CoChat
Sign Up
Cited by 65Viral gastroenteritis research and epidemiologyAdvanced Electron Microscopy Techniques and ApplicationsEnzyme Structure and Function

Structural Insights into Calicivirus Attachment and Uncoating

Open access
Bhella, David, Gatherer, Derek, Chaudhry, Yasmin, Pink, Rebecca, Goodfellow, Ian G.·2008·Journal of Virology
DOI 10.1128/jvi.00550-08PMC PMC2519574
Open this paper in CoChat — free account

Abstract

The Caliciviridae family comprises positive-sense RNA viruses of medical and veterinary significance. In humans, caliciviruses are a major cause of acute gastroenteritis, while in animals respiratory illness, conjunctivitis, stomatitis, and hemorrhagic disease are documented. Investigation of virus-host interactions is limited by a lack of culture systems for many viruses in this family. Feline calicivirus (FCV), a member of the Vesivirus genus, provides a tractable model, since it may be propagated in cell culture. Feline junctional adhesion molecule 1 (fJAM-1) was recently identified as a functional receptor for FCV. We have analyzed the structure of this virus-receptor complex by cryo-electron microscopy and three-dimensional image reconstruction, combined with fitting of homology modeled high-resolution coordinates. We show that domain 1 of fJAM-1 binds to the outer face of the P2 domain of the FCV capsid protein VP1, inducing conformational changes in the viral capsid. This study provides the first structural view of a native calicivirus-protein receptor complex and insights into the mechanisms of virus attachment and uncoating.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1128/jvi.00550-08

