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Full-length and defective enterovirus G genomes with distinct torovirus protease insertions are highly prevalent on a Chinese pig farm

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Abstract

Recombination occurs frequently between enteroviruses (EVs) which are classified within the same species of the Picornaviridae family. Here, using viral metagenomics, the genomes of two recombinant EV-Gs (strains EVG 01/NC_CHI/2014 and EVG 02/NC_CHI/2014) found in the feces of pigs from a swine farm in China are described. The two strains are characterized by distinct insertion of a papain-like protease gene from toroviruses classified within the Coronaviridae family. According to recent reports the site of the torovirus protease insertion was located at the 2C/3A junction region in EVG 02/NC_CHI/2014. For the other variant EVG 01/NC_CHI/2014, the inserted protease sequence replaced the entire viral capsid protein region up to the VP1/2A junction. These two EV-G strains were highly prevalent in the same pig farm with all animals shedding the full-length genome (EVG 02/NC_CHI/2014) while 65% also shed the capsid deletion mutant (EVG 01/NC_CHI/2014). A helper-defective virus relationship between the two co-circulating EV-G recombinants is hypothesized.

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Reference

  1. Anbalagan S, Hesse RA, Hause BM (2014) First identification and characterization of porcine enterovirus G in the United States. PLoS ONE 9:e97517

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Baez-Santos YM, Mielech AM, Deng X, Baker S, Mesecar AD (2014) Catalytic function and substrate specificity of the papain-like protease domain of nsp3 from the Middle East respiratory syndrome coronavirus. J Virol 88:12511–12527

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Blom N, Hansen J, Blaas D, Brunak S (1996) Cleavage site analysis in picornaviral polyproteins: discovering cellular targets by neural networks. Protein Sci 5:2203–2216

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Boros A, Pankovics P, Reuter G (2011) Characterization of a novel porcine enterovirus in domestic pig in Hungary. Infect Genet Evol 11:1096–1102

    Article  PubMed  CAS  Google Scholar 

  5. Boros A, Pankovics P, Knowles NJ, Reuter G (2012) Natural interspecies recombinant bovine/porcine enterovirus in sheep. J Gen Virol 93:1941–1951

    Article  PubMed  CAS  Google Scholar 

  6. Bunke J, Receveur K, Oeser AC, Fickenscher H, Zell R, Krumbholz A (2018) High genetic diversity of porcine enterovirus G in Schleswig-Holstein, Germany. Adv Virol 163:489–493

    CAS  Google Scholar 

  7. Conceicao-Neto N, Theuns S, Cui T, Zeller M, Yinda CK, Christiaens I, Heylen E, Van Ranst M, Carpentier S, Nauwynck HJ, Matthijnssens J (2017) Identification of an enterovirus recombinant with a torovirus-like gene insertion during a diarrhea outbreak in fattening pigs. VIRUS Evol 3:vex024

    Article  PubMed  PubMed Central  Google Scholar 

  8. Deng X, Naccache SN, Ng T, Federman S, Li L, Chiu CY, Delwart EL (2015) An ensemble strategy that significantly improves de novo assembly of microbial genomes from metagenomic next-generation sequencing data. Nucleic Acids Res 43:e46

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Kitamura N, Adler C, Wimmer E (1980) Structure and expression of the picornavirus genome. Ann N Y Acad Sci 354:183–201

    Article  PubMed  CAS  Google Scholar 

  10. Knutson TP, Velayudhan BT, Marthaler DG (2017) A porcine enterovirus G associated with enteric disease contains a novel papain-like cysteine protease. J Gen Virol 98:1305–1310

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Li J, Chai QY, Liu CH (2016) The ubiquitin system: a critical regulator of innate immunity and pathogen-host interactions. Cell Mol Immunol 13:560–576

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Martinez-Salas E, Fernandez-Miragall O (2004) Picornavirus IRES: structure function relationship. Curr Pharm Des 10:3757–3767

    Article  PubMed  CAS  Google Scholar 

  13. Mielech AM, Chen Y, Mesecar AD, Baker SC (2014) Nidovirus papain-like proteases: multifunctional enzymes with protease, deubiquitinating and deISGylating activities. Virus Res 194:184–190

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Shang P, Misra S, Hause B, Fang Y (2017) A naturally occurring recombinant enterovirus expresses a torovirus deubiquitinase. J Virol 91:e00450

    Article  PubMed  PubMed Central  Google Scholar 

  15. Sulea T, Lindner HA, Purisima EO, Menard R (2005) Deubiquitination, a new function of the severe acute respiratory syndrome coronavirus papain-like protease? J Virol 79:4550–4551

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Sun Z, Li Y, Ransburgh R, Snijder EJ, Fang Y (2012) Nonstructural protein 2 of porcine reproductive and respiratory syndrome virus inhibits the antiviral function of interferon-stimulated gene 15. J Virol 86:3839–3850

