Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-26T06:49:01.860Z Has data issue: false hasContentIssue false
  • English
  • Français

Histo-blood group antigens: a common niche for norovirus and rotavirus

Published online by Cambridge University Press:  10 March 2014

Ming Tan  and
Xi Jiang
Ming Tan
Affiliation:
Cincinnati Children's Hospital Medical Center, University of Cincinnati College of Medicine, Cincinnati, OH, USA
Xi Jiang*
Affiliation:
Cincinnati Children's Hospital Medical Center, University of Cincinnati College of Medicine, Cincinnati, OH, USA
*
*Corresponding author: Xi Jiang, PhD, Division of Infectious Diseases, Department of Pediatrics, Cincinnati Children's Hospital Medical Center, University of Cincinnati College of Medicine, 3333 Burnet Avenue, Cincinnati, OH 45229, USA. E-mail: [email protected]; [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Noroviruses (NoVs) and rotaviruses (RVs), the two most important causes of viral acute gastroenteritis, are found to recognise histo-blood group antigens (HBGAs) as receptors or ligands for attachment. Human HBGAs are highly polymorphic containing ABO, secretor and Lewis antigens. In addition, both NoVs and RVs are highly diverse in how they recognise these HBGAs. Structural analysis of the HBGA-binding interfaces of NoVs revealed a conserved central binding pocket (CBP) interacting with a common major binding saccharide (MaBS) of HBGAs and a variable surrounding region interacting with additional minor binding saccharides. The conserved CBP indicates a strong selection of NoVs by the host HBGAs, whereas the variable surrounding region explains the diverse recognition patterns of different HBGAs by NoVs and RVs as functional adaptations of the viruses to human HBGAs. Diverse recognition of HBGAs has also been found in bacterial pathogen Helicobacter pylori. Thus, exploratory research into whether such diverse recognitions also occur for other viral and bacterial pathogens that recognise HBGAs is warranted.

Type
Review Article
Information
Expert Reviews in Molecular Medicine , Volume 16 , 2014 , e5
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

References

1Marionneau, S. et al. (2001) ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie 83, 565-573Google Scholar
2Tan, M. and Jiang, X. (2005) Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends in Microbiology 13, 285-293CrossRefGoogle ScholarPubMed
3Tan, M. and Jiang, X. (2007) Norovirus-host interaction: implications for disease control and prevention. Expert Reviews in Molecular Medicine 9, 1-22Google Scholar
4Tan, M. and Jiang, X. (2010) Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathogens 6, e1000983CrossRefGoogle ScholarPubMed
5Tan, M. and Jiang, X. (2010) Virus-host interaction and cellular receptors of caliciviruses. In Caliciruses (Hansman, G., Jiang, X. and Green, K., eds), pp. 111-130, Caister Academic Press, NorwichGoogle Scholar
6Hutson, A.M., Atmar, R.L. and Estes, M.K. (2004) Norovirus disease: changing epidemiology and host susceptibility factors. Trends in Microbiology 12, 279-287CrossRefGoogle ScholarPubMed
7Hutson, A.M. et al. (2002) Norwalk virus infection and disease is associated with ABO histo-blood group type. The Journal of Infectious Diseases 185, 1335-1337Google Scholar
8Lindesmith, L. et al. (2003) Human susceptibility and resistance to Norwalk virus infection. Nature Medicine 9, 548-553Google Scholar
9Frenck, R. et al. (2012) Predicting susceptibility to norovirus GII.4 by use of a challenge model involving humans. The Journal of Infectious Diseases 206, 1386-1393CrossRefGoogle ScholarPubMed
10Tan, M. et al. (2008) Outbreak studies of a GII-3 and a GII-4 norovirus revealed an association between HBGA phenotypes and viral infection. Journal of Medical Virology 80, 1296-1301CrossRefGoogle Scholar
11Bu, W. et al. (2008) Structural basis for the receptor binding specificity of Norwalk virus. Journal of Virology 82, 5340-5347CrossRefGoogle ScholarPubMed
12Cao, S. et al. (2007) Structural basis for the recognition of blood group trisaccharides by norovirus. Journal of Virology 81, 5949-5957Google Scholar
13Chen, Y. et al. (2011) Crystallography of a lewis-binding norovirus, elucidation of strain-specificity to the polymorphic human histo-blood group antigens. PLoS Pathogens 7, e1002152Google Scholar
