Skip to main content
Top
Published in: Gut Pathogens 1/2022

Open Access 01-12-2022 | Research

Rapid screening for antigenic characterization of GII.17 norovirus strains with variations in capsid gene

Authors: Yingyin Liao, Liang Xue, Junshan Gao, Yueting Zuo, Yanhui Liang, Yueting Jiang, Weicheng Cai, Jiale Yang, Jumei Zhang, Yu Ding, Moutong Chen, Aiwu Wu, Xiaoxia Kou, Qingping Wu

Published in: Gut Pathogens | Issue 1/2022

Login to get access

Abstract

The emergence of the novel GII.17 Kawasaki 2014 norovirus variant raising the interest of the public, has replaced GII.4 as the predominant cause of noroviruses outbreaks in East Asia during 2014–2015. Antigenic variation of the capsid protein is considered as one of the key mechanisms of norovirus evolution. In this study, we screened a panel of GII.17 mutants. First, we produced norovirus P proteins using cell-free protein synthesis (CFPS) system, comparing the results to pure proteins expressed in a cell-based system. Next, we determined the binding capability of specific monoclonal antibody (mAb) 2D11 using a unique set of wild-type GII.17 strains. Results of the EIA involving a panel of mutant cell-free proteins indicated that Q298 was the key residue within loop 1. These data highlighted the essential residues in the linear antibody binding characteristics of novel GII.17. Furthermore, it supported the CFPS as a promising tool for rapidly screening mutants via the scalable expression of norovirus P proteins.
Appendix
Available only for authorised users
Literature
1.
go back to reference Liao Y, Hong X, Wu A, Jiang Y, Liang Y, Gao J, et al. Global prevalence of norovirus in cases of acute gastroenteritis from 1997 to 2021: an updated systematic review and meta-analysis. Microb Pathog. 2021;161: 105259.PubMedCrossRef Liao Y, Hong X, Wu A, Jiang Y, Liang Y, Gao J, et al. Global prevalence of norovirus in cases of acute gastroenteritis from 1997 to 2021: an updated systematic review and meta-analysis. Microb Pathog. 2021;161: 105259.PubMedCrossRef
2.
go back to reference Payne DC, Vinje J, Szilagyi PG, Edwards KM, Staat MA, Weinberg GA, et al. Norovirus and medically attended gastroenteritis in U.S. Children. N Engl J Med. 2013;368:1121–30.PubMedPubMedCentralCrossRef Payne DC, Vinje J, Szilagyi PG, Edwards KM, Staat MA, Weinberg GA, et al. Norovirus and medically attended gastroenteritis in U.S. Children. N Engl J Med. 2013;368:1121–30.PubMedPubMedCentralCrossRef
5.
go back to reference Teunis PFM, Moe CL, Liu P, Miller SE, Lindesmith L, Baric RS, et al. Norwalk virus: how infectious is it? J Med Virol. 2008;80:1468–76.PubMedCrossRef Teunis PFM, Moe CL, Liu P, Miller SE, Lindesmith L, Baric RS, et al. Norwalk virus: how infectious is it? J Med Virol. 2008;80:1468–76.PubMedCrossRef
6.
go back to reference Cates JE, Vinjé J, Parashar U, Hall AJ. Recent advances in human norovirus research and implications for candidate vaccines. Expert Rev Vaccines. 2020;19:539–48.PubMedCrossRef Cates JE, Vinjé J, Parashar U, Hall AJ. Recent advances in human norovirus research and implications for candidate vaccines. Expert Rev Vaccines. 2020;19:539–48.PubMedCrossRef
7.
go back to reference Ford-Siltz LA, Tohma K, Parra GI. Understanding the relationship between norovirus diversity and immunity. Gut microbes. 2021;13:1–13.PubMedCrossRef Ford-Siltz LA, Tohma K, Parra GI. Understanding the relationship between norovirus diversity and immunity. Gut microbes. 2021;13:1–13.PubMedCrossRef
