Genetic Changes of S Gene during Co-inoculation of Two Infectious Bronchitis Virus Vaccines in SPF Chicks

Document Type : Original Article

Authors

1 Reference Laboratory for Veterinary Quality Control on Poultry Production, Animal Health Research Institute, Agricultural Research Centre, PO Box 246, Dokki, Giza, 12618, Egypt

2 Department of Virology, Faculty of Veterinary Medicine, University of Sadat City, Sadat 32897, Egypt

3 Professor of Virology, Vaccines, and immunology Faculty of veterinary Medicine, University of Sadat City, Egypt.

Abstract

Despite widespread immunizations, infectious bronchitis (IB) remains a significant issue in the Egyptian poultry industry. Multiple IBV genotypes, GI-1, GI-13, GI-16, and GI-23 have been continually circulating among chicken flocks in Egypt, inducing a substantial economic loss to the poultry sector. In addition, live attenuated vaccines representing classical and variant strains can control IBV in Egypt, mainly H120 and 793B. The H120 vaccine is widely spread and offers inadequate protection against heterotypic IBVs in the field. Therefore, a homologous live-attenuated VAR2 vaccine was developed from the Egyptian variant-2 strain Eg/1212B/2012.IB. Variant II vaccine protects against the homologous IBV challenge under experimental and field circumstances. In this study, an experimental trial was performed to simulate field practices such as heterologous vaccination of day-old specific pathogen-free chicks with IBV H120 vaccine (representing GI-1) and IB Var 2 vaccine (representing GI- 23). The current study aimed to determine the existence of nucleotide and amino acid variations within the S gene in isolated viruses following ten passages in the same bird. The deduced amino acid sequence of the S gene indicated viruses isolated from the 6th and 10th passages were identical and shared (96 %) and (83 %) identities with the IB variant II vaccine and H120, respectively. However, amino acid substitutions were observed at 26 positions in the N terminal domain (S1) and S2 is conserved compared to IB Var 2 vaccine. Most amino acid modifications occurred in the receptor binding domain (RBD) of the S1 gene. HVR2 has seven amino acid changes compared to the IB Var II vaccine. Isolates of P6 and P10 lacked IBV glycosylation site at position 139 which was detected in IBV/EG/1212B/2012 as well as IB variant II vaccine. The study also revealed no evidence of recombination between the two used live vaccines.
The deduced amino acid sequence of the S gene indicated viruses isolated from the 6th and 10th passages were identical and shared (96 %) and (83 %) identities with the IB variant II vaccine and H120, respectively. However, amino acid substitutions were observed at 26 positions in the N terminal domain (S1) and S2 is conserved compared to IB Var 2 vaccine. Most amino acid modifications occurred in the receptor binding domain (RBD) of the S1 gene. HVR2 has seven amino acid changes compared to the IB Var II vaccine. Isolates of P6 and P10 lacked IBV glycosylation site at position 139 which was detected in IBV/EG/1212B/2012 as well as IB variant II vaccine. The study also revealed no evidence of recombination between the two used live vaccines.

