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An Effective Platform for Exploring Rotavirus Receptors by Bacterial Surface Display System

  • Danlei Liu
  • Haoran Geng
  • Zilei Zhang
  • Yifan Xing
  • Danlu Yang
  • Zhicheng Liu
  • Dapeng WangEmail author
RESEARCH ARTICLE

Abstract

Rotavirus (RV) is a major foodborne pathogen. For RV prevention and control, it is a key to uncover the interaction mechanism between virus and its receptors. However, it is hard to specially purify the viral receptors, including histo-blood group antigens (HBGAs). Previously, the protruding domain protein (P protein) of human norovirus (genotype II.4) was displayed on the surface of Escherichia coli, and it specifically recognized and captured the viral ligands. In order to further verify the feasibility of the system, P protein was replaced by VP8* of RV (G9P[8]) in this study. In the system, VP8* could be correctly released by thrombin treatment with antigenicity retaining, which was confirmed by Western blot and Enzyme-Linked Immunosorbent Assays. Type A HBGAs from porcine gastric mucin (PGM) were recognized and captured by this system. From saliva mixture, the captured viral receptor bound with displayed VP8* was confirmed positive with monoclonal antibody against type A HBGAs. It indicated that the target ligands could be easily separated from the complex matrix. These results demonstrate that the bacterial surface display system will be an effective platform to explore viral receptors/ligands from cell lines or food matrix.

Keywords

Rotavirus Bacterial surface display system Receptors Histo-blood group antigens (HBGAs) Saliva 

Notes

Acknowledgements

This work was jointly supported by the National Key Research and Development Program of China (2017YFF0210200) and the National Natural Science Foundation of China (31772078).

Author Contributions

DL and DW performed the experiments, DL, HG, ZZ and DW analyzed results and wrote the manuscript. DL, HG, ZZ, YX, DY and DW contributed to experimental design and carried out part of the experiments. All authors read and approved the final manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Animal and Human Rights Statement