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 52

  1. [1]Adrian, M., J. Dubochet, J. Lepault, and A. W. McDowall. 1984. Cryo-electron microscopy of viruses. Nature 30832-36. [DOI] [PubMed] [Google Scholar]
  2. [2]Asanaka, M., R. L. Atmar, V. Ruvolo, S. E. Crawford, F. H. Neill, and M. K. Estes. 2005. Replication and packaging of Norwalk virus RNA in cultured mammalian cells. Proc. Natl. Acad. Sci. USA 10210327-10332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. [3]Baker, T. S., and R. H. Cheng. 1996. A model-based approach for determining orientations of biological macromolecules imaged by cryoelectron microscopy. J. Struct. Biol. 116120-130. [DOI] [PubMed] [Google Scholar]
  4. [4]Barton, E. S., J. L. Connolly, J. C. Forrest, J. D. Chappell, and T. S. Dermody. 2001. Utilization of sialic acid as a coreceptor enhances reovirus attachment by multistep adhesion strengthening. J. Biol. Chem. 2762200-2211. [DOI] [PubMed] [Google Scholar]
  5. [5]Barton, E. S., J. C. Forrest, J. L. Connolly, J. D. Chappell, Y. Liu, F. J. Schnell, A. Nusrat, C. A. Parkos, and T. S. Dermody. 2001. Junction adhesion molecule is a receptor for reovirus. Cell 104441-451. [DOI] [PubMed] [Google Scholar]
  6. [6]Bella, J., and M. G. Rossmann. 1999. Review: rhinoviruses and their ICAM receptors. J. Struct. Biol. 12869-74. [DOI] [PubMed] [Google Scholar]
  7. [7]Bubeck, D., D. J. Filman, N. Cheng, A. C. Steven, J. M. Hogle, and D. M. Belnap. 2005. The structure of the poliovirus 135S cell entry intermediate at 10-angstrom resolution reveals the location of an externalized polypeptide that binds to membranes. J. Virol. 797745-7755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. [8]Cao, S., Z. Lou, M. Tan, Y. Chen, Y. Liu, Z. Zhang, X. C. Zhang, X. Jiang, X. Li, and Z. Rao. 2007. Structural basis for the recognition of blood group trisaccharides by norovirus. J. Virol. 815949-5957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. [9]Chen, R., J. D. Neill, M. K. Estes, and B. V. Prasad. 2006. X-ray structure of a native calicivirus: structural insights into antigenic diversity and host specificity. Proc. Natl. Acad. Sci. USA 1038048-8053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. [10]Conway, J. F., and A. C. Steven. 1999. Methods for reconstructing density maps of “single” particles from cryoelectron micrographs to subnanometer resolution. J. Struct. Biol. 128106-118. [DOI] [PubMed] [Google Scholar]
  11. [11]Coyne, C. B., and J. M. Bergelson. 2006. Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124119-131. [DOI] [PubMed] [Google Scholar]
  12. [12]Crowther, R. A., L. A. Amos, J. T. Finch, D. J. De Rosier, and A. Klug. 1970. Three dimensional reconstructions of spherical viruses by Fourier synthesis from electron micrographs. Nature 226421-425. [DOI] [PubMed] [Google Scholar]
  13. [13]Dveksler, G. S., M. N. Pensiero, C. B. Cardellichio, R. K. Williams, G. S. Jiang, K. V. Holmes, and C. W. Dieffenbach. 1991. Cloning of the mouse hepatitis-virus (Mhv) receptor: expression in human and hamster cell lines confers susceptibility to Mhv. J. Virol. 656881-6891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. [14]Fechteler, T., U. Dengler, and D. Schomburg. 1995. Prediction of protein three-dimensional structures in insertion and deletion regions: a procedure for searching databases of representative protein fragments using geometric scoring criteria. J. Mol. Biol. 253114-131. [DOI] [PubMed] [Google Scholar]
  15. [15]Fuller, S. D., S. J. Butcher, R. H. Cheng, and T. S. Baker. 1996. Three-dimensional reconstruction of icosahedral particles: the uncommon line. J. Struct. Biol. 11648-55. [DOI] [PubMed] [Google Scholar]
  16. [16]Green, K. Y., T. Ando, M. S. Balayan, T. Berke, I. N. Clarke, M. K. Estes, D. O. Matson, S. Nakata, J. D. Neill, M. J. Studdert, and H. J. Thiel. 2000. Taxonomy of the caliciviruses. J. Infect. Dis. 181(Suppl. 2)S322-S330. [DOI] [PubMed] [Google Scholar]
  17. [17]Guglielmi, K. M., E. Kirchner, G. H. Holm, T. Stehle, and T. S. Dermody. 2007. Reovirus binding determinants in junctional adhesion molecule-A. J. Biol. Chem. 28217930-17940. [DOI] [PubMed] [Google Scholar]
  18. [18]Guix, S., M. Asanaka, K. Katayama, S. E. Crawford, F. H. Neill, R. L. Atmar, and M. K. Estes. 2007. Norwalk virus RNA is infectious in mammalian cells. J. Virol. 8112238-12248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. [19]Harrington, P. R., L. Lindesmith, B. Yount, C. L. Moe, and R. S. Baric. 2002. Binding of Norwalk virus-like particles to ABH histo-blood group antigens is blocked by antisera from infected human volunteers or experimentally vaccinated mice. J. Virol. 7612335-12343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. [20]Heymann, J. B. 2001. Bsoft: image and molecular processing in electron microscopy. J. Struct. Biol. 133156-169. [DOI] [PubMed] [Google Scholar]
  21. [21]Hogle, J. M. 2002. Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu. Rev. Microbiol. 56677-702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. [22]Hooverlitty, H., and J. M. Greve. 1993. Formation of rhinovirus-soluble ICAM-1 complexes and conformational changes in the virion. J. Virol. 67390-397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. [23]Hurley, K. E., P. A. Pesavento, N. C. Pedersen, A. M. Poland, E. Wilson, and J. E. Foley. 2004. An outbreak of virulent systemic feline calicivirus disease. J. Am. Vet. Med. Assoc. 224241-249. [DOI] [PubMed] [Google Scholar]
  24. [24]Hutson, A. M., F. Airaud, J. LePendu, M. K. Estes, and R. L. Atmar. 2005. Norwalk virus infection associates with secretor status genotyped from sera. J. Med. Virol. 77116-120. [DOI] [PubMed] [Google Scholar]
  25. [25]Kapikian, A. Z., R. G. Wyatt, R. Dolin, T. S. Thornhill, A. R. Kalica, and R. M. Chanock. 1972. Visualization by immune electron microscopy of a 27-nm particle associated with acute infectious nonbacterial gastroenteritis. J. Virol. 101075-1081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. [26]Kostrewa, D., M. Brockhaus, A. D'Arcy, G. E. Dale, P. Nelboeck, G. Schmid, F. Mueller, G. Bazzoni, E. Dejana, T. Bartfai, F. K. Winkler, and M. Hennig. 2001. X-ray structure of junctional adhesion molecule: structural basis for homophilic adhesion via a novel dimerization motif. EMBO J. 204391-4398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 26a.Labute, P. 2008. The generalized Born/volume integral implicit solvent model: estimation of the free energy of hydration using London dispersion instead of atomic surface area. J. Comp. Chem. 291693-1698. [DOI] [PubMed] [Google Scholar]