Keywords

Main Subjects

References

ABDEL-MONEIM, A.S., EL-KADY, M.F., LADMAN, B.S., and GELB, J., 2006. S1 gene sequence analysis of a neuropathogenic strain of avian infectious bronchitis virus in Egypt. Virology journal, 3(1), 1-9. DOI: 10.1186/1743-422X-3-78
ABDEL-SABOUR, M.A., AL-EBSHAHY, E.M., KHALIEL, S.A., ABDEL-WANIS, N.A., and YANAI, T., 2017. Isolation and molecular characterization of novel infectious bronchitis virus variants from vaccinated broiler flocks in Egypt. Avian diseases, 61(3), 307-310. https://DOI.org/10.1637/11566-121516-RegR
ABOLNIK, C. 2015. Genomic and single nucleotide polymorphism analysis of infectious bronchitis coronavirus. Infection, Genetics and Evolution, 32, 416-424. https://DOI.org/10.1016/j.meegid.2015.03.033
ABOZEID, H.H.. and NAGUIB, M.M., 2020. Infectious bronchitis virus in Egypt: Genetic diversity and vaccination strategies. Veterinary Sciences, 7(4), 204. https://DOI.org/10.3390/vetsci7040204
ABOZEID, H.H., PALDURAI, A., KHATTAR, S.K., AFIFI, M.A., EL-KADY, M.F., EL-DEEB, A.H.. and SAMAL, S.K., 2017. Complete genome sequences of two avian infectious bronchitis viruses isolated in Egypt: evidence for genetic drift and genetic recombination in the circulating viruses. Infection, Genetics and Evolution, 53, 7-14. https://DOI.org/10.1016/j.meegid.2017.05.006
ADZHAR, A., GOUGH, RE, HAYDON, D., SHAW, K., BRITTON, P.. and CAVANAGH, D., 1997. Molecular analysis of the 793/B serotype of infectious bronchitis virus in Great Britain. Avian Pathology, 26(3), 625 640 https://DOI.org/10.1080/03079459708419239
ALI, A., KILANY, W.H., EL-ABIDEEN, M.A.Z., EL SAYED, M.. and ELKADY, M., 2018. Safety and efficacy of attenuated classic and variant 2 infectious bronchitis virus candidate vaccines. Poultry Science, 97(12), 4238-4244. https://DOI.org/10.3382/ps/pey312
ARINAMINPATHY, N., RATMANN, O., KOELLE, K., EPSTEIN, SL, PRICE, GE, VIBOUD, C., MILLER, M.A., and GRENFELL, BT, 2012. Impact of cross-protective vaccines on epidemiological and evolutionary dynamics of influenza. Proceedings of the National Academy of Sciences, 109(8), 3173-3177. https://DOI.org/10.1073/pnas.1113342109
BALL, C., BENNETT, S., FORRESTER, A., and GANAPATHY, K., 2016. Genetic mutations in live infectious bronchitis vaccine viruses following single or dual in vitro infection of tracheal organ cultures. Journal of General Virology, 97, 3232-3237. DOI: 10.1099/jgv.0.000628
BALL, C., AWAD, F., HUTTON, S., FORRESTER, A., BAYLIS, M., and GANAPATHY, K., 2017. Infectious bronchitis vaccine virus detection and part-S1 genetic variation following single or dual inoculation in broiler chicks. Avian Pathology, 46(3), 309-318. https://DOI.org/10.1080/03079457.2016.1268675
BELOUZARD, S., MILLET, JK, LICITRA, B.N., and WHITTAKER, GR, 2012. Mechanisms of coronavirus cell entry mediated by the viral spike protein. Viruses, 4(6), 1011-1033. https://DOI.org/10.3390/v4061011
BIJLENGA, G., COOK, J.K., GELB, JR, J., and WIT, J.D., 2004. Development and use of the H strain of avian infectious bronchitis virus from the Netherlands as a vaccine: a review. Avian Pathology, 33(6), 550-557. https://DOI.org/10.1080/03079450400013154
BINNS, M.M., BOURSNELL, M.E., TOMLEY, F.M., and BROWN, T.D.K., 1986. Comparison of the spike precursor sequences of coronavirus IBV strains M41 and 6/82 with that of IBV Beaudette. Journal of General Virology, 67(12), 2825-2831. https://DOI.org/10.1099/0022-1317-67-12-2825
BOSCH, B.J., VAN DER ZEE, R., DE HAAN, C.A., and ROTTIER, P.J., 2003. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. Journal of virology, 77(16), 8801-8811 https://DOI.org/10.1128/JVI.77.16.8801-8811.2003.
