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Calicivirus VP2 forms a portal-like assembly following receptor engagement.

Conley MJ, McElwee M, Azmi L, Gabrielsen M, Byron O, Goodfellow IG, Bhella D
Nature 565 377-381 (2019)
Cited: 61 times
EuropePMC logo PMID: 30626974

Abstract

To initiate infection, many viruses enter their host cells by triggering endocytosis following receptor engagement. However, the mechanisms by which non-enveloped viruses escape the endosome are poorly understood. Here we present near-atomic-resolution cryo-electron microscopy structures for feline calicivirus both undecorated and labelled with a soluble fragment of its cellular receptor, feline junctional adhesion molecule A. We show that VP2, a minor capsid protein encoded by all caliciviruses1,2, forms a large portal-like assembly at a unique three-fold axis of symmetry, following receptor engagement. This assembly-which was not detected in undecorated virions-is formed of twelve copies of VP2, arranged with their hydrophobic N termini pointing away from the virion surface. Local rearrangement at the portal site leads to the opening of a pore in the capsid shell. We hypothesize that the portal-like assembly functions as a channel for the delivery of the calicivirus genome, through the endosomal membrane, into the cytoplasm of a host cell, thereby initiating infection. VP2 was previously known to be critical for the production of infectious virus3; our findings provide insights into its structure and function that advance our understanding of the Caliciviridae.

Reviews - 6gsi mentioned but not cited (2)

  1. Norovirus Attachment and Entry. Graziano VR, Wei J, Wilen CB. Viruses 11 (2019)
  2. Structural and dynamic asymmetry in icosahedrally symmetric virus capsids. Jana AK, May ER. Curr Opin Virol 45 8-16 (2020)

Articles - 6gsi mentioned but not cited (3)

  1. Multiple Correspondence Analysis on Amino Acid Properties within the Variable Region of the Capsid Protein Shows Differences between Classical and Virulent Systemic Feline Calicivirus Strains. Brunet S, Sigoillot-Claude C, Pialot D, Poulet H. Viruses 11 (2019)
  2. Structure-Based In Silico Screening of Marine Phlorotannins for Potential Walrus Calicivirus Inhibitor. Kang N, Kim EA, Heo SY, Heo SJ. Int J Mol Sci 24 15774 (2023)
  3. The Cryo-EM Structure of Vesivirus 2117 Highlights Functional Variations in Entry Pathways for Viruses in Different Clades of the Vesivirus Genus. Sutherland H, Conley MJ, Emmott E, Streetley J, Goodfellow IG, Bhella D. J Virol 95 e0028221 (2021)


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  1. The epidemiology of norovirus gastroenteritis in China: disease burden and distribution of genotypes. Zhou H, Wang S, von Seidlein L, Wang X. Front Med 14 1-7 (2020)
  2. Bile Goes Viral. Tenge VR, Murakami K, Salmen W, Lin SC, Crawford SE, Neill FH, Prasad BVV, Atmar RL, Estes MK. Viruses 13 998 (2021)
  3. Caliciviridae Other Than Noroviruses. Desselberger U. Viruses 11 (2019)
  4. Current and Future Antiviral Strategies to Tackle Gastrointestinal Viral Infections. Santos-Ferreira N, Van Dycke J, Neyts J, Rocha-Pereira J. Microorganisms 9 1599 (2021)
  5. Asymmetric analysis reveals novel virus capsid features. Conley MJ, Bhella D. Biophys Rev 11 603-609 (2019)
  6. Calicivirus Infection in Cats. Hofmann-Lehmann R, Hosie MJ, Hartmann K, Egberink H, Truyen U, Tasker S, Belák S, Boucraut-Baralon C, Frymus T, Lloret A, Marsilio F, Pennisi MG, Addie DD, Lutz H, Thiry E, Radford AD, Möstl K. Viruses 14 937 (2022)
  7. Norovirus encounters in the gut: multifaceted interactions and disease outcomes. Hassan E, Baldridge MT. Mucosal Immunol 12 1259-1267 (2019)
  8. The Dynamic Capsid Structures of the Noroviruses. Smith HQ, Smith TJ. Viruses 11 (2019)
  9. Noroviruses-The State of the Art, Nearly Fifty Years after Their Initial Discovery. Ludwig-Begall LF, Mauroy A, Thiry E. Viruses 13 1541 (2021)
  10. Calicivirus RNA-Dependent RNA Polymerases: Evolution, Structure, Protein Dynamics, and Function. Smertina E, Urakova N, Strive T, Frese M. Front Microbiol 10 1280 (2019)
  11. Immune Response Modulation by Caliciviruses. Peñaflor-Téllez Y, Trujillo-Uscanga A, Escobar-Almazán JA, Gutiérrez-Escolano AL. Front Immunol 10 2334 (2019)
  12. Interferon responses to norovirus infections: current and future perspectives. Jahun AS, Goodfellow IG. J Gen Virol 102 (2021)
  13. Membranes under the Magnetic Lens: A Dive into the Diverse World of Membrane Protein Structures Using Cryo-EM. Piper SJ, Johnson RM, Wootten D, Sexton PM. Chem Rev 122 13989-14017 (2022)
  14. Norovirus Capsid Protein-Derived Nanoparticles and Polymers as Versatile Platforms for Antigen Presentation and Vaccine Development. Tan M, Jiang X. Pharmaceutics 11 (2019)
  15. Structural Features of Tight-Junction Proteins. Heinemann U, Schuetz A. Int J Mol Sci 20 (2019)

