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Citation: Danlei Liu, Haoran Geng, Zilei Zhang, Yifan Xing, Danlu Yang, Zhicheng Liu, Dapeng Wang. An Effective Platform for Exploring Rotavirus Receptors by Bacterial Surface Display System [J].VIROLOGICA SINICA, 2020, 35(1) : 103-109.  http://dx.doi.org/10.1007/s12250-019-00174-5

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

  • Corresponding author: Dapeng Wang, dapengwang@sjtu.edu.cn, ORCID: http://orcid.org/0000-0001-5794-8861
  • Received Date: 28 March 2019
    Accepted Date: 28 August 2019
    Published Date: 27 November 2019
    Available online: 01 February 2020
  • 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.

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    1. Baker M, Prasad B (2010) Rotavirus cell entry. Curr Top Microbiol Immunol 343:121–148

    2. BarbéL, 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):12961–12974
        doi: 10.1038/s41598-018-31005-4

    3. Böhm R, Fleming F, Maggioni A, Dang V, Holloway G, Coulson B, von Itzstein M, Haselhorst T (2015) Revisiting the role of histoblood group antigens in rotavirus host-cell invasion. Nat Commun 6:1–12
        doi: 10.1038/ncomms6907

    4. Fleming F, Graham K, Takada Y, Coulson B (2011) Determinants of the specificity of rotavirus interactions with the a2b1 integrin. J Biol Chem 286:6165–6174
        doi: 10.1074/jbc.M110.142992

    5. Graham K, Halasz P, Tan Y, Hewish M, Takada Y, Mackow E, Robinson M, Coulson B (2003) Integrin-using rotaviruses bind a2b1 integrin a2 I domain via VP4 DGE sequence and recognize aXb2 and aVb3 by using VP7 during cell entry. J Virol 77(18):9969–9978
        doi: 10.1128/JVI.77.18.9969-9978.2003

    6. Grove J, Marsh M (2011) The cell biology of receptor-mediated virus entry. J Cell Biol 195:1071–1082
        doi: 10.1083/jcb.201108131

    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 126:683–688
        doi: 10.1093/oxfordjournals.jbchem.a022503

    8. Harrington P, Vinje J, Moe C, Baric R (2004) Norovirus capture with histo-blood group antigens reveals novel virus-ligand interactions. J Virol 78:3035–3045
        doi: 10.1128/JVI.78.6.3035-3045.2004

    9. Hewish M, Takada Y, Coulson B (2000) Integrins a2b1 and a4b1 can mediate SA11 rotavirus attachment and entry into cells. J Virol 74:228–236
        doi: 10.1128/JVI.74.1.228-236.2000

    10. Howley P, Knipe D (eds) (2001) Fundamental virology. Lippincott Williams & Wilkins, Philadelphia

    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 485:256–259
        doi: 10.1038/nature10996

    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 86:4833–4843
        doi: 10.1128/JVI.05507-11

    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 279:373–377
        doi: 10.1126/science.279.5349.373

    14. Iša P, Realpe M, Romero P, López S, Arias C (2004) Rotavirus RRV associates with lipid membrane microdomains during cell entry. Virology 322:370–381
        doi: 10.1016/j.virol.2004.02.018

    15. Lee J, Shin K, Pan J, Kim C (2000) Surface-displayed viral antigens on Salmonella carrier vaccine. Nat Biotechnol 18:645–648
        doi: 10.1038/76494

    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 217:1399–1407
        doi: 10.1093/infdis/jiy054

    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 299:44–52
        doi: 10.1111/j.1574-6968.2009.01724.x

    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 8:1097–1108
        doi: 10.7150/ijbs.4524

    19. López S, Arias C (2004) Multistep entry of rotavirus into cells: a versailles que dance. Trends Microbiol 12:271–278
        doi: 10.1016/j.tim.2004.04.003

    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 156:1397–1413

    21. Méndez E, López S, Cuadras M, Romero P, Arias C (1999) Entry of rotaviruses is a multistep process. Virology 263:450–459
        doi: 10.1006/viro.1999.9976

    22. Nakagomi T, Nakagomi O (2009) A critical review on a globallylicensed, live, orally-administrable, monovalent human rotavirus vaccine: rotarix. Expert Opin Biol Ther 9:1073–1086
        doi: 10.1517/14712590903103787

    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 79:582–590
        doi: 10.1002/jmv.20857

    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 6:1448–1454
        doi: 10.1016/j.micinf.2011.04.004

    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 59:1567–1573
        doi: 10.1093/cid/ciu633

    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 14:1224–1231
        doi: 10.3201/eid1408.071114

    27. Patton J (2012) Rotavirus diversity and evolution in the post-vaccine world. Discovery Medicine 13:85–97

    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 67:4848–4855
        doi: 10.1128/JVI.67.8.4848-4855.1993

    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 57:390–396
        doi: 10.1002/(SICI)1096-9071(199904)57:4<390::AID-JMV11>3.0.CO;2-0

    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 66:461–463
        doi: 10.1292/jvms.66.461

    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):1943–1946
        doi: 10.1128/JCM.02181-09

    32. Trask S, Kim I, Harrison S, Dormitzer P (2010) A rotavirus spike protein conformational intermediate binds lipid bilayers. J Virol 84:1764–1770
        doi: 10.1128/JVI.01682-09

    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 172:958–965
        doi: 10.1001/jamapediatrics.2018.1960

    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 8:251–259
        doi: 10.3389/fmicb.2017.00251

    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 8:2405–2413
        doi: 10.3389/fmicb.2017.02405

    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 79:148–154
        doi: 10.1172/JCI112775

    37. Zarate S, Cuadras MA, Espinosa R, Romero P, Juarez K, CamachoNuez M, Arias C, Lopez S (2003) Interaction of rotaviruses with HSC70 during cell entry is mediated by VP5. J Virol 77:7254–7260
        doi: 10.1128/JVI.77.13.7254-7260.2003

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

      Corresponding author: Dapeng Wang, dapengwang@sjtu.edu.cn
    • 1. Department of Food Science and Technology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China
    • 2. State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangdong Institute of Microbiology, Guangzhou 510070, China
    • 3. Shanghai Food Safety and Engineering Technology Research Center, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China

    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.