Abstract
Gallid herpesvirus-1 (GaHV-1), commonly named infectious laryngotracheitis (ILT) virus, causes the respiratory disease in chickens known as ILT. The molecular determinants associated with differences in pathogenicity of GaHV-1 strains are not completely understood, and a comparison of genomic sequences of isolates that belong to different genotypes could help identify genes involved in virulence. Dideoxy sequencing, 454 pyrosequencing and Illumina sequencing-by-synthesis were used to determine the nucleotide sequences of four genotypes of virulent strains from GaHV-1 groups I–VI. Three hundred and twenty-five open reading frames (ORFs) were compared with those of the recently sequenced genome of the Serva vaccine strain. Only four ORFs, ORF C, UL37, ICP4 and US2 differed in amino acid (aa) lengths among the newly sequenced genomes. Genome sequence alignments were used to identify two regions (5′ terminus and the unique short/repeat short junction) that contained deletions. Seventy-eight synonymous and 118 non-synonymous amino acid substitutions were identified with the examined ORFs. Exclusive to the genome of the Serva vaccine strain, seven non-synonymous mutations were identified in the predicted translation products of the genes encoding glycoproteins gB, gE, gL and gM and three non-structural proteins UL28 (DNA packaging protein), UL5 (helicase-primase) and the immediate early protein ICP4. Furthermore, our comparative sequence analysis of published and newly sequenced GaHV-1 isolates has provided evidence placing the cleavage/packaging site (a-like sequence) within the inverted repeats instead of its placement at the 3′ end of the UL region as annotated in the GenBank’s entries NC006623 and HQ630064.
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References
P.C. Chang, Y.L. Lee, J.H. Shien, H.K. Shieh, Rapid differentiation of vaccine strains and field isolates of infectious laryngotracheitis virus by restriction fragment length polymorphism of PCR products. J. Virol. Methods 66, 179–186 (1997)
B. Chevreux, T. Wetter, S. Suhai, Genome sequence assembly using trace signal and additional sequence information. Comput. Sci. Biol. GCB 1, 45–56 (1999)
F. Corpet, Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881–10890 (1988)
J.L. Creelan, V.M. Calvert, D.A. Graham, S.J. McCullough, Rapid detection and characterization from field cases of infectious laryngotracheitis virus by real-time polymerase chain reaction and restriction fragment length polymorphism. Avian Pathol. 35, 173–179 (2006)
A.J. Davison, R. Eberle, G.S. Hayward, D.J. McGeoch, A.C. Minson, P.E. Pellet, B. Roizman, M.J. Studdert, E. Thiry, Family Herpesviridae, in Virus Taxonomy: Eight Report of the International Committee on Taxonony of Viruses, ed. by C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball (Academic Press, San Diego, 2005), pp. 193–212
W. Fuchs, T.C. Mettenleiter, DNA sequence and transcriptional analysis of the UL1 to UL5 gene cluster of infectious laryngotracheitis virus. J. Gen. Virol. 77(Pt 9), 2221–2229 (1996)
W. Fuchs, T.C. Mettenleiter, DNA sequence of the UL6 to UL20 genes of infectious laryngotracheitis virus and characterization of the UL10 gene product as a nonglycosylated and nonessential virion protein. J. Gen. Virol. 80(Pt 8), 2173–2182 (1999)
W. Fuchs, T.C. Mettenleiter, The nonessential UL49.5 gene of infectious laryngotracheitis virus encodes an O-glycosylated protein which forms a complex with the non-glycosylated UL10 gene product. Virus Res. 112, 108–114 (2005)
W. Fuchs, J. Veits, D. Helferich, H. Granzow, J.P. Teifke, T.C. Mettenleiter, Molecular biology of avian infectious laryngotracheitis virus. Vet. Res. 38, 261–279 (2007)
W. Fuchs, K. Ziemann, J.P. Teifke, O. Werner, T.C. Mettenleiter, The non-essential UL50 gene of avian infectious laryngotracheitis virus encodes a functional dUTPase which is not a virulence factor. J. Gen. Virol. 81, 627–638 (2000)