8.
go back to reference Chan MCW, Lee N, Hung T-N, Kwok K, Cheung K, Tin EKY, et al. Rapid emergence and predominance of a broadly recognizing and fast-evolving norovirus GII.17 variant in late 2014. Nat Commun. 2015;6:10061.PubMedCrossRef Chan MCW, Lee N, Hung T-N, Kwok K, Cheung K, Tin EKY, et al. Rapid emergence and predominance of a broadly recognizing and fast-evolving norovirus GII.17 variant in late 2014. Nat Commun. 2015;6:10061.PubMedCrossRef
9.
go back to reference Zheng DP, Widdowson MA, Glass RI, Vinje J. Molecular epidemiology of genogroup II-genotype 4 noroviruses in the United States between 1994 and 2006. J Clin Microbiol. 2010;48:168–77.PubMedCrossRef Zheng DP, Widdowson MA, Glass RI, Vinje J. Molecular epidemiology of genogroup II-genotype 4 noroviruses in the United States between 1994 and 2006. J Clin Microbiol. 2010;48:168–77.PubMedCrossRef
10.
go back to reference de Graaf M, van Beek J, Vennema H, Podkolzin AT, Hewitt J, Bucardo F, et al. Emergence of a novel GII.17 norovirus—End of the GII.4 era? Euro Surveill. 2015;20:21178.PubMedCrossRef de Graaf M, van Beek J, Vennema H, Podkolzin AT, Hewitt J, Bucardo F, et al. Emergence of a novel GII.17 norovirus—End of the GII.4 era? Euro Surveill. 2015;20:21178.PubMedCrossRef
11.
go back to reference Parra GI, Squires RB, Karangwa CK, Johnson JA, Lepore CJ, Sosnovtsev SV, et al. Static and evolving norovirus genotypes: implications for epidemiology and immunity. Plos Patho. 2017;13: e1006136.CrossRef Parra GI, Squires RB, Karangwa CK, Johnson JA, Lepore CJ, Sosnovtsev SV, et al. Static and evolving norovirus genotypes: implications for epidemiology and immunity. Plos Patho. 2017;13: e1006136.CrossRef
12.
go back to reference Singh BK, Koromyslova A, Hefele L, Gurth C, Hansman GS. Structural evolution of the emerging 2014–2015 GII.17 noroviruses. J Virol. 2015;90:2710–5.PubMedCrossRef Singh BK, Koromyslova A, Hefele L, Gurth C, Hansman GS. Structural evolution of the emerging 2014–2015 GII.17 noroviruses. J Virol. 2015;90:2710–5.PubMedCrossRef
13.
go back to reference Jin M, Zhou YK, Xie HP, Fu JG, He YQ, Zhang S, et al. Characterization of the new GII.17 norovirus variant that emerged recently as the predominant strain in China. J Gen Virol. 2016;97:2620–32.PubMedPubMedCentralCrossRef Jin M, Zhou YK, Xie HP, Fu JG, He YQ, Zhang S, et al. Characterization of the new GII.17 norovirus variant that emerged recently as the predominant strain in China. J Gen Virol. 2016;97:2620–32.PubMedPubMedCentralCrossRef
14.
go back to reference Qian Y, Song M, Jiang X, Xia M, Meller J, Tan M, et al. Structural Adaptations of Norovirus GII.17/13/21 lineage through two distinct evolutionary paths. J Virol. 2019;93:e01655-01618.PubMed Qian Y, Song M, Jiang X, Xia M, Meller J, Tan M, et al. Structural Adaptations of Norovirus GII.17/13/21 lineage through two distinct evolutionary paths. J Virol. 2019;93:e01655-01618.PubMed
15.
16.
go back to reference Liu W-Q, Zhang L, Chen M, Li J. Cell-free protein synthesis: recent advances in bacterial extract sources and expanded applications. Biochem Eng J. 2019;141:182–9.CrossRef Liu W-Q, Zhang L, Chen M, Li J. Cell-free protein synthesis: recent advances in bacterial extract sources and expanded applications. Biochem Eng J. 2019;141:182–9.CrossRef
