Abstract
Recently, NADC30-like porcine reproductive and respiratory syndrome viruses (PRRSVs), which are genetically similar to the NADC30 strain isolated in the United States of America in 2008, have become prevalent in China. Here, a novel variant PRRSV strain named HNhx was successfully isolated on porcine alveolar macrophages from Henan province and the full-length genome sequence was determined. Phylogenetic analysis indicated that HNhx strain was classified into the NADC30-like PRRSV subgroup, in which all the strains had the unique discontinuous 131-amino acid deletion relative to that of the nonstructural protein 2 (Nsp2) of the VR2332 strain. Genetically, HNhx shared 92.9% nucleotide similarity to NADC30. Furthermore, HNhx strain contained extensive amino acid mutations in GP5. In particular, the S32H, N33D, D34N, and S36G variations resulted in that HNhx lost all the putative N-linked glycosylation sites at amino acid positions 30, 32, 33, 34, and 35. Recombination analysis revealed that HNhx was the result of recombination between the NADC30 strain and the highly pathogenic PRRSV vaccine strain circulating in China in Nsp4 (nt 5261) to Nsp9 (nt 7911). The novel genome data of HNhx will be helpful for understanding the evolution and epidemiology of PRRSV in China.
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References
R. Allende, G.F. Kutish, W. Laegreid, Z. Lu, T.L. Lewis, D.L. Rock, J. Friesen, J.A. Galeota, A.R. Doster, F.A. Osorio, Mutations in the genome of porcine reproductive and respiratory syndrome virus responsible for the attenuation phenotype. Adv. Virol. 145, 1149–1161 (2000)
R. Allende, T.L. Lewis, Z. Lu, D.L. Rock, G.F. Kutish, A. Ali, A.R. Doster, F.A. Osorio, North American and European porcine reproductive and respiratory syndrome viruses differ in non-structural protein coding regions. J. Gen. Virol. 80(Pt 2), 307–315 (1999)
X. Bai, Y. Wang, X. Xu, Z. Sun, Y. Xiao, G. Ji, Y. Li, F. Tan, X. Li, K. Tian, Commercial vaccines provide limited protection to NADC30-like PRRSV infection. Vaccine 34, 5540–5545 (2016)
S.L. Brockmeier, C.L. Loving, A.C. Vorwald, M.E. Kehrli Jr., R.B. Baker, T.L. Nicholson, K.M. Lager, L.C. Miller, K.S. Faaberg, Genomic sequence and virulence comparison of four Type 2 porcine reproductive and respiratory syndrome virus strains. Virus Res. 169, 212–221 (2012)
K.K. Conzelmann, N. Visser, P. Van Woensel, H.J. Thiel, Molecular characterization of porcine reproductive and respiratory syndrome virus, a member of the arterivirus group. Virology 193, 329–339 (1993)
M. de Lima, A.K. Pattnaik, E.F. Flores, F.A. Osorio, Serologic marker candidates identified among B-cell linear epitopes of Nsp2 and structural proteins of a North American strain of porcine reproductive and respiratory syndrome virus. Virology 353, 410–421 (2006)
S. Dea, C.A. Gagnon, H. Mardassi, B. Pirzadeh, D. Rogan, Current knowledge on the structural proteins of porcine reproductive and respiratory syndrome (PRRS) virus: comparison of the North American and European isolates. Adv. Virol. 145, 659–688 (2000)
A.E. Firth, J.C. Zevenhoven-Dobbe, N.M. Wills, Y.Y. Go, U.B. Balasuriya, J.F. Atkins, E.J. Snijder, C.C. Posthuma, Discovery of a small arterivirus gene that overlaps the GP5 coding sequence and is important for virus production. J. Gen. Virol. 92, 1097–1106 (2011)
C.R. Johnson, T.F. Griggs, J. Gnanandarajah, M.P. Murtaugh, Novel structural protein in porcine reproductive and respiratory syndrome virus encoded by an alternative ORF5 present in all arteriviruses. J. Gen. Virol. 92, 1107–1116 (2011)
J.H. Kuhn, M. Lauck, A.L. Bailey, A.M. Shchetinin, T.V. Vishnevskaya, Y. Bao, T.F. Ng, M. LeBreton, B.S. Schneider, A. Gillis, U. Tamoufe, D. Diffo Jle, J.M. Takuo, N.O. Kondov, L.L. Coffey, N.D. Wolfe, E. Delwart, A.N. Clawson, E. Postnikova, L. Bollinger, M.G. Lackemeyer, S.R. Radoshitzky, G. Palacios, J. Wada, Z.V. Shevtsova, P.B. Jahrling, B.A. Lapin, P.G. Deriabin, M. Dunowska, S.V. Alkhovsky, J. Rogers, T.C. Friedrich, D.H. O’Connor, T.L. Goldberg, Reorganization and expansion of the nidoviral family Arteriviridae. Adv. Virol. 161, 755–768 (2016)