  28. [27]Levitt, M. 1992. Accurate modeling of protein conformation by automatic segment matching. J. Mol. Biol. 226507-533. [DOI] [PubMed] [Google Scholar]
  29. [28]Lindesmith, L., C. Moe, S. Marionneau, N. Ruvoen, X. Jiang, L. Lindblad, P. Stewart, J. LePendu, and R. Baric. 2003. Human susceptibility and resistance to Norwalk virus infection. Nat. Med. 9548-553. [DOI] [PubMed] [Google Scholar]
  30. [29]Makino, A., M. Shimojima, T. Miyazawa, K. Kato, Y. Tohya, and H. Akashi. 2006. Junctional adhesion molecule 1 is a functional receptor for feline calicivirus. J. Virol. 804482-4490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. [30]Marionneau, S., F. Airaud, N. V. Bovin, J. Le Pendu, and N. Ruvoen-Clouet. 2005. Influence of the combined ABO, FUT2, and FUT3 polymorphism on susceptibility to Norwalk virus attachment. J. Infect. Dis. 1921071-1077. [DOI] [PubMed] [Google Scholar]
  32. [31]Marionneau, S., N. Ruvoen, B. Le Moullac-Vaidye, M. Clement, A. Cailleau-Thomas, G. Ruiz-Palacois, P. Huang, X. Jiang, and J. Le Pendu. 2002. Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 1221967-1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. [32]Mothes, W., A. L. Boerger, S. Narayan, J. M. Cunningham, and J. A. Young. 2000. Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. Cell 103679-689. [DOI] [PubMed] [Google Scholar]
  34. [33]Nurani, G., B. Lindqvist, and J. M. Casasnovas. 2003. Receptor priming of major group human rhinoviruses for uncoating and entry at mild low-pH environments. J. Virol. 7711985-11991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. [34]Ossiboff, R. J., and J. S. Parker. 2007. Identification of regions and residues in feline junctional adhesion molecule required for feline calicivirus binding and infection. J. Virol. 8113608-13621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. [35]Ossiboff, R. J., A. Sheh, J. Shotton, P. A. Pesavento, and J. S. Parker. 2007. Feline caliciviruses (FCVs) isolated from cats with virulent systemic disease possess in vitro phenotypes distinct from those of other FCV isolates. J. Gen. Virol. 88506-517. [DOI] [PubMed] [Google Scholar]
  37. [36]Pettersen, E. F., T. D. Goddard, C. C. Huang, G. S. Couch, D. M. Greenblatt, E. C. Meng, and T. E. Ferrin. 2004. UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 251605-1612. [DOI] [PubMed] [Google Scholar]
  38. [37]Pettigrew, D. M., D. T. Williams, D. Kerrigan, D. J. Evans, S. M. Lea, and D. Bhella. 2006. Structural and functional insights into the interaction of echoviruses and decay-accelerating factor. J. Biol. Chem. 2815169-5177. [DOI] [PubMed] [Google Scholar]
  39. [38]Philipson, L., and R. F. Pettersson. 2004. The coxsackie-adenovirus receptor-a new receptor in the immunoglobulin family involved in cell adhesion. Curr. Top. Microbiol. Immunol. 27387-111. [DOI] [PubMed] [Google Scholar]
  40. [39]Prasad, B. V., M. E. Hardy, T. Dokland, J. Bella, M. G. Rossmann, and M. K. Estes. 1999. X-ray crystallographic structure of the Norwalk virus capsid. Science 286287-290. [DOI] [PubMed] [Google Scholar]
  41. [40]Prasad, B. V., D. O. Matson, and A. W. Smith. 1994. Three-dimensional structure of calicivirus. J. Mol. Biol. 240256-264. [DOI] [PubMed] [Google Scholar]
  42. [41]Prota, A. E., J. A. Campbell, P. Schelling, J. C. Forrest, M. J. Watson, T. R. Peters, M. Aurrand-Lions, B. A. Imhof, T. S. Dermody, and T. Stehle. 2003. Crystal structure of human junctional adhesion molecule 1: implications for reovirus binding. Proc. Natl. Acad. Sci. USA 1005366-5371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. [42]Radford, A. D., K. P. Coyne, S. Dawson, C. J. Porter, and R. M. Gaskell. 2007. Feline calicivirus. Vet. Res. 38319-335. [DOI] [PubMed] [Google Scholar]
  44. [43]Seal, B. S., J. F. Ridpath, and W. L. Mengeling. 1993. Analysis of feline calicivirus capsid protein genes: identification of variable antigenic determinant regions of the protein. J. Gen. Virol. 74(Pt. 11)2519-2524. [DOI] [PubMed] [Google Scholar]
  45. [44]Stuart, A. D., and T. D. Brown. 2007. Alpha2,6-linked sialic acid acts as a receptor for Feline calicivirus. J. Gen. Virol. 88177-186. [DOI] [PubMed] [Google Scholar]
  46. [45]Stuart, A. D., and T. D. Brown. 2006. Entry of feline calicivirus is dependent on clathrin-mediated endocytosis and acidification in endosomes. J. Virol. 807500-7509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. [46]Thiel, H. J., and M. Konig. 1999. Caliciviruses: an overview. Vet. Microbiol. 6955-62. [DOI] [PubMed] [Google Scholar]
  48. [47]Thoulouze, M. I., M. Lafage, M. Schachner, U. Hartmann, H. Cremer, and M. Lafon. 1998. The neural cell adhesion molecule is a receptor for rabies virus. J. Virol. 727181-7190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. [48]Waddington, S. N., J. H. McVey, D. Bhella, A. L. Parker, K. Barker, H. Atoda, R. Pink, S. M. Buckley, J. A. Greig, L. Denby, J. Custers, T. Morita, I. M. Francischetti, R. Q. Monteiro, D. H. Barouch, N. van Rooijen, C. Napoli, M. J. Havenga, S. A. Nicklin, and A. H. Baker. 2008. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 132397-409. [DOI] [PubMed] [Google Scholar]
  50. [49]Wang, J. M., P. Cieplak, and P. A. Kollman. 2000. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 211049-1074. [Google Scholar]
  51. [50]Wriggers, W., R. A. Milligan, and J. A. McCammon. 1999. Situs: a package for docking crystal structures into low-resolution maps from electron microscopy. J. Struct. Biol. 125185-195. [DOI] [PubMed] [Google Scholar]
  52. [51]Zhou, L., Q. Z. Yu, and M. Luo. 1994. Characterization of two density populations of feline calicivirus particles. Virology 205530-533. [DOI] [PubMed] [Google Scholar]