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

  1. Baker M, Prasad B (2010) Rotavirus cell entry. Curr Top Microbiol Immunol 343:121–148PubMedGoogle Scholar
  2. Barbé L, Le Moullac-Vaidye B, Echasserieau K, Bernardeau K, Carton T, Bovin N, Le Pendu J (2018) Histo-blood group antigen-binding specificities of human rotaviruses are associated with gastroenteritis but not with in vitro infection. Sci Rep 8(1):12961–12974CrossRefGoogle Scholar
  3. Böhm R, Fleming F, Maggioni A, Dang V, Holloway G, Coulson B, von Itzstein M, Haselhorst T (2015) Revisiting the role of histo-blood group antigens in rotavirus host-cell invasion. Nat Commun 6:1–12CrossRefGoogle Scholar
  4. Fleming F, Graham K, Takada Y, Coulson B (2011) Determinants of the specificity of rotavirus interactions with the α2β1 integrin. J Biol Chem 286:6165–6174CrossRefGoogle Scholar
  5. Graham K, Halasz P, Tan Y, Hewish M, Takada Y, Mackow E, Robinson M, Coulson B (2003) Integrin-using rotaviruses bind α2β1 integrin α2 I domain via VP4 DGE sequence and recognize αXβ2 and αVβ3 by using VP7 during cell entry. J Virol 77(18):9969–9978CrossRefGoogle Scholar
  6. Grove J, Marsh M (2011) The cell biology of receptor-mediated virus entry. J Cell Biol 195:1071–1082CrossRefGoogle Scholar
  7. Guo C, Nakagomi O, Mochizuki M, Ishida H, Kiso M, Ohta Y, Suzuki T, Miyamoto D, Hidari K, Suzuki Y (1999) Ganglioside GM1a on the cell surface is involved in the infection by human rotavirus KUN and MO strains. J Biochem 126:683–688CrossRefGoogle Scholar
  8. Harrington P, Vinje J, Moe C, Baric R (2004) Norovirus capture with histo-blood group antigens reveals novel virus-ligand interactions. J Virol 78:3035–3045CrossRefGoogle Scholar
  9. Hewish M, Takada Y, Coulson B (2000) Integrins α2β1 and α4β1 can mediate SA11 rotavirus attachment and entry into cells. J Virol 74:228–236CrossRefGoogle Scholar
  10. Howley P, Knipe D (eds) (2001) Fundamental virology. Lippincott Williams & Wilkins, PhiladelphiaGoogle Scholar
  11. Hu L, Crawford S, Czako R, Cortes-Penfield N, Smith D, Le Pendu J, Estes M, Prasad B (2012) Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 485:256–259CrossRefGoogle Scholar
  12. Huang P, Xia M, Tan M, Zhong W, Wei C, Wang L, Morrow A, Jiang X (2012) Spike protein VP8* of human rotavirus recognizes histo-blood group antigens in a type-specific manner. J Virol 86:4833–4843CrossRefGoogle Scholar
  13. Ilver D, Arnqvist A, Ogren J, Frick I, Kersulyte D, Incecik E, Berg D, Covacci A, Engstrand L, Boren T (1998) Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279:373–377CrossRefGoogle Scholar
  14. Iša P, Realpe M, Romero P, López S, Arias C (2004) Rotavirus RRV associates with lipid membrane microdomains during cell entry. Virology 322:370–381CrossRefGoogle Scholar
  15. Lee J, Shin K, Pan J, Kim C (2000) Surface-displayed viral antigens on Salmonella carrier vaccine. Nat Biotechnol 18:645–648CrossRefGoogle Scholar
  16. Lee B, Dickson DM, decamp AC, Colgate ER, Diehl SA, Uddin MI, Sharmin S, Islam S, Bhuiyan TR, Alam M, Nayak U, Mychaleckyj JC, Taniuchi M, Petri WA Jr, Haque R, Qadri F, Kirkpatrick BD (2018) Histo–Blood group antigen phenotype determines susceptibility to genotype-specific Rotavirus infections and impacts measures of Rotavirus vaccine efficacy. J Infect Dis 217:1399–1407CrossRefGoogle Scholar
  17. Li Q, Yu Z, Shao X, He J, Li L (2010) Improved phosphate biosorption by bacterial surface display of phosphate-binding protein utilizing ice nucleation protein. FEMS Microbiol Lett 299:44–52CrossRefGoogle Scholar
  18. Li Q, Yan Q, Chen J, He Y, Wang J, Zhang H, Yu Z, Li L (2012) Molecular characterization of an ice nucleation protein variant (inaQ) from Pseudomonas syringae and the analysis of its transmembrane transport activity in Escherichia coli. Int J Biol Sci 8:1097–1108CrossRefGoogle Scholar
  19. López S, Arias C (2004) Multistep entry of rotavirus into cells: a versailles que dance. Trends Microbiol 12:271–278CrossRefGoogle Scholar
  20. Matthijnssens J, Ciarlet M, McDonald S, Attoui H, Bányai K, Brister J, Buesa J, Esona M, Estes M, Gentsch J, Iturriza-Gómara M, Johne R, Kirkwood C, Martella V, Mertens P, Nakagomi O, Parreño V, Rahman M, Ruggeri F, Saif L, Santos N, Steyer A, Taniguchi K, Patton J, Desselberger U, Van Ranst M (2011) Uniformity of rotavirus strain nomenclature proposed by the rotavirus classification working group (RCWG). Adv Virol 156:1397–1413Google Scholar