B. Kwon, I.H. Ansari, A.K. Pattnaik, F.A. Osorio, Identification of virulence determinants of porcine reproductive and respiratory syndrome virus through construction of chimeric clones. Virology 380, 371–378 (2008)
B. Li, L. Fang, X. Guo, J. Gao, T. Song, J. Bi, K. He, H. Chen, S. Xiao, Epidemiology and evolutionary characteristics of the porcine reproductive and respiratory syndrome virus in China between 2006 and 2010. J. Clin. Microbiol. 49, 3175–3183 (2011)
Y. Li, G. Ji, J. Wang, F. Tan, J. Zhuang, X. Li, K. Tian, Complete genome sequence of an NADC30-like porcine reproductive and respiratory syndrome virus characterized by recombination with other strains. Genome Announc. 4(3), e00330 (2016)
Y. Li, L. Zhou, J. Zhang, X. Ge, R. Zhou, H. Zheng, G. Geng, X. Guo, H. Yang, Nsp9 and Nsp10 contribute to the fatal virulence of highly pathogenic porcine reproductive and respiratory syndrome virus emerging in China. PLoS Pathog. 10, e1004216 (2014)
W.H. Lu, H.M. Tun, B.L. Sun, J. Mo, Q.F. Zhou, Y.X. Deng, Q.M. Xie, Y.Z. Bi, F.C. Leung, J.Y. Ma, Re-emerging of porcine respiratory and reproductive syndrome virus (lineage 3) and increased pathogenicity after genomic recombination with vaccine variant. Vet. Microbiol. 175, 332–340 (2015)
J.K. Lunney, D.A. Benfield, R.R. Rowland, Porcine reproductive and respiratory syndrome virus: an update on an emerging and re-emerging viral disease of swine. Virus Res. 154, 1–6 (2010)
J.J. Meulenberg, M.M. Hulst, E.J. de Meijer, P.L. Moonen, A. den Besten, E.P. de Kluyver, G. Wensvoort, R.J. Moormann, Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV. Virology 192, 62–72 (1993)
J.J. Meulenberg, A. Petersen-den Besten, Identification and characterization of a sixth structural protein of Lelystad virus: the glycoprotein GP2 encoded by ORF2 is incorporated in virus particles. Virology 225, 44–51 (1996)
J.J. Meulenberg, A. Petersen-den Besten, E.P. De Kluyver, R.J. Moormann, W.M. Schaaper, G. Wensvoort, Characterization of proteins encoded by ORFs 2 to 7 of Lelystad virus. Virology 206, 155–163 (1995)
C. Mu, X. Lu, E. Duan, J. Chen, W. Li, F. Zhang, D.P. Martin, M. Yang, P. Xia, B. Cui, Molecular evolution of porcine reproductive and respiratory syndrome virus isolates from central China. Res. Vet. Sci. 95, 908–912 (2013)
C.J. Nelsen, M.P. Murtaugh, K.S. Faaberg, Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J. Virol. 73, 270–280 (1999)
E.A. Nelson, J. Christopher-Hennings, T. Drew, G. Wensvoort, J.E. Collins, D.A. Benfield, Differentiation of U.S. and European isolates of porcine reproductive and respiratory syndrome virus by monoclonal antibodies. J. Clin. Microbiol. 31, 3184–3189 (1993)
L.N. Popescu, B.R. Trible, N. Chen, R.R.R. Rowland, GP5 of porcine reproductive and respiratory syndrome virus (PRRSV) as a target for homologous and broadly neutralizing antibodies. Vet. Microbiol. 209, 90–96 (2017)
M. Shi, E.C. Holmes, M.S. Brar, F.C. Leung, Recombination is associated with an outbreak of novel highly pathogenic porcine reproductive and respiratory syndrome viruses in China. J. Virol. 87, 10904–10907 (2013)
M. Shi, T.T. Lam, C.C. Hon, R.K. Hui, K.S. Faaberg, T. Wennblom, M.P. Murtaugh, T. Stadejek, F.C. Leung, Molecular epidemiology of PRRSV: a phylogenetic perspective. Virus Res. 154, 7–17 (2010)
E.J. Snijder, J.J. Meulenberg, The molecular biology of arteriviruses. J. Gen. Virol. 79(Pt 5), 961–979 (1998)
Z. Sun, J. Wang, X. Bai, G. Ji, H. Yan, Y. Li, Y. Wang, F. Tan, Y. Xiao, X. Li, K. Tian, Pathogenicity comparison between highly pathogenic and NADC30-like porcine reproductive and respiratory syndrome virus. Adv. Virol. 161, 2257–2261 (2016)
B. Thaa, B.C. Sinhadri, C. Tielesch, E. Krause, M. Veit, Signal peptide cleavage from GP5 of PRRSV: a minor fraction of molecules retains the decoy epitope, a presumed molecular cause for viral persistence. PLoS ONE 8, e65548 (2013)