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  1. Updated classification of norovirus genogroups and genotypes. Chhabra P, de Graaf M, Parra GI, Chan MC, Green K, Martella V, Wang Q, White PA, Katayama K, Vennema H, Koopmans MPG, Vinjé J. J Gen Virol 100 1393-1406 (2019)
  2. Bile acids and ceramide overcome the entry restriction for GII.3 human norovirus replication in human intestinal enteroids. Murakami K, Tenge VR, Karandikar UC, Lin SC, Ramani S, Ettayebi K, Crawford SE, Zeng XL, Neill FH, Ayyar BV, Katayama K, Graham DY, Bieberich E, Atmar RL, Estes MK. Proc Natl Acad Sci U S A 117 1700-1710 (2020)
  3. Inhibitory Effects of Laminaria japonica Fucoidans Against Noroviruses. Kim H, Lim CY, Lee DB, Seok JH, Kim KH, Chung MS. Viruses 12 E997 (2020)
  4. Nanobody-Mediated Neutralization Reveals an Achilles Heel for Norovirus. Koromyslova AD, Devant JM, Kilic T, Sabin CD, Malak V, Hansman GS. J Virol 94 e00660-20 (2020)
  5. Frequent intergenotypic recombination between the non-structural and structural genes is a major driver of epidemiological fitness in caliciviruses. Mahar JE, Jenckel M, Huang N, Smertina E, Holmes EC, Strive T, Hall RN. Virus Evol 7 veab080 (2021)
  6. Norovirus-Specific CD8+ T Cell Responses in Human Blood and Tissues. Pattekar A, Mayer LS, Lau CW, Liu C, Palko O, Bewtra M, Consortium H, Lindesmith LC, Brewer-Jensen PD, Baric RS, Betts MR, Naji A, Wherry EJ, Tomov VT. Cell Mol Gastroenterol Hepatol 11 1267-1289 (2021)
  7. Co-circulation and evolution of genogroups I and II of respiratory and enteric feline calicivirus isolates in cats. Guo J, Ding Y, Sun F, Zhou H, He P, Chen J, Guo J, Zeng H, Long J, Wei Z, Ouyang K, Huang W, Chen Y. Transbound Emerg Dis 69 2924-2937 (2022)
  8. Structural basis of rotavirus RNA chaperone displacement and RNA annealing. Bravo JPK, Bartnik K, Venditti L, Acker J, Gail EH, Colyer A, Davidovich C, Lamb DC, Tuma R, Calabrese AN, Borodavka A. Proc Natl Acad Sci U S A 118 e2100198118 (2021)
  9. Structural changes in bacteriophage T7 upon receptor-induced genome ejection. Chen W, Xiao H, Wang L, Wang X, Tan Z, Han Z, Li X, Yang F, Liu Z, Song J, Liu H, Cheng L. Proc Natl Acad Sci U S A 118 e2102003118 (2021)
  10. Atomic Structure of the Human Sapovirus Capsid Reveals a Unique Capsid Protein Conformation in Caliciviruses. Miyazaki N, Song C, Oka T, Miki M, Murakami K, Iwasaki K, Katayama K, Murata K. J Virol 96 e0029822 (2022)
  11. Letter Cryo-electron microscopy: an introduction to the technique, and considerations when working to establish a national facility. Bhella D. Biophys Rev 11 515-519 (2019)
  12. Dynamic rotation of the protruding domain enhances the infectivity of norovirus. Song C, Takai-Todaka R, Miki M, Haga K, Fujimoto A, Ishiyama R, Oikawa K, Yokoyama M, Miyazaki N, Iwasaki K, Murakami K, Katayama K, Murata K. PLoS Pathog 16 e1008619 (2020)
  13. Dynamics in the murine norovirus capsid revealed by high-resolution cryo-EM. Snowden JS, Hurdiss DL, Adeyemi OO, Ranson NA, Herod MR, Stonehouse NJ. PLoS Biol 18 e3000649 (2020)