17.
go back to reference Endo Y, Sawasaki T. Cell-free expression systems for eukaryotic protein production. Curr Opin Biotech. 2006;17:373–80.PubMedCrossRef Endo Y, Sawasaki T. Cell-free expression systems for eukaryotic protein production. Curr Opin Biotech. 2006;17:373–80.PubMedCrossRef
18.
go back to reference Jackson K, Khnouf R, Fan ZH. Cell-free protein synthesis in microfluidic 96-well plates. Methods in Mol Biol (Clifton, NJ). 2014;1118:157–68.CrossRef Jackson K, Khnouf R, Fan ZH. Cell-free protein synthesis in microfluidic 96-well plates. Methods in Mol Biol (Clifton, NJ). 2014;1118:157–68.CrossRef
20.
go back to reference Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.PubMedPubMedCentralCrossRef Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.PubMedPubMedCentralCrossRef
22.
go back to reference Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21.PubMedCrossRef Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21.PubMedCrossRef
23.
go back to reference Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution. 2018;4(1):vey016.PubMedPubMedCentralCrossRef Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution. 2018;4(1):vey016.PubMedPubMedCentralCrossRef
24.
go back to reference Xue L, Dong R, Wu Q, Li Y, Cai W, Kou X, et al. Molecular epidemiology of noroviruses associated with sporadic gastroenteritis in Guangzhou, China, 2013–2015. Arch Virol. 2016;161:1377–84.PubMedCrossRef Xue L, Dong R, Wu Q, Li Y, Cai W, Kou X, et al. Molecular epidemiology of noroviruses associated with sporadic gastroenteritis in Guangzhou, China, 2013–2015. Arch Virol. 2016;161:1377–84.PubMedCrossRef
25.
go back to reference Xue L, Cai W, Wu Q, Zhang J, Guo W. Direct sequencing and analysis of the genomes of newly emerging GII17 norovirus strains in South China. J Appl Microbiol. 2016;120:1130–5.PubMedCrossRef Xue L, Cai W, Wu Q, Zhang J, Guo W. Direct sequencing and analysis of the genomes of newly emerging GII17 norovirus strains in South China. J Appl Microbiol. 2016;120:1130–5.PubMedCrossRef
26.
go back to reference Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics. 2006;22:195–201.PubMedCrossRef Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics. 2006;22:195–201.PubMedCrossRef
27.
go back to reference Lindesmith LC, Debbink K, Swanstrom J, Vinjé J, Costantini V, Baric RS, et al. Monoclonal antibody-based antigenic mapping of norovirus GII.4-2002. J Virol. 2012;86:873–83.PubMedPubMedCentralCrossRef Lindesmith LC, Debbink K, Swanstrom J, Vinjé J, Costantini V, Baric RS, et al. Monoclonal antibody-based antigenic mapping of norovirus GII.4-2002. J Virol. 2012;86:873–83.PubMedPubMedCentralCrossRef
28.
go back to reference Lindesmith LC, Brewer-Jensen PD, Mallory ML, Yount B, Collins MH, Debbink K, et al. Human Norovirus Epitope D plasticity allows escape from antibody immunity without loss of capacity for binding cellular ligands. J Virol. 2019;93:e01813-01818.PubMedPubMedCentralCrossRef Lindesmith LC, Brewer-Jensen PD, Mallory ML, Yount B, Collins MH, Debbink K, et al. Human Norovirus Epitope D plasticity allows escape from antibody immunity without loss of capacity for binding cellular ligands. J Virol. 2019;93:e01813-01818.PubMedPubMedCentralCrossRef
29.