CAVANAGH, D. 1995. The Coronavirus Surface Glycoprotein. In: Siddell, S.G. (eds) The Coronaviridae. The Viruses. Springer, Boston, MA, 73-113. https://DOI.org/10.1007/978-1-4899-1531-3_5
CAVANAGH, D. 2007. Coronavirus avian infectious bronchitis virus. Veterinary Research, 38(2), 281-297.   DOI: 10.1051/vetres:2006055
CAVANAGH, D., DAVIS, P.J., and MOCKETT, A.A., 1988. Amino acids within hypervariable region 1 of avian coronavirus IBV (Massachusetts serotype) spike glycoprotein are associated with neutralization epitopes. Virus Research, 11(2), 141-150.https://DOI.org/10.1016/0168-1702(88)90039-1
CAVANAGH, D., DAVIS, P.J., COOK, J.K., LI, D., KANT, A., and KOCH, G., 1992. Location of the amino acid differences in the S1 spike glycoprotein subunit of closely related serotypes of infectious bronchitis virus. Avian Pathology, 21(1), 33-43. https://DOI.org/10.1080/03079459208418816
COOK, J.K., ORBELL, S.J., WOODS, M.A., and HUGGINS, M.B., 1999. Breadth of protection of the respiratory tract provided by different live-attenuated infectious bronchitis vaccines against challenge with infectious bronchitis viruses of heterologous serotypes. Avian Pathology, 28(5), 477-485. https://DOI.org/10.1080/03079459994506
COOK, J.K., JACKWOOD, M., and JONES, R.C., 2012. The long view: 40 years of infectious bronchitis research. Avian Pathology, 41(3), 239-250. https://DOI.org/10.1080/03079457.2012.680432
DE WIT, J.J., NIEUWENHUISEN-VAN WILGEN, J., HOOGKAMER, A., VAN DE SANDE, H., ZUIDAM, G.J.. and FABRI, T.H.F., 2011. Induction of cystic oviducts and protection against early challenge with infectious bronchitis virus serotype D388 (genotype QX) by maternally derived antibodies and by early vaccination. Avian Pathology, 40(5), 463-471. https://DOI.org/10.1080/03079457.2011.599060
GANAPATHY, K. 2009. Diagnosis of infectious bronchitis in chickens. In Practice, 31(9), 424-431. https://doi.org/10.1136/inpract.31.9.424
GHETAS, A.M., KUTKAT, M.A., AMER, M.M., and AWAAD, M.H., 2016. Isolation and molecular identification of IBV isolates in different governorates in Egypt. Journal of the Egyptian Society of Parasitology, 46(2),341-346. DOI: 10.21608/JESP.2016.88682
HALL, T. 2004. BioEdit version 7.0.0. Distributed by author,http://www.mbio.ncsu.edu/BioEdit/bioedit.html.
HAN, DP, LOHANI, M. and CHO, MW, 2007. Specific asparagine-linked glycosylation sites are critical for DC-SIGN-and L-SIGN-mediated severe acute respiratory syndrome coronavirus entry. Journal of Virology, 81(21), 12029-12039. https://DOI.org/10.1128/JVI.00315-07
HEWSON, K.A., NOORMOHAMMADI, A.H., DEVLIN, J.M., BROWNING, G.F., SCHULTZ, B.K., and IGNJATOVIC, J., 2014. Evaluation of a novel strain of infectious bronchitis virus emerged as a result of spike gene recombination between two highly diverged parent strains. Avian Pathology, 43(3), 249-257. https://DOI.org/10.1080/03079457.2014.914624
HOPKINS, S.R., and YODER J.R. H.W., 1986. Reversion to virulence of chicken-passaged infectious bronchitis vaccine virus. Avian Diseases, 30(1), 221-223. https://DOI.org/10.2307/1590639
HUSSEIN, A.H., EMARA, M.M., ROHAIM, M.A., GANAPATHY, K.. and ARAFA, A.M., 2014. Sequence analysis of infectious bronchitis virus IS/1494 like strain isolated from broiler chicken co-infected with Newcastle disease virus in Egypt during 2012. International Journal of Poultry Science 13(9), 530-536. DOI:10.3923/ijps.2014.530.536