E. Gelenczei, E. Marty, Strain stability and immunologic characteristics of tissue-culture modified infectious laryngotracheitis virus. Avian Dis. 9, 44–56 (1962)
D. Gordon, C. Abajian, P. Green, Consed: a graphical tool for sequence finishing. Genome Res. 8, 195–202 (1998)
A.M. Griffin, The complete sequence of the capsid p40 gene from infectious laryngotracheitis virus. Nucleic Acids Res. 18, 3664 (1990)
A.M. Griffin, Identification of 21 genes of infectious laryngotracheitis virus using random sequencing of genomic DNA. J. Gen. Virol. 70(Pt 11), 3085–3089 (1989)
A.M. Griffin, The nucleotide sequence of the glycoprotein gB gene of infectious laryngotracheitis virus: analysis and evolutionary relationship to the homologous gene from other herpesviruses. J. Gen. Virol. 72(Pt 2), 393–398 (1991)
A.M. Griffin, M.E. Boursnell, Analysis of the nucleotide sequence of DNA from the region of the thymidine kinase gene of infectious laryngotracheitis virus; potential evolutionary relationships between the herpesvirus subfamilies. J. Gen. Virol. 71(Pt 4), 841–850 (1990)
J.S. Guy, T.J. Bagust, Laryngotracheitis, in Disease of Poultry, 11th edn., ed. by Y.M. Saif, H.J. Barnes, J.R. Glisson, A.M. Fadly, L.R. McDougald, D.E. Swayne (Iowa State Press, Ames, 2003), pp. 121–134
J.S. Guy, M. Garcia, Infectious Laryngotracheitis Virus, 12th edn. (Wiley-Blackwell, Hoboken, 2008)
M.G. Han, S.J. Kim, Analysis of Korean strains of infectious laryngotracheitis virus by nucleotide sequences and restriction fragment length polymorphism. Vet. Microbiol. 83, 321–331 (2001)
B. Hirt, Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 26, 365–369 (1967)
X. Huang, A. Madan, CAP3: a DNA sequence assembly program. Genome Res. 9, 868–877 (1999)
M.A. Johnson, C.T. Prideaux, K. Kongsuwan, M. Sheppard, K.J. Fahey, Gallid herpesvirus 1 (infectious laryngotracheitis virus): cloning and physical maps of the SA-2 strain. Arch. Virol. 119, 181–198 (1991)
M.A. Johnson, C.T. Prideaux, K. Kongsuwan, S.G. Tyack, M. Sheppard, ICP27 immediate early gene, glycoprotein K (gK) and DNA helicase homologues of infectious laryngotracheitis virus (gallid herpesvirus 1) SA-2 strain. Arch. Virol. 140, 623–634 (1995)
M.A. Johnson, S.G. Tyack, C. Prideaux, K. Kongsuwan, M. Sheppard, Nucleotide sequence of infectious laryngotracheitis virus (gallid herpesvirus 1) ICP4 gene. Virus Res. 35, 193–204 (1995)
M.A. Johnson, S.G. Tyack, C.T. Prideaux, K. Kongsuwan, M. Sheppard, Nucleotide sequence of the left-terminus of infectious laryngotracheitis virus (Gallid herpesvirus 1) SA-2 strain. Arch. Virol. 142, 1903–1910 (1997)
M.A. Johnson, S.G. Tyack, C.T. Prideaux, K. Kongsuwan, M. Sheppard, Sequence characteristics of a gene in infectious laryngotracheitis virus homologous to glycoprotein D of herpes simplex virus. DNA Seq. 5, 191–194 (1995)
R.C. Jone, Viral respiratory diseases (ILT, aMPV infections, IB): are they ever under control? Br. Poult. Sci. 51, 1–11 (2010)
K. Katoh, K. Kuma, H. Toh, T. Miyata, MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511–518 (2005)
C.L. Keeler Jr., J.W. Hazel, J.E. Hastings, J.K. Rosenberger, Restriction endonuclease analysis of Delmarva field isolates of infectious laryngotracheitis virus. Avian Dis. 37, 418–426 (1993)
D.H. Kingsley, J.W. Hazel, C.L. Keeler Jr, Identification and characterization of the infectious laryngotracheitis virus glycoprotein C gene. Virology 203, 336–343 (1994)
N.C. Kirkpatrick, A. Mahmoudian, D. O’Rourke, A.H. Noormohammadia, Differentiation of infectious laryngotracheitis virus isolates by restriction fragment length polymorphic analysis of polymerase chain reaction products amplified from multiple genes. Avian Dis. 50, 28–34 (2006)