go back to reference Sheng J, Lei S, Yuan L, Feng X. Cell-free protein synthesis of norovirus virus-like particles. RSC Adv. 2017;7:28837–40.CrossRef Sheng J, Lei S, Yuan L, Feng X. Cell-free protein synthesis of norovirus virus-like particles. RSC Adv. 2017;7:28837–40.CrossRef
30.
go back to reference Lindesmith LC, Kocher JF, Donaldson EF, Debbink K, Mallory ML, Swann EW, et al. Emergence of novel human norovirus GII.17 strains correlates with changes in blockade antibody epitopes. J Infect Dis. 2017;216:1227–34.PubMedPubMedCentralCrossRef Lindesmith LC, Kocher JF, Donaldson EF, Debbink K, Mallory ML, Swann EW, et al. Emergence of novel human norovirus GII.17 strains correlates with changes in blockade antibody epitopes. J Infect Dis. 2017;216:1227–34.PubMedPubMedCentralCrossRef
31.
go back to reference Tohma K, Lepore CJ, Ford-Siltz LA, Parra GI. Evolutionary dynamics of non-GII genotype 4 (GII.4) noroviruses reveal limited and independent diversification of variants. J Gen Virol. 2018;99:1027–35.PubMedCrossRef Tohma K, Lepore CJ, Ford-Siltz LA, Parra GI. Evolutionary dynamics of non-GII genotype 4 (GII.4) noroviruses reveal limited and independent diversification of variants. J Gen Virol. 2018;99:1027–35.PubMedCrossRef
32.
go back to reference Chen H, Qian F, Xu J, Chan M, Shen Z, Zai S, et al. A novel norovirus GII.17 lineage contributed to adult gastroenteritis in Shanghai, China, during the winter of 2014–2015. Emerg Microbes Infect. 2015;4:e67.PubMedPubMedCentral Chen H, Qian F, Xu J, Chan M, Shen Z, Zai S, et al. A novel norovirus GII.17 lineage contributed to adult gastroenteritis in Shanghai, China, during the winter of 2014–2015. Emerg Microbes Infect. 2015;4:e67.PubMedPubMedCentral
33.
go back to reference Xue L, Wu Q, Cai W, Zhang J, Guo W. Molecular characterization of new emerging GII.17 norovirus strains from South China. Infect Genet Evol. 2016;40:1–7.PubMedCrossRef Xue L, Wu Q, Cai W, Zhang J, Guo W. Molecular characterization of new emerging GII.17 norovirus strains from South China. Infect Genet Evol. 2016;40:1–7.PubMedCrossRef
34.
go back to reference Yi Y, Wang X, Wang S, Xiong P, Liu Q, Zhang C, et al. Identification of a blockade epitope of human norovirus GII.17. Emerg Microbes Infect. 2021;10:954–63.PubMedPubMedCentralCrossRef Yi Y, Wang X, Wang S, Xiong P, Liu Q, Zhang C, et al. Identification of a blockade epitope of human norovirus GII.17. Emerg Microbes Infect. 2021;10:954–63.PubMedPubMedCentralCrossRef
35.
go back to reference Debbink K, Donaldson EF, Lindesmith LC, Baric RS. Genetic mapping of a highly variable norovirus GII.4 blockade epitope: potential role in escape from human herd immunity. J Virol. 2012;86:1214–26.PubMedPubMedCentralCrossRef Debbink K, Donaldson EF, Lindesmith LC, Baric RS. Genetic mapping of a highly variable norovirus GII.4 blockade epitope: potential role in escape from human herd immunity. J Virol. 2012;86:1214–26.PubMedPubMedCentralCrossRef
36.
go back to reference Lindesmith LC, Costantini V, Swanstrom J, Debbink K, Donaldson EF, Vinjé J, et al. Emergence of a norovirus GII.4 strain correlates with changes in evolving blockade epitopes. J Virol. 2013;87:2803–13.PubMedPubMedCentralCrossRef Lindesmith LC, Costantini V, Swanstrom J, Debbink K, Donaldson EF, Vinjé J, et al. Emergence of a norovirus GII.4 strain correlates with changes in evolving blockade epitopes. J Virol. 2013;87:2803–13.PubMedPubMedCentralCrossRef
37.