JACKWOOD, M.W. 2012. Review of infectious bronchitis virus around the world. Avian Diseases, 56(4), 634-641. https://DOI.org/10.1637/10227-043012-Review.1
JACKWOOD, M.W., and DE WIT, S., 2013. Infectious bronchitis. Diseases of Poultry,14th edition, 139-159. https://DOI.org/10.1002/9781119371199.ch4
KANT, A., KOCH, G., VAN ROOZELAAR, D.J., KUSTERS, J.G., POELWIJK, F.A.J., and VAN DER ZEIJST, B.A.M., 1992. Location of antigenic sites defined by neutralizing monoclonal antibodies on the S1 avian infectious bronchitis virus glycopolypeptide. Journal of General Virology, 73(3), 591-596. https://DOI.org/10.1099/0022-1317-73-3-591
KOCH, G., HARTOG, L., KANT, A.V., and VAN ROOZELAAR, D.J., 1990. Antigenic domains on the peplomer protein of avian infectious bronchitis virus: correlation with biological functions. Journal of General Virology, 71(9), 1929-1935. https://DOI.org/10.1099/0022-1317-71-9-1929
KUSTERS, J.G., NIESTERS, H.G.M., LENSTRA, J.A., HORZINEK, M.C., and VAN DER ZEIJST, B.A.M., 1989. Phylogeny of antigenic variants of avian coronavirus IBV. Virology, 169(1), 217-221. https://DOI.org/10.1016/0042-6822(89)90058-5
LI, W., JUNKER, D., HOCK, L., EBIARY, E., and COLLISSON, EW, 1994. Evolutionary implications of genetic variations in the S1 gene of infectious bronchitis virus. Virus Research, 34(3), 327-338. https://DOI.org/10.1016/0168-1702(94)90132-5
LIN, S.Y., and CHEN, H.W., 2017. Infectious bronchitis virus variants: molecular analysis and pathogenicity investigation. International Journal of Molecular Sciences, 18(10), 2030. https://DOI.org/10.3390/ijms18102030
MASTERS, P.S., and PERLMAN, S., 2013. Coronaviridae. In Fields Virology, (Knipe, DM and Howley, PM, eds) 2, 825–858
MEIR, R., MAHARAT, O., FARNUSHI, Y., and SIMANOV, L., 2010. Development of a real-time TaqMan® RT-PCR assay for the detection of infectious bronchitis virus in chickens, and comparison of RT-PCR and virus isolation. Journal of Virological Methods, 163(2), 190-194. https://DOI.org/10.1016/j.jviromet.2009.09.014
MOCKETT, A.A., CAVANAGH, D., and BROWN, T.D.K., 1984. Monoclonal antibodies to the S1 spike and membrane proteins of avian infectious bronchitis coronavirus strain Massachusetts M41. Journal of General Virology, 65(12), 2281-2286. https://DOI.org/10.1099/0022-1317-65-12-2281
MOHARAM, I., SULTAN, H., HASSAN, K., IBRAHIM, M., SHANY, S., SHEHATA, A.A., ABO-ELKHAIR, M., PFAFF, F., HÖPER, D., KADY, M.E., and BEER, M., 2020. Emerging infectious bronchitis virus (IBV) in Egypt: evidence for an evolutionary advantage of a new S1 variant with a unique gene 3ab constellation. Infection, Genetics and Evolution, 85, 104433. https://DOI.org/10.1016/j.meegid.2020.104433
MOORE, K.M., JACKWOOD, M.W., and HILT, D.A., 1997. Identification of amino acids involved in a serotype and neutralization specific epitope within the s1 subunit of avian infectious bronchitis virus. Archives of Virology, 142(11), 2249-2256. DOI: 10.1007/s007050050239
PAYNE, S. 2017. Chapter 17-Family Coronaviridae”. În Viruses, ediție de Susan Payne, 149–58. DOI: 10.1016/B978-0-12-803109-4.00017-9.
ROHAIM, MA, EL NAGGAR, RF, ABDELSABOUR, MA, MOHAMED, MH, EL-SABAGH, IM and MUNIR, M., 2020. Evolutionary analysis of infectious bronchitis virus reveals marked genetic diversity and recombination events. Genes, 11(6), 605. https://DOI.org/10.3390/genes11060605
SCHIJNS, V. E. J. C., SHARMA, J., and TARPEY, I. 2008. Practical Aspects of Poultry Vaccination. Avian Immunology, 373-393. Elsevier Ltd. https://DOI.org/10.1016/B978-012370634-8.50023-8