B.W. Kong, Identification of virus encoding microRNAs using 454 FLX sequencing platform. Methods Mol. Biol. 733, 81–91 (2011)
K. Kongsuwan, M.A. Johnson, C.T. Prideaux, M. Sheppard, Identification of an infectious laryngotracheitis virus gene encoding an immunogenic protein with a predicted M(r) of 32 kilodaltons. Virus Res. 29, 125–140 (1993)
K. Kongsuwan, M.A. Johnson, C.T. Prideaux, M. Sheppard, Use of lambda gt11 and monoclonal antibodies to map the gene for the 60, 000 dalton glycoprotein of infectious laryngotracheitis virus. Virus Genes 7, 297–303 (1993)
K. Kongsuwan, C.T. Prideaux, M.A. Johnson, M. Sheppard, K.J. Fahey, Nucleotide sequence of the gene encoding infectious laryngotracheitis virus glycoprotein B. Virology 184, 404–410 (1991)
K. Kongsuwan, C.T. Prideaux, M.A. Johnson, M. Sheppard, S. Rhodes, Nucleotide sequence analysis of an infectious laryngotracheitis virus gene corresponding to the US3 of HSV-1 and a unique gene encoding a 67 kDa protein. Arch. Virol. 140, 27–39 (1995)
S.W. Lee, P.F. Markham, J.F. Markham, I. Petermann, A.H. Noormohammadi, G.F. Browning, N.P. Ficorilli, C.A. Hartley, J.M. Devlin, First complete genome sequence of infectious laryngotracheitis virus. BMC Genomics 12, 197 (2011)
D.A. Leib, J.M. Bradbury, C.A. Hart, K. McCarthy, Genome isomerism in two alphaherpesviruses: Herpesvirus saimiri-1 (Herpesvirus tamarinus) and avian infectious laryngotracheitis virus. Brief Report. Arch. Virol. 93, 287–294 (1987)
M. Margulies, M. Egholm, W.E. Altman, S. Attiya, J.S. Bader, L.A. Bemben, J. Berka, M.S. Braverman, Y.J. Chen, Z. Chen, S.B. Dewell, L. Du, J.M. Fierro, X.V. Gomes, B.C. Godwin, W. He, S. Helgesen, C.H. Ho, G.P. Irzyk, S.C. Jando, M.L. Alenquer, T.P. Jarvie, K.B. Jirage, J.B. Kim, J.R. Knight, J.R. Lanza, J.H. Leamon, S.M. Lefkowitz, M. Lei, J. Li, K.L. Lohman, H. Lu, V.B. Makhijani, K.E. McDade, M.P. McKenna, E.W. Myers, E. Nickerson, J.R. Nobile, R. Plant, B.P. Puc, M.T. Ronan, G.T. Roth, G.J. Sarkis, J.F. Simons, J.W. Simpson, M. Srinivasan, K.R. Tartaro, A. Tomasz, K.A. Vogt, G.A. Volkmer, S.H. Wang, Y. Wang, M.P. Weiner, P. Yu, R.F. Begley, J.M. Rothberg, Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376–380 (2005)
C.J. Neff, C. Sudler, R.K. Hoop, Characterisation of western European field isolates of avian infectious laryngotracheitis virus by restriction fragment length polymorphisms and sequencing. Avian Dis. 52, 278–283 (2008)
M. Niikura, J.B. Dodgson, H.H. Cheng, Stability of Marek’s disease virus 132-bp repeats during serial in vitro passages. Arch. Virol. 151, 1431–1438 (2006)
D. Ojkic, J. Swinton, M. Vallieres, E. Martin, J. Shapiro, B. Sanei, B. Binnington, Characterization of field isolates of infectious laryngotracheitis virus from Ontario. Avian Pathol. 35, 286–292 (2006)
I. Oldoni, A. Rodriguez-Avila, S. Riblet, M. Garcia, Characterization of infectious laryngotracheitis virus (ILTV) isolates from commercial poultry by polymerase chain reaction and restriction fragment length polymorphisms (PCR-RFLP). Avian Dis. 52, 59–63 (2008)
D.J. Poulsen, C.R. Burton, J.J. O’Brian, S.J. Rabin, C.L. Keeler Jr, Identification of the infectious laryngotracheitis virus glycoprotein gB gene by the polymerase chain reaction. Virus Genes 5, 335–347 (1991)
R. Rachamadugu, J.Y. Lee, A. Wooming, B.W. Kong, Identification and expression analysis of infectious laryngotracheitis virus encoding microRNAs. Virus Genes 39, 301–308 (2009)
Y. Samberg, I. Aronovici, The development of a vaccine against avian infectious laryngotracheitis I. Modification of a laryngotracheitis virus. Refug. Vet. 26, 54–59 (1969)
S.J. Spatz, M. Garcia, C.L. Keeler Jr., C.L. Afonso, E. Mundt, S. Riblet, L. Zsak, D.L. Rock, in Presented at the 5th international workshop on the molecular pathogenesis of Marek’s disease virus and 1st symposium on avian herpesviruses, Athens, GA, USA.