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Van Dung N, Anh PH, Van Cuong N, Hoa NT, Carrique-Mas J, Hien VB, Campbell J, Baker S, Farrar J, Woolhouse ME, Bryant JE, Simmonds P (2014) Prevalence, genetic diversity and recombination of species G enteroviruses infecting pigs in Vietnam. J Gen Virol 95:549–556

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Villarroya-Beltri C, Guerra S, Sanchez-Madrid F (2017) ISGylation - a key to lock the cell gates for preventing the spread of threats. J Cell Sci 130:2961–2969

    Article  PubMed  CAS  Google Scholar 

  19. Yang S, Wang Y, Shen Q, Zhang W, Hua X (2013) Prevalence of porcine enterovirus 9 in pigs in middle and eastern China. Virol J 10:99

    Article  PubMed  PubMed Central  Google Scholar 

  20. Yang X, Chen X, Bian G, Tu J, Xing Y, Wang Y, Chen Z (2014) Proteolytic processing, deubiquitinase and interferon antagonist activities of Middle East respiratory syndrome coronavirus papain-like protease. J Gen Virol 95:614–626

    Article  PubMed  CAS  Google Scholar 

  21. Zell R, Sidigi K, Henke A, Schmidt-Brauns J, Hoey E, Martin S, Stelzner A (1999) Functional features of the bovine enterovirus 5’-non-translated region. J Gen Virol 80(Pt 9):2299–2309

    Article  PubMed  CAS  Google Scholar 

  22. Zell R, Delwart E, Gorbalenya AE, Hovi T, King AMQ, Knowles NJ, Lindberg AM, Pallansch MA, Palmenberg AC, Reuter G, Simmonds P, Skern T, Stanway G, Yamashita T, Ictv Report C (2017) ICTV virus taxonomy profile: picornaviridae. J Gen Virol 98:2421–2422

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Zhang W, Yang S, Shen Q, Ren L, Shan T, Wei J, Cui L, Hua X (2012) Complete genome sequence of a novel porcine enterovirus strain in China. J Virol 86:7008–7009

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Zhang W, Li L, Deng X, Kapusinszky B, Pesavento PA, Delwart E (2014) Faecal virome of cats in an animal shelter. J Gen Virol 95:2553–2564

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Zoll J, Heus HA, van Kuppeveld FJ, Melchers WJ (2009) The structure-function relationship of the enterovirus 3’-UTR. Virus Res 139:209–216

    Article  PubMed  CAS  Google Scholar 

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Funding

This work was supported by National Key Research and Development Programs of China No. 2017YFC1200201, Jiangsu Provincial Key Research and Development Projects No. BE2017693, the National Natural Science Foundation of China No. 31402211, and the Professional Research Foundation for Advanced Talents of Jiangsu University No. 12JDG085 and 13JDG087, the Postdoctoral Foundation of Jiangsu Province No. 1302057C and 1302058C.

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Authors and Affiliations

  1. School of Medicine, Jiangsu University, Zhenjiang, 212013, Jiangsu, People’s Republic of China

    Yan Wang, Wen Zhang, Zhijian Liu, Xingli Fu, Jiaqi Yuan, Jieji Zhao, Quan Shen, Xiaochun Wang & Shixing Yang

  2. School of Basic Medical Sciences, Ningxia Medical University, Yinchuan, 750000, Ningxia, People’s Republic of China

    Yuan Lin

  3. Blood Systems Research Institute, San Francisco, California, USA

    Xutao Deng & Eric Delwart

  4. Department of Swine Infectious Disease, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai, 200241, People’s Republic of China

    Tongling Shan

  5. School of Medicine, Jiangsu University, 301 Xuefu Road, Zhenjiang, 200240, Jiangsu, People’s Republic of China

    Shixing Yang

Authors
  1. Yan Wang
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  2. Wen Zhang
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  3. Zhijian Liu
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  4. Xingli Fu
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  7. Yuan Lin
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  8. Quan Shen
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  9. Xiaochun Wang
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  10. Xutao Deng
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  11. Eric Delwart
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  12. Tongling Shan
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  13. Shixing Yang
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Corresponding authors

Correspondence to Tongling Shan or Shixing Yang.

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The authors declare that they have no competing interests.

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The research reported here did not involve experimentation with human participants or animals.

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Handling Editor: Ayato Takada.

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Wang, Y., Zhang, W., Liu, Z. et al. Full-length and defective enterovirus G genomes with distinct torovirus protease insertions are highly prevalent on a Chinese pig farm. Arch Virol 163, 2471–2476 (2018). https://doi.org/10.1007/s00705-018-3875-x

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  • DOI: https://doi.org/10.1007/s00705-018-3875-x

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