  21. Méndez E, López S, Cuadras M, Romero P, Arias C (1999) Entry of rotaviruses is a multistep process. Virology 263:450–459CrossRefGoogle Scholar
  22. Nakagomi T, Nakagomi O (2009) A critical review on a globally-licensed, live, orally-administrable, monovalent human rotavirus vaccine: rotarix. Expert Opin Biol Ther 9:1073–1086CrossRefGoogle Scholar
  23. Nguyen T, Yagyu F, Okame M, Phan T, Trinh Q, Yan H, Hoang K, Cao A, Le H, Okitsu S (2007) Diversity of viruses associated with acute gastroenteritis in children hospitalized with diarrhea in Ho Chi Minh City, Vietnam. J Med Virol 79:582–590CrossRefGoogle Scholar
  24. Niu M, Yu Q, Tian P, Gao Z, Wang D, Shi X (2015) Engineering bacterial surface displayed human norovirus capsid proteins: a novel system to explore interaction between norovirus and ligands. Front Microbiol 6:1448–1454CrossRefGoogle Scholar
  25. Nordgren J, Sharma S, Bucardo F, Nasir W, Günaydın G, Ouermi D, Nitiema LW, Becker-Dreps S, Simpore J, Hammarström L, Larson G, Svensson L (2014) Both Lewis and secretor status mediate susceptibility to rotavirus infections in a rotavirus genotype-dependent manner. Clin Infect Dis 59:1567–1573CrossRefGoogle Scholar
  26. Patel M, Widdowson M, Glass R, Akazawa K, Vinjé J, Parashar UD (2008) Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14:1224–1231CrossRefGoogle Scholar
  27. Patton J (2012) Rotavirus diversity and evolution in the post-vaccine world. Discovery Medicine 13:85–97PubMedPubMedCentralGoogle Scholar
  28. Patton J, Hua J, Mansell E (1993) Location of intrachain disulfide bonds in the VP5* and VP8* trypsin cleavage fragments of the rhesus rotavirus spike protein VP4. J Virol 67:4848–4855PubMedPubMedCentralGoogle Scholar
  29. Qiao H, Nilsson M, Abreu E, Hedlund K, Johansen K, Zaori G, Svensson L (1999) Viral diarrhea in children in Beijing, China. J Med Virol 57:390–396CrossRefGoogle Scholar
  30. Sugiyama M, Goto K, Uemukai H, Mori Y, Ito N, Minamoto N (2004) Attachment and infection to MA104 cells of avian rotaviruses require the presence of sialic acid on the cell surface. J Vet Med Sci 66:461–463CrossRefGoogle Scholar
  31. Tran A, Talmud D, Lejeune B, Jovenin N, Renois F, Payan C, Leveque N, Andreoletti L (2010) Prevalence of rotavirus, adenovirus, norovirus, and astrovirus infections and coinfections among hospitalized children in Northern France. J Clin Microbiol 48(5):1943–1946CrossRefGoogle Scholar
  32. Trask S, Kim I, Harrison S, Dormitzer P (2010) A rotavirus spike protein conformational intermediate binds lipid bilayers. J Virol 84:1764–1770CrossRefGoogle Scholar
  33. Troeger C, Khalil I, Rao P, Cao S, Blacker B, Ahmed T, Armah G, Bines J, Brewer T, Colombara D, Kang G, Kirkpatrick B, Kirkwood C, Mwenda J, Parashar U, Petri W, Riddle M, Steele A, Thompson R, Walson J, Sanders J, Mokdad A, Murray CJ, Hay S, Reiner R (2018) Rotavirus vaccination and the global burden of rotavirus diarrhea among children younger than 5 years. JAMA Pediatr 172:958–965CrossRefGoogle Scholar
  34. Wang M, Rong S, Tian P, Zhou Y, Guan S, Li Q, Wang D (2017) Bacterial surface-displayed GII.4 human norovirus capsid proteins bound to HBGA-like molecules in romaine lettuce. Front Microbiol 8:251–259PubMedPubMedCentralGoogle Scholar
  35. Xu Q, Ni P, Liu D, Yin Y, Li Q, Zhang J, Wu Q, Tian P, Shi X, Wang D (2017) A bacterial surface display system expressing cleavable capsid proteins of human norovirus: a novel system to discover candidate receptors. Front Microbiol 8:2405–2413CrossRefGoogle Scholar
  36. Yolken R, Willoughby R, Wee S, Miskuff R, Vonderfecht S (1987) Sialic acid glycoproteins inhibit in vitro and in vivo replication of rotaviruses. J Clin Investig 79:148–154CrossRefGoogle Scholar
  37. Zarate S, Cuadras MA, Espinosa R, Romero P, Juarez K, Camacho-Nuez M, Arias C, Lopez S (2003) Interaction of rotaviruses with HSC70 during cell entry is mediated by VP5. J Virol 77:7254–7260CrossRefGoogle Scholar

Copyright information

© Wuhan Institute of Virology, CAS 2019

Authors and Affiliations

  1. 1.Department of Food Science and Technology, School of Agriculture and BiologyShanghai Jiao Tong UniversityShanghaiChina
  2. 2.State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied MicrobiologyGuangdong Institute of MicrobiologyGuangzhouChina
  3. 3.Shanghai Food Safety and Engineering Technology Research Center, School of Agriculture and BiologyShanghai Jiao Tong UniversityShanghaiChina

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