go back to reference Allen DJ, Gray JJ, Gallimore CI, Xerry J, Iturriza-Gómara M. Analysis of amino acid variation in the P2 domain of the GII-4 norovirus VP1 protein reveals putative variant-specific epitopes. PLoS ONE. 2008;3: e1485.PubMedPubMedCentralCrossRef Allen DJ, Gray JJ, Gallimore CI, Xerry J, Iturriza-Gómara M. Analysis of amino acid variation in the P2 domain of the GII-4 norovirus VP1 protein reveals putative variant-specific epitopes. PLoS ONE. 2008;3: e1485.PubMedPubMedCentralCrossRef
38.
go back to reference Lindesmith LC, Costantini V, Swanstrom J, Debbink K, Donaldson EF, Vinje J, et al. Emergence of a norovirus GII.4 strain correlates with changes in evolving blockade epitopes. J Virol. 2013;87:2803–13.PubMedPubMedCentralCrossRef Lindesmith LC, Costantini V, Swanstrom J, Debbink K, Donaldson EF, Vinje J, et al. Emergence of a norovirus GII.4 strain correlates with changes in evolving blockade epitopes. J Virol. 2013;87:2803–13.PubMedPubMedCentralCrossRef
39.
go back to reference Debbink K, Lindesmith LC, Donaldson EF, Costantini V, Beltramello M, Corti D, et al. Emergence of new pandemic GII.4 Sydney norovirus strain correlates with escape from herd immunity. J Infect Dis. 2013;208:1877–87.PubMedPubMedCentralCrossRef Debbink K, Lindesmith LC, Donaldson EF, Costantini V, Beltramello M, Corti D, et al. Emergence of new pandemic GII.4 Sydney norovirus strain correlates with escape from herd immunity. J Infect Dis. 2013;208:1877–87.PubMedPubMedCentralCrossRef
40.
go back to reference Lindesmith LC, Donaldson EF, Baric RS. Norovirus GII.4 strain antigenic variation. J Virol. 2011;85:231–42.PubMedCrossRef Lindesmith LC, Donaldson EF, Baric RS. Norovirus GII.4 strain antigenic variation. J Virol. 2011;85:231–42.PubMedCrossRef
41.
go back to reference Xue L, Cai W, Gao J, Zhang L, Dong R, Li Y, et al. The resurgence of the norovirus GII.4 variant associated with sporadic gastroenteritis in the post-GII.7 period in South China, 2015 to 2017. BMC Infect Dis. 2019;19:696.PubMedPubMedCentralCrossRef Xue L, Cai W, Gao J, Zhang L, Dong R, Li Y, et al. The resurgence of the norovirus GII.4 variant associated with sporadic gastroenteritis in the post-GII.7 period in South China, 2015 to 2017. BMC Infect Dis. 2019;19:696.PubMedPubMedCentralCrossRef
42.
go back to reference Fiege B, Leuthold M, Parra F, Dalton KP, Meloncelli PJ, Lowary TL, et al. Epitope mapping of histo blood group antigens bound to norovirus VLPs using STD NMR experiments reveals fine details of molecular recognition. Glycoconjugate J. 2017;34:679–89.CrossRef Fiege B, Leuthold M, Parra F, Dalton KP, Meloncelli PJ, Lowary TL, et al. Epitope mapping of histo blood group antigens bound to norovirus VLPs using STD NMR experiments reveals fine details of molecular recognition. Glycoconjugate J. 2017;34:679–89.CrossRef
Metadata
Title
Rapid screening for antigenic characterization of GII.17 norovirus strains with variations in capsid gene
Authors
Yingyin Liao
Liang Xue
Junshan Gao
Yueting Zuo
Yanhui Liang
Yueting Jiang
Weicheng Cai
Jiale Yang
Jumei Zhang
Yu Ding
Moutong Chen
Aiwu Wu
Xiaoxia Kou
Qingping Wu
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2022
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-022-00504-1

Other articles of this Issue 1/2022

Gut Pathogens 1/2022 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.