Skip to main content
SpringerLink
Log in

Direct evidence of host genome acquisition by the alphaherpesvirus Marek’s disease virus

  • Published:
Archives of Virology Aims and scope Submit manuscript

Summary.

Many herpesviruses including Marek’s disease virus (MDV), a poultry alphaherpesvirus, carry homologous host genes presumably acquired during viral evolution. We have characterized one recent acquisition by MDV in considerable detail. The virulent MDV strain Md11 previously was isolated from a commercial chicken and initially propagated on duck cells. In the process of cloning the entire Md11 genome in a bacterial artificial chromosome (BAC), we obtained an infectious clone in which the entire terminal repeat short segment was replaced with a portion of the duck genome that corresponds to chicken chromosome 19. This sequence is not predicted to express any protein even though it contains one exon of the VAMP1 gene. The replacement did not affect MDV replication in vitro, despite the virus having only one copy of ICP4. Furthermore, we have shown that the variant MDV genome containing the duck genome substitution is present in the parental Md11 population and has been maintained through several subsequent propagations of the virus on chicken cells. This finding provides direct evidence that host genome acquisition by MDV actually occurs during virus replication, and that one or more such MDV genomes with host sequences may exist within MDV viral stocks which tend to be polyclonal, due to the cell-associated nature of its infection process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • CL Afonso ER Tulman Z