14Choi, J.M. et al. (2008) Atomic resolution structural characterization of recognition of histo-blood group antigens by Norwalk virus. Proceedings of the National Academy of Sciences of the United States of America 105, 9175-9180Google Scholar
15Hansman, G.S. et al. (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. Journal of Virology 85, 6687-6701Google Scholar
16Shanker, S. et al. (2011) Structural analysis of histo-blood group antigen binding specificity in a norovirus GII.4 epidemic variant: implications for epochal evolution. Journal of Virology 85, 8635-8645CrossRefGoogle Scholar
17Kubota, T. et al. (2012) Structural basis for the recognition of Lewis antigens by genogroup I norovirus. Journal of Virology 86, 11138-11150Google Scholar
18Bertolotti-Ciarlet, A. et al. (2002) Structural requirements for the assembly of Norwalk virus-like particles. Journal of Virology 76, 4044-4055CrossRefGoogle ScholarPubMed
19Zarate, S. et al. (2003) Interaction of rotaviruses with Hsc70 during cell entry is mediated by VP5. Journal of Virology 77, 7254-7260Google Scholar
20Lopez, S. and Arias, C.F. (2004) Multistep entry of rotavirus into cells: a Versaillesque dance. Trends in Microbiology 12, 271-278Google Scholar
21Lopez, S. and Arias, C.F. (2006) Early steps in rotavirus cell entry. Current Topics in Microbiology and Immunology 309, 39-66Google Scholar
22Guo, C.T. et al. (1999) Ganglioside GM(1a) on the cell surface is involved in the infection by human rotavirus KUN and MO strains. Journal of Biochemistry (Tokyo) 126, 683-688Google Scholar
23Delorme, C. et al. (2001) Glycosphingolipid binding specificities of rotavirus: identification of a sialic acid-binding epitope. Journal of Virology 75, 2276-2287Google Scholar
24Isa, P. et al. (2004) Rotavirus RRV associates with lipid membrane microdomains during cell entry. Virology 322, 370-381Google Scholar
25Coulson, B.S., Londrigan, S.L. and Lee, D.J. (1997) Rotavirus contains integrin ligand sequences and a disintegrin-like domain that are implicated in virus entry into cells. Proceedings of the National Academy of Sciences of the United States of America 94, 5389-5394CrossRefGoogle Scholar
26Hewish, M.J., Takada, Y. and Coulson, B.S. (2000) Integrins alpha2beta1 and alpha4beta1 can mediate SA11 rotavirus attachment and entry into cells. Journal of Virology 74, 228-236Google Scholar
27Graham, K.L. et al. (2003) Integrin-using rotaviruses bind alpha2beta1 integrin alpha2 I domain via VP4 DGE sequence and recognize alphaXbeta2 and alphaVbeta3 by using VP7 during cell entry. Journal of Virology 77, 9969-9978Google Scholar
28Hu, L. et al. (2012) Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 485, 256-259CrossRefGoogle ScholarPubMed
29Huang, P. et al. (2012) Spike protein VP8* of human rotavirus recognizes histo-blood group antigens in a type-specific manner. Journal of Virology 86, 4833-4843Google Scholar
30Liu, Y. et al. (2012) Rotavirus VP8*: phylogeny, host range, and interaction with histo-blood group antigens. Journal of Virology 86, 9899-9910Google Scholar
31Aspholm-Hurtig, M. et al. (2004) Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science (New York, NY) 305, 519-522Google Scholar
32Aspholm, M. et al. (2006) SabA is the H. pylori hemagglutinin and is polymorphic in binding to sialylated glycans. PLoS Pathogens 2, e110Google Scholar
33Bok, K. and Green, K.Y. (2012) Norovirus gastroenteritis in immunocompromised patients. New England Journal of Medicine 367, 2126-2132Google Scholar
34Rayani, A. et al. (2007) Rotavirus infections in paediatric oncology patients: a matched-pairs analysis. Scandinavian Journal of Gastroenterology 42, 81-87CrossRefGoogle ScholarPubMed
35Tan, M., Hegde, R.S. and Jiang, X. (2004) The P domain of norovirus capsid protein forms dimer and binds to histo-blood group antigen receptors. Journal of Virology 78, 6233-6242CrossRefGoogle Scholar
36Tan, M. et al. (2003) Mutations within the P2 domain of norovirus capsid affect binding to human histo-blood group antigens: evidence for a binding pocket. Journal of Virology 77, 12562-12571CrossRefGoogle ScholarPubMed
37Prasad, B.V. et al. (1999) X-ray crystallographic structure of the Norwalk virus capsid. Science 286, 287-290Google Scholar