D.R. Thureen, C.L. Keeler Jr, Psittacid herpesvirus 1 and infectious laryngotracheitis virus: comparative genome sequence analysis of two avian alphaherpesviruses. J. Virol. 80, 7863–7872 (2006)
D.N. Tripathy, M. García, Laryngotracheitis, in Isolation and Identification of Avian Pathogens, 5th edn., ed. by D.E. Swayne, J.R. Glisson, M.W. Jackwood, W.M. Reed (American Association of Avian Pathologist, University of Pennsylvania, New Bolton Center, 2008), pp. 94–98
J.D. Volkening, S.J. Spatz, Purification of DNA from the cell-associated herpesvirus Marek’s disease virus for 454 pyrosequencing using micrococcal nuclease digestion and polyethylene glycol precipitation. J. Virol. Methods 157, 55–61 (2009)
L.A. Waidner, J. Burnside, A.S. Anderson, E.L. Bernberg, M.A. German, B.C. Meyers, P.J. Green, R.W. Morgan, A microRNA of infectious laryngotracheitis virus can downregulate and direct cleavage of ICP4 mRNA. Virology 411, 25–31 (2011)
W. Wanasawaeng, N. Chansiripornchai, Molecular classification of infectious laryngotracheitis virus from chick embryo origin vaccine, tissue culture origin vaccine and field isolates. Thai J. Vet. Med. 40, 393–398 (2010)
M.A. Wild, S. Cook, M. Cochran, A genomic map of infectious laryngotracheitis virus and the sequence and organization of genes present in the unique short and flanking regions. Virus Genes 12, 107–116 (1996)
K. Ziemann, T.C. Mettenleiter, W. Fuchs, Gene arrangement within the unique long genome region of infectious laryngotracheitis virus is distinct from that of other alphaherpesviruses. J. Virol. 72, 847–852 (1998)
K. Ziemann, T.C. Mettenleiter, W. Fuchs, Infectious laryngotracheitis herpesvirus expresses a related pair of unique nuclear proteins which are encoded by split genes located at the right end of the UL genome region. J. Virol. 72, 6867–6874 (1998)
Acknowledgments
We thank Robert Mullis for his contributions in the bioinformatic analysis of the sequencing data. This research was funded by the United States Department of Agriculture CRIS program (project number 6612-32000-052) and the US Poultry and Egg Association (Project F032).
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11262_2011_696_MOESM1_ESM.pptx
Sup. 1 Single nucleotide polymorphisms resulting in synonymous amino acid substitutions in ORFs within the genome of five GaHV-1 strains. All Serva ORFs encoding amino acid of lengths >60 were examined for synonymous amino acids substitutions in comparison with homologous ORFs found within the genomes of the USDA (group I), 81658 (group III), 63140 (group V) and 1874C5 (group VI) strains. The list includes 80 ORFs as defined by Lee et al. within the Serva genome as well as three additional short ORFs (ilt240, ilt247 and ilt249, located between the ICP4 and US10 genes) that contained synonymous substitutions. Codons in bold are not found in the Serva ORF. (PPTX 101 kb)
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Spatz, S.J., Volkening, J.D., Keeler, C.L. et al. Comparative full genome analysis of four infectious laryngotracheitis virus (Gallid herpesvirus-1) virulent isolates from the United States. Virus Genes 44, 273–285 (2012). https://doi.org/10.1007/s11262-011-0696-3
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DOI: https://doi.org/10.1007/s11262-011-0696-3