Cited by

Sorted by citations

Authors
Bhella, D., Gatherer, D., Chaudhry, Y., Pink, R., & Goodfellow, I. G.
Affiliations
  • University of Glasgow (GB)
  • Imperial College London (GB)
Corresponding author
Bhella, David
ORCID
Venue
Journal of Virology
Publisher
American Society for Microbiology
Published
2008-08-15
Volume
82
Issue
16
Pages
8051-8058
ISSN
  • 0022-538X (ISSN-L)
  • 1098-5514
DOI
10.1128/jvi.00550-08
PMC
PMC2519574
OpenAlex
W1989465852
Cited by
65
References
0
Citations by year
2026: 2 · 2025: 3 · 2024: 3 · 2022: 5 · 2021: 4 · 2020: 2 · 2019: 4 · 2018: 6 · 2017: 1 · 2016: 3 · 2015: 1 · 2014: 6 · 2013: 4 · 2012: 5
FWCI
3.44
Type
journal article
Language
en
Open access
Licence
journals.asm.org/non-commercial-tdm-license (tdm)
Locations
  • Journal of Virology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion)
  • Lancaster EPrints (Lancaster University) (submittedVersion)
Funders
Wellcome Trust (081624)
Topics
  • Health Sciences › Medicine › Infectious Diseases › Viral gastroenteritis research and epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
  • Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
Keywords
feline calicivirus, viral uncoating, VP1 capsid protein, P2 domain, capsid conformational change, Vesivirus, receptor binding domain, viral entry mechanism
MeSH terms
Animals, Epitopes, Caliciviridae, Capsid, Cats, Cell Adhesion, Image Processing, Computer-Assisted, Kidney, Microscopy, Electron, Molecular Conformation, Polysaccharides, Protein Binding, Protein Structure, Tertiary, Calicivirus, Feline, Cryoelectron Microscopy

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review