38Jiang, X. et al. (1992) Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. Journal of Virology 66, 6527-6532CrossRefGoogle ScholarPubMed
39Huang, P. et al. (2003) Noroviruses bind to human ABO, Lewis, and secretor histo-blood group antigens: identification of 4 distinct strain-specific patterns. The Journal of Infectious Diseases 188, 19-31Google Scholar
40Huang, P. et al. (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. Journal of Virology 79, 6714-6722Google Scholar
41Harrington, P.R. et al. (2004) Norovirus capture with histo-blood group antigens reveals novel virus-ligand interactions. Journal of Virology 78, 3035-3045Google Scholar
42Lindesmith, L.C. et al. (2008) Mechanisms of GII.4 norovirus persistence in human populations. PLoS Medicine 5, e31Google Scholar
43Tan, M. et al. (2011) Terminal modifications of norovirus P domain resulted in a new type of subviral particles, the small P particles. Virology 410, 345-352Google Scholar
44Tan, M. and Jiang, X. (2005) The p domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors. Journal of Virology 79, 14017-14030CrossRefGoogle Scholar
45Tan, M. and Jiang, X. (2012) Norovirus P particle, a subviral nanoparticle for vaccine development against norovirus, rotavirus and influenza virus. Nanomedicine 7, 1-9CrossRefGoogle ScholarPubMed
46Tan, M. et al. (2011) Norovirus P Particle as a Platform for Antigen Presentation. Procedia in Vaccinology 4, 19-26CrossRefGoogle Scholar
47Tan, M. and Jiang, X. (2012) Norovirus P particle: a subviral nanoparticle for vaccine development against norovirus, rotavirus and influenza virus. Nanomedicine (Lond) 7, 889-897Google Scholar
48Tan, M. et al. (2008) Elucidation of strain-specific interaction of a GII-4 norovirus with HBGA receptors by site-directed mutagenesis study. Virology 379, 324-334Google Scholar
49Tan, M. et al. (2009) Conservation of carbohydrate binding interfaces: evidence of human HBGA selection in norovirus evolution. PLoS ONE 4, e5058Google Scholar
50Dai, Y.C. et al. (2012) Evaluation of anti-norovirus IgY from egg yolk of chickens immunized with norovirus P particles. Journal of Virological Methods 186, 126-131Google Scholar
51Dai, Y.C. et al. (2013) A dual chicken IgY against rotavirus and norovirus. Antiviral Research 97, 293-300CrossRefGoogle ScholarPubMed
52Aad, G. et al. (2013) Measurement of Z boson production in Pb-Pb collisions at sqrt[s_{NN}] = 2.76TeV with the ATLAS detector. Physical Review Letters 110, 022301Google Scholar
53Greenberg, H.B. et al. (1981) Proteins of Norwalk virus. Journal of Virology 37, 994-999Google Scholar
54Hardy, M.E. et al. (1995) Specific proteolytic cleavage of recombinant Norwalk virus capsid protein. Journal of Virology 69, 1693-1698CrossRefGoogle ScholarPubMed
55Tan, M., Meller, J. and Jiang, X. (2006) C-terminal arginine cluster is essential for receptor binding of norovirus capsid protein. Journal of Virology 80, 7322-7331Google Scholar
56Settembre, E.C. et al. (2011) Atomic model of an infectious rotavirus particle. The EMBO Journal 30, 408-416Google Scholar
57Trask, S.D., Ogden, K.M. and Patton, J.T. (2012) Interactions among capsid proteins orchestrate rotavirus particle functions. Current Opinion in Virology 2, 373-379CrossRefGoogle ScholarPubMed
58Ruggeri, F.M. and Greenberg, H.B. (1991) Antibodies to the trypsin cleavage peptide VP8 neutralize rotavirus by inhibiting binding of virions to target cells in culture. Journal of Virology 65, 2211-2219Google Scholar
59Pesavento, J.B. et al. (2005) pH-induced conformational change of the rotavirus VP4 spike: implications for cell entry and antibody neutralization. Journal of Virology 79, 8572-8580Google Scholar
60Fiore, L., Greenberg, H.B. and Mackow, E.R. (1991) The VP8 fragment of VP4 is the rhesus rotavirus hemagglutinin. Virology 181, 553-563CrossRefGoogle ScholarPubMed
61Patton, J.T., Hua, J. and Mansell, E.A. (1993) Location of intrachain disulfide bonds in the VP5* and VP8* trypsin cleavage fragments of the rhesus rotavirus spike protein VP4. Journal of Virology 67, 4848-4855Google Scholar
62Padilla-Noriega, L. et al. (1995) Identification of two independent neutralization domains on the VP4 trypsin cleavage products VP5* and VP8* of human rotavirus ST3. Virology 206, 148-154Google Scholar