  14. Genomics Analyses of GIV and GVI Noroviruses Reveal the Distinct Clustering of Human and Animal Viruses. Ford-Siltz LA, Mullis L, Sanad YM, Tohma K, Lepore CJ, Azevedo M, Parra GI. Viruses 11 (2019)
  15. High-resolution cryo-EM structures of outbreak strain human norovirus shells reveal size variations. Jung J, Grant T, Thomas DR, Diehnelt CW, Grigorieff N, Joshua-Tor L. Proc. Natl. Acad. Sci. U.S.A. 116 12828-12832 (2019)
  16. In vitro functional analysis of gRNA sites regulating assembly of hepatitis B virus. Patel N, Clark S, Weiß EU, Mata CP, Bohon J, Farquhar ER, Maskell DP, Ranson NA, Twarock R, Stockley PG. Commun Biol 4 1407 (2021)
  17. Lewis b antigen is a common ligand for genogroup I norovirus strains. Someya Y. FEBS Open Bio 12 1688-1695 (2022)
  18. A single nanobody neutralizes multiple epochally evolving human noroviruses by modulating capsid plasticity. Salmen W, Hu L, Bok M, Chaimongkol N, Ettayebi K, Sosnovtsev SV, Soni K, Ayyar BV, Shanker S, Neill FH, Sankaran B, Atmar RL, Estes MK, Green KY, Parreño V, Prasad BVV. Nat Commun 14 6516 (2023)
  19. Amino acid substitutions in norovirus VP1 dictate host dissemination via variations in cellular attachment. Mills JT, Minogue SC, Snowden JS, Arden WKC, Rowlands DJ, Stonehouse NJ, Wobus CE, Herod MR. J Virol 97 e0171923 (2023)
  20. Antiviral Activities of Asarones and Rhizomes of Acorus gramineus on Murine Norovirus. Kim H, Maeng JY, Lee DB, Kim KH, Chung MS. Viruses 14 2228 (2022)
  21. Assembly of infectious enteroviruses depends on multiple, conserved genomic RNA-coat protein contacts. Chandler-Bostock R, Mata CP, Bingham RJ, Dykeman EC, Meng B, Tuthill TJ, Rowlands DJ, Ranson NA, Twarock R, Stockley PG. PLoS Pathog 16 e1009146 (2020)
  22. Atomic structure of the predominant GII.4 human norovirus capsid reveals novel stability and plasticity. Hu L, Salmen W, Chen R, Zhou Y, Neill F, Crowe JE, Atmar RL, Estes MK, Prasad BVV. Nat Commun 13 1241 (2022)
  23. Characterization of a Human Sapovirus Genotype GII.3 Strain Generated by a Reverse Genetics System: VP2 Is a Minor Structural Protein of the Virion. Li TC, Kataoka M, Doan YH, Saito H, Takagi H, Muramatsu M, Oka T. Viruses 14 1649 (2022)
  24. Characterization of surface-exposed structural loops as insertion sites for foreign antigen delivery in calicivirus-derived VLP platform. Panasiuk M, Chraniuk M, Zimmer K, Hovhannisyan L, Krapchev V, Peszyńska-Sularz G, Narajczyk M, Węsławski J, Konopacka A, Gromadzka B. Front Microbiol 14 1111947 (2023)
  25. Complete Genome Sequence, Molecular Characterization and Phylogenetic Relationships of a Temminck's Stint Calicivirus: Evidence for a New Genus within Caliciviridae Family. Matsvay A, Dyachkova M, Sai A, Burskaia V, Artyushin I, Shipulin G. Microorganisms 10 1540 (2022)
  26. Complete genome characterization of human noroviruses allows comparison of minor alleles during acute and chronic infections. Kelly D, Jere KC, Darby AC, Allen DJ, Iturriza-Gómara M. Access Microbiol 3 000203 (2021)
  27. Cryo-EM structures reveal two distinct conformational states in a picornavirus cell entry intermediate. Shah PNM, Filman DJ, Karunatilaka KS, Hesketh EL, Groppelli E, Strauss M, Hogle JM. PLoS Pathog 16 e1008920 (2020)