SHANG, J., ZHENG, Y., YANG, Y., LIU, C., GENG, Q., TAI, W., DU, L., ZHOU, Y., ZHANG, W., and LI, F., 2018. Cryo-electron microscopy structure of porcine delta coronavirus spike protein in the prefusion state. Journal of Virology, 92(4), e01556-17. https://DOI.org/10.1128/JVI.01556-17
SULTAN, H.A., ALI, A., EL FEIL, W.K., BAZID, A.H.I., ZAIN EL-ABIDEEN, M.A., and KILANY, W.H., 2019. Protective efficacy of different live attenuated infectious bronchitis virus vaccination regimes against challenge with IBV variant-2 circulating in the Middle East. Frontiers in Veterinary Science, 6, 341.  DOI: 10.3389/fvets.2019.00341
THOR, S.W., HILT, D.A., KISSINGER, J.C., PATERSON, A.H., and JACKWOOD, M.W., 2011. Recombination in avian gamma-coronavirus infectious bronchitis virus. Viruses, 3(9), 1777-1799. https://DOI.org/10.3390/v3091777
TORO, H., PENNINGTON, D., GALLARDO, RA, VAN SANTEN, VL, VAN GINKEL, FW, ZHANG, J., and JOINER, KS, 2012. Infectious bronchitis virus subpopulations in vaccinated chickens after challenge. Avian Diseases, 56(3), 501-508. https://DOI.org/10.1637/9982-110811-Reg.1
TORTORICI, M.A., WALLS, A.C., LANG, Y., WANG, C., LI, Z., KOERHUIS, D., BOONS, G.J., BOSCH, B.J., REY, F.A., DE GROOT, R.J., and VEESLER, D., 2019. Structural basis for human coronavirus attachment to sialic acid receptors. Nature Structural and Molecular Biology, 26(6), 481-489. https://DOI.org/10.1038/s41594-019-0233-y
WALLS, A.C., XIONG, X., PARK, Y.J., TORTORICI, M.A., SNIJDER, J., QUISPE, J., CAMERONI, E., GOPAL, R., DAI, M., LANZAVECCHIA, A., and ZAMBON, M., 2019. Unexpected receptor functional mimicry elucidates activation of coronavirus fusion. Cell, 176(5), 1026-1039. https://DOI.org/10.1016/j.cell.2018.12.028
WANG, C.H., and HUANG, Y.C., 2000. Relationship between serotypes and genotypes based on the hypervariable region of the S1 gene of infectious bronchitis virus. Archives of Virology, 145(2), 291-300. https://DOI.org/10.1007/s007050050024
WICKRAMASINGHE, I.A., DE VRIES, R.P., GRÖNE, A., DE HAAN, C.A.M., and VERHEIJE, M.H., 2011. Binding of avian coronavirus spike proteins to host factors reflects virus tropism and pathogenicity. Journal of Virology, 85(17), 8903-8912. https://DOI.org/10.1128/JVI.05112-11
ZANATY, A., NAGUIB, M.M., EL-HUSSEINY, M.H., MADY, W., HAGAG, N., and ARAFA, A.S., 2016A. The sequence of the full spike S1 glycoprotein of infectious bronchitis virus circulating in Egypt reveals evidence of intra-genotypic recombination. Archives of Virology, 161(12), 3583-3587. https://DOI.org/10.1007/s00705-016-3042-1
ZANATY, A., ARAFA, A.S., HAGAG, N., and EL-KADY, M., 2016B. Genotyping and pathotyping of diversified strains of infectious bronchitis viruses circulating in Egypt. World Journal of Virology, 5(3), 125.  doi: 10.5501/wjv.v5.i3.125
ZHENG, J., YAMADA, Y., FUNG, T.S., HUANG, M., CHIA, R., and LIU, D.X., 2018. Identification of N-linked glycosylation sites in the spike protein and their functional impact on the replication and infectivity of coronavirus infectious bronchitis virus in cell culture. Virology, 513, 65-74. https://DOI.org/10.1016/j.virol.2017.10.003
ZHOU, Y., LU, K., PFEFFERLE, S., BERTRAM, S., GLOWACKA, I., DROSTEN, C., PÖHLMANN, S., and SIMMONS, G., 2010. A single asparagine-linked glycosylation site of the severe acute respiratory syndrome coronavirus spike glycoprotein facilitates inhibition by mannose-binding lectin through multiple mechanisms. Journal of virology, 84(17), 8753-8764. https://DOI.org/10.1128/JVI.00554-10

Files

History

  • Receive Date: 30 August 2022
  • Revise Date: 01 October 2022
  • Accept Date: 15 November 2022

Share

How to cite

Statistics