63Arias, C.F. et al. (2002) Molecular biology of rotavirus cell entry. Archives of Medical Research 33, 356-361Google Scholar
64Monnier, N. et al. (2006) High-resolution molecular and antigen structure of the VP8* core of a sialic acid-independent human rotavirus strain. Journal of Virology 80, 1513-1523Google Scholar
65Zheng, D.P. et al. (2006) Norovirus classification and proposed strain nomenclature. Virology 346, 312-323CrossRefGoogle ScholarPubMed
66Esona, M.D. et al. (2010) Reassortant group A rotavirus from straw-colored fruit bat (Eidolon helvum). Emerging Infectious Diseases 16, 1844-1852Google Scholar
67Khamrin, P. et al. (2006) Emergence of human G9 rotavirus with an exceptionally high frequency in children admitted to hospital with diarrhea in Chiang Mai, Thailand. Journal of Medical Virology 78, 273-280Google Scholar
68Le Pendu, J. (2004) Histo-blood group antigen and human milk oligosaccharides: genetic polymorphism and risk of infectious diseases. Advances in Experimental Medicine and Biology 554, 135-143CrossRefGoogle ScholarPubMed
69Ravn, V. and Dabelsteen, E. (2000) Tissue distribution of histo-blood group antigens. APMIS 108, 1-28Google Scholar
70Hutson, A.M. et al. (2003) Norwalk virus-like particle hemagglutination by binding to h histo-blood group antigens. Journal of Virology 77, 405-415CrossRefGoogle ScholarPubMed
71Hutson, A.M. et al. (2005) Norwalk virus infection associates with secretor status genotyped from sera. Journal of Medical Virology 77, 116-120Google Scholar
72Rockx, B.H. et al. (2005) Association of histo-blood group antigens and susceptibility to norovirus infections. The Journal of Infectious Diseases 191, 749-754Google Scholar
73Duizr, E. et al. (2004) Laboratory efforts to cultivate noroviruses. The Journal of General Virology 85(Pt 1), 79-87Google Scholar
74Lindesmith, L. et al. (2005) Cellular and humoral immunity following Snow Mountain virus challenge. Journal of Virology 79, 2900-2909Google Scholar
75Ruvoen-Clouet, N. et al. (2000) Binding of rabbit hemorrhagic disease virus to antigens of the ABH histo-blood group family. Journal of Virology 74, 11950-11954CrossRefGoogle ScholarPubMed
76Nystrom, K. et al. (2011) Histo-blood group antigens act as attachment factors of rabbit hemorrhagic disease virus infection in a virus strain-dependent manner. PLoS Pathogens 7, e1002188Google Scholar
77Farkas, T. et al. (2010) Genetic diversity and histo-blood group antigen interactions of rhesus enteric caliciviruses. Journal of Virology 84, 8617-8625Google Scholar
78Taube, S. et al. (2012) Murine noroviruses bind glycolipid and glycoprotein attachment receptors in a strain-dependent manner. Journal of Virology 86, 5584-5593Google Scholar
79Stuart, A.D. and Brown, T.D. (2007) Alpha2,6-linked sialic acid acts as a receptor for Feline calicivirus. The Journal of General Virology 88(Pt 1), 177-186Google Scholar
80Zakhour, M. et al. (2010) Bovine norovirus: carbohydrate ligand, environmental contamination, and potential cross-species transmission via oysters. Applied and Environmental Microbiology 76, 6404-6411CrossRefGoogle ScholarPubMed
81Ossiboff, R.J. and Parker, J.S. (2007) Identification of regions and residues in feline junctional adhesion molecule required for feline calicivirus binding and infection. Journal of Virology 81, 13608-13621Google Scholar
82Liu, Y. et al. (2013) Poly-LacNAc as an Age-Specific Ligand for Rotavirus P[11] in neonates and infants. PLoS ONE [Electronic Resource] 8, e78113Google Scholar
83(2011) Rotavirus surveillance – worldwide, 2009. MMWR Morbidity and Mortality Weekly Report 60, 514–516Google Scholar
84Shirato, H. et al. (2008) Noroviruses distinguish between type 1 and type 2 histo-blood group antigens for binding. Journal of Virology 82, 10756-10767Google Scholar
85Blanchard, H. et al. (2007) Insight into host cell carbohydrate-recognition by human and porcine rotavirus from crystal structures of the virion spike associated carbohydrate-binding domain (VP8*). Journal of Molecular Biology 367, 1215-1226CrossRefGoogle ScholarPubMed
86Dormitzer, P.R. et al. (2002) The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. The EMBO Journal 21, 885-897Google Scholar