K. Tian, X. Yu, T. Zhao, Y. Feng, Z. Cao, C. Wang, Y. Hu, X. Chen, D. Hu, X. Tian, D. Liu, S. Zhang, X. Deng, Y. Ding, L. Yang, Y. Zhang, H. Xiao, M. Qiao, B. Wang, L. Hou, X. Wang, X. Yang, L. Kang, M. Sun, P. Jin, S. Wang, Y. Kitamura, J. Yan, G.F. Gao, Emergence of fatal PRRSV variants: unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLoS ONE 2, e526 (2007)
J.J. van Vugt, T. Storgaard, M.B. Oleksiewicz, A. Botner, High frequency RNA recombination in porcine reproductive and respiratory syndrome virus occurs preferentially between parental sequences with high similarity. J. Gen. Virol. 82, 2615–2620 (2001)
P.P. Wang, J.G. Dong, L.Y. Zhang, P.S. Liang, Y.L. Liu, L. Wang, F.H. Fan, C.X. Song, Sequence and phylogenetic analyses of the Nsp2 and ORF5 genes of porcine reproductive and respiratory syndrome virus in boars from South China in 2015. Transbound. Emerg. Dis. (2016). https://doi.org/10.1111/(ISSN)1865-1682
G. Wensvoort, C. Terpstra, J.M. Pol, E.A. ter Laak, M. Bloemraad, E.P. de Kluyver, C. Kragten, L. van Buiten, A. den Besten, F. Wagenaar et al., Mystery swine disease in the Netherlands: the isolation of Lelystad virus. Vet. Q. 13, 121–130 (1991)
W.H. Wu, Y. Fang, R. Farwell, M. Steffen-Bien, R.R. Rowland, J. Christopher-Hennings, E.A. Nelson, A 10-kDa structural protein of porcine reproductive and respiratory syndrome virus encoded by ORF2b. Virology 287, 183–191 (2001)
J. Xie, T. Cui, J. Cui, Y. Chen, M. Zhang, P. Zhou, S. Deng, S. Su, G. Zhang, Epidemiological and evolutionary characteristics of the PRRSV in Southern China from 2010 to 2013. Microb. Pathog. 75, 7–15 (2014)
H. Zhao, Q. Han, L. Zhang, Z. Zhang, Y. Wu, H. Shen, P. Jiang, Emergence of mosaic recombinant strains potentially associated with vaccine JXA1-R and predominant circulating strains of porcine reproductive and respiratory syndrome virus in different provinces of China. Virol. J. 14, 67 (2017)
K. Zhao, C. Ye, X.B. Chang, C.G. Jiang, S.J. Wang, X.H. Cai, G.Z. Tong, Z.J. Tian, M. Shi, T.Q. An, Importation and recombination are responsible for the latest emergence of highly pathogenic porcine reproductive and respiratory syndrome virus in China. J. Virol. 89, 10712–10716 (2015)
L. Zhou, Z. Wang, Y. Ding, X. Ge, X. Guo, H. Yang, NADC30-like strain of porcine reproductive and respiratory syndrome virus, China. Emerg. Infect. Dis. 21, 2256–2257 (2015)
L. Zhou, J. Zhang, J. Zeng, S. Yin, Y. Li, L. Zheng, X. Guo, X. Ge, H. Yang, The 30-amino-acid deletion in the Nsp2 of highly pathogenic porcine reproductive and respiratory syndrome virus emerging in China is not related to its virulence. J. Virol. 83, 5156–5167 (2009)
Acknowledgements
This study was supported by grants from National Natural Science Funds (31502043, 31502040), the key project of National Natural Science Foundation of China (31490601), China Agriculture Research System (No. CARS-36), the Pig Industry Technology System Innovation Team Project of Henan Province (S2012-06).
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Lin-jian Wang, Xin-xin Chen, and Gaiping Zhang conceived and designed the experiments. Lin-jian Wang, Bo Wan, and Zhenhua Guo performed the experiments. Bo Wan, Songlin Qiao, Rui Li, and Sha Xie contributed data analysis. Lin-jian Wang and Xin-xin Chen wrote the manuscript. Zhenhua Guo, Songlin Qiao, Rui Li, Sha Xie, Gaiping Zhang revised the manuscipt content. Gaiping Zhang, Songlin Qiao, and Xin-xin Chen approved final version of manuscript.
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All authors state that they have no conflicts of interest. This article does not contain any studies with animals performed by any of the authors. Informed consent was obtained from all individual participants included in the study.
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Wang, Lj., Wan, B., Guo, Z. et al. Genomic analysis of a recombinant NADC30-like porcine reproductive and respiratory syndrome virus in china. Virus Genes 54, 86–97 (2018). https://doi.org/10.1007/s11262-017-1516-1
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DOI: https://doi.org/10.1007/s11262-017-1516-1