol158: 2059-2068

DOI

14
Kubota T, Kumagai A, Ito H, Furukawa S, Someya Y, Takeda N, Ishii K, Wakita T, Narimatsu H, Shirato H (2012) Structural basis for the recognition of Lewis antigens by genogroup I norovirus. J Virol86: 11138-11150

DOI

15
Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr26: 283-291

DOI

16
Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X, Lindblad L, Stewart P, LePendu J, Baric R (2003) Human susceptibility and resistance to Norwalk virus infection. Nat Med9: 548-553

DOI

17
McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr40: 658-674

DOI

18
Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr53: 240-255

DOI

19
Nordgren J, Nitiema LW, Ouermi D, Simpore J, Svensson L (2013) Host genetic factors affect susceptibility to norovirus infections in Burkina Faso. PLoS One8: e69557

DOI

20
Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol276: 307-326

DOI

21
Prasad BVV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK (1999) X-ray crystallographic structure of the Norwalk virus capsid. Science286: 287

DOI

22
Shanker S, Choi JM, Sankaran B, Atmar RL, Estes MK, Prasad BV (2011) Structural analysis of histo-blood group antigen binding specificity in a norovirus GII. 4 epidemic variant: implications for epochal evolution. J Virol85: 8635-8645

DOI

23
Shanker S, Czako R, Sankaran B, Atmar RL, Estes MK, Prasad BV (2014) Structural analysis of determinants of histo-blood group antigen binding specificity in genogroup I noroviruses. J Virol88: 6168-6180

DOI

24
Shirato H, Ogawa S, Ito H, Sato T, Kameyama A, Narimatsu H, Zheng X, Miyamura T, Wakita T, Ishii K, Takeda N (2008) Noroviruses distinguish between type 1 and type 2 histo-blood group antigens for binding. J Virol82: 10756-10767

DOI

25
Tan M, Jiang X (2005) The p domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors. J Virol79: 14017-14030

DOI

26
Tan M, Jiang X (2010) Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathog6: e1000983

DOI

27
Tan M, Jiang X (2011) Norovirus-host interaction: Multi-selections by human histo-blood group antigens. Trends Microbiol19: 382-388

DOI

28
Tan M, Jiang X (2014) Histo-blood group antigens: a common niche for norovirus and rotavirus. Expert Rev Mol Med16: e5

DOI

29
Tan M, Hegde RS, Jiang X (2004) The P domain of norovirus capsid protein forms dimer and binds to histo-blood group antigen receptors. J Virol78: 6233-6242

DOI

30
Tan M, Fang P, Chachiyo T, Xia M, Huang P, Fang Z, Jiang W, Jiang X (2008a) Noroviral P particle: Structure, function and applications in virus-host interaction. Virology382: 115-123

DOI

31
Tan M, Jin M, Xie H, Duan Z, Jiang X, Fang Z (2008b) Outbreak studies of a GII-3 and a GII-4 norovirus revealed an association between HBGA phenotypes and viral infection. J Med Virol80: 1296-1301

DOI

32
Tan M, Xia M, Cao S, Huang P, Farkas T, Meller J, Hegde RS, Li X, Rao Z, Jiang X (2008c) Elucidation of strain-specific interaction of a GII-4 norovirus with HBGA receptors by site-directed mutagenesis study. Virology379: 324-334

DOI

33
Tan M, Xia M, Chen Y, Bu W, Hegde RS, Meller J, Li X, Jiang X (2009) Conservation of carbohydrate binding interfaces: evidence of human HBGA selection in norovirus evolution. PloS One4: e5058

DOI

34
Tan M, Fang PA, Xia M, Chachiyo T, Jiang W, Jiang X (2011) Terminal modifications of norovirus P domain resulted in a new type of subviral particles, the small P particles. Virology410: 345-352

DOI

35
Zhang XJ, Matthews BW (1995) EDPDB: a multifunctional tool for protein structure analysis. J Appl Crystallogr28: 624-630

DOI

36
Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS (2006) Norovirus classification and proposed strain nomenclature. Virology346: 312-323

DOI

Outlines

/