87Ablikim, M. et al. (2006) Observation of two new N* peaks in J/psi – >ppi − n and ppi + n decays. Physical Review Letters 97, 062001Google Scholar
88de Rougemont, A. et al. (2011) Qualitative and quantitative analysis of the binding of GII.4 norovirus variants onto human blood group antigens. Journal of Virology 85, 4057-4070Google Scholar
89Bishop, J.R. and Gagneux, P. (2007) Evolution of carbohydrate antigens – microbial forces shaping host glycomes? Glycobiology 17, 23R–34RGoogle Scholar
90Zakhour, M. et al. (2009) The alphaGal epitope of the histo-blood group antigen family is a ligand for bovine norovirus Newbury2 expected to prevent cross-species transmission. PLoS Pathogens 5, e1000504CrossRefGoogle ScholarPubMed
91Souza, M. et al. (2007) Cytokine and antibody responses in gnotobiotic pigs after infection with human norovirus genogroup II.4 (HS66 strain). Journal of Virology 81, 9183-9192Google Scholar
92Souza, M. et al. (2008) Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II.4-HS66 strain of human norovirus. Journal of Virology 82, 1777-1786Google Scholar
93Tian, P. et al. (2010) Specificity and kinetics of norovirus binding to magnetic bead-conjugated histo-blood group antigens. Journal of Applied Microbiology 109, 1753-1762Google Scholar
94Le Pendu, J. et al. (2006) Mendelian resistance to human norovirus infections. Seminars in Immunology 18, 375-86Google Scholar
95de Rougemont, A. et al. (2011) Qualitative and quantitative analysis of the binding of GII.4 norovirus variants onto human blood group antigens. Journal of Virology 85, 4057-4070CrossRefGoogle ScholarPubMed
96Tan, M. and Jiang, X. (2011) Norovirus-host interaction: multi-selections by the human HBGAs. Trends in Microbiology 19, 382-388Google Scholar
97Yang, Y. et al. (2010) Genetic and phenotypic characterization of GII-4 noroviruses that circulated during 1987 to 2008. Journal of Virology 84, 9595-9607Google Scholar
98Lindesmith, L.C. et al. (2012) Immunogenetic mechanisms driving norovirus GII.4 antigenic variation. PLoS Pathogens 8, e1002705Google Scholar
99Parra, G.I. et al. (2012) Multiple antigenic sites are involved in blocking the interaction of GII.4 norovirus capsid with ABH histo-blood group antigens. Journal of Virology 86, 7414-7426Google Scholar
100Lindesmith, L.C. et al. (2012) Monoclonal antibody-based antigenic mapping of norovirus GII.4–2002. Journal of Virology 86, 873-883Google Scholar
101Niv, Y. et al. (1996) Helicobacter pylori infection and blood groups. The American Journal of Gastroenterology 91, 101-104Google Scholar
102May, S.J., Blackwell, C.C. and Weir, D.M. (1989) Lewis a blood group antigen of non-secretors: a receptor for candida blastospores. FEMS Microbiology Immunology 1, 407-409Google Scholar
103Darwazeh, A.M. et al. (1990) The relationship between colonisation, secretor status and in-vitro adhesion of Candida albicans to buccal epithelial cells from diabetics. Journal of Medical Microbiology 33, 43-49Google Scholar
104Burford-Mason, A.P., Weber, J.C. and Willoughby, J.M. (1988) Oral carriage of Candida albicans, ABO blood group and secretor status in healthy subjects. Journal of Medical and Veterinary Mycology: Bi-monthly Publication of the International Society for Human and Animal Mycology 26, 49-56Google Scholar
105Shin, E.-S. et al. (2003) The relationship between oral Candida carriage and the secretor status of blood group antigens in saliva. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics 96, 48-53Google Scholar
106Bush, R.M. et al. (1999) Predicting the evolution of human influenza A. Science 286, 1921-1925Google Scholar
107Ha, Y. et al. (2001) X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proceedings of the National Academy of Sciences of the United States of America 98, 11181-11186CrossRefGoogle ScholarPubMed

Further reading, resources and contacts

CDC – Norovirus Home Page (http://www.cdc.gov/norovirus/about/index.html): provides basic information about norovirus and its illness, including how norovirus spreads, symptoms of norovirus illness and prevention of norovirus infection.Google Scholar
CDC – Rotavirus Home Page (http://www.cdc.gov/rotavirus/index.html): provides common knowledge of rotavirus and its disease, transmission, treatment and vaccination.Google Scholar