  28. Emerging Novel GII.P16 Noroviruses Associated with Multiple Capsid Genotypes. Barclay L, Cannon JL, Wikswo ME, Phillips AR, Browne H, Montmayeur AM, Tatusov RL, Burke RM, Hall AJ, Vinjé J. Viruses 11 (2019)
  29. Evolutionary analyses of emerging GII.2[P16] and GII.4 Sydney [P16] noroviruses. Zheng GL, Zhu ZX, Cui JL, Yu JM. Virus Evol 8 veac030 (2022)
  30. Experimental Adaptation of Murine Norovirus to Calcium Hydroxide. Oishi W, Sato M, Kubota K, Ishiyama R, Takai-Todaka R, Haga K, Katayama K, Sano D. Front Microbiol 13 848439 (2022)
  31. Feline calicivirus strain 2280 p30 antagonizes type I interferon-mediated antiviral innate immunity through directly degrading IFNAR1 mRNA. Tian J, Kang H, Huang J, Li Z, Pan Y, Li Y, Chen S, Zhang J, Yin H, Qu L. PLoS Pathog 16 e1008944 (2020)
  32. Icariin, Formononetin and Caffeic Acid Phenethyl Ester Inhibit Feline Calicivirus Replication In Vitro. Cui Z, Wang Q, Li D, Zhao S, Zhang Q, Tan Y, Gong Q, Liu T, Shao J, Zhang S, Huang H, Wang J, Pei Z, Dong H, Wang K, Hu G, Li Z. Arch Virol 166 2443-2450 (2021)
  33. Lewis fucose is a key moiety for the recognition of histo-blood group antigens by GI.9 norovirus, as revealed by structural analysis. Kimura-Someya T, Kato-Murayama M, Katsura K, Sakai N, Murayama K, Hanada K, Shirouzu M, Someya Y. FEBS Open Bio 12 560-570 (2022)
  34. Major Capsid Protein Synthesis from the Genomic RNA of Feline Calicivirus. Urban C, Luttermann C. J Virol 94 (2020)
  35. Molecular Characterization and Phylogenetic Analysis of Feline Calicivirus Isolated in Guangdong Province, China from 2018 to 2022. Mao J, Ye S, Li Q, Bai Y, Wu J, Xu L, Wang Z, Wang J, Zhou P, Li S. Viruses 14 2421 (2022)
  36. Mutagenic Analysis of a DNA Translocating Tube's Interior Surface. Roznowski AP, Fisher JM, Fane BA. Viruses 12 (2020)
  37. Precise location of linear epitopes on the capsid surface of feline calicivirus recognized by neutralizing and non-neutralizing monoclonal antibodies. Cubillos-Zapata C, Angulo I, Almanza H, Borrego B, Zamora-Ceballos M, Castón JR, Mena I, Blanco E, Bárcena J. Vet Res 51 59 (2020)
  38. Structural insight into Pichia pastoris fatty acid synthase. Snowden JS, Alzahrani J, Sherry L, Stacey M, Rowlands DJ, Ranson NA, Stonehouse NJ. Sci Rep 11 9773 (2021)
  39. Structural puzzles in virology solved with an overarching icosahedral design principle. Twarock R, Luque A. Nat Commun 10 4414 (2019)
  40. Utilizing Molecular Epidemiology and Citizen Science for the Surveillance of Lagoviruses in Australia. Peng NYG, Hall RN, Huang N, West P, Cox TE, Mahar JE, Mason H, Campbell S, O'Connor T, Read AJ, Patel KK, Taggart PL, Smith IL, Strive T, Jenckel M. Viruses 15 2348 (2023)
  41. VelcroVax: a "Bolt-On" Vaccine Platform for Glycoprotein Display. Kingston NJ, Grehan K, Snowden JS, Hassall M, Alzahrani J, Paesen GC, Sherry L, Hayward C, Roe A, Stephen S, Tomlinson D, Zeltina A, Doores KJ, Ranson NA, Stacey M, Page M, Rose NJ, Bowden TA, Rowlands DJ, Stonehouse NJ. mSphere 8 e0056822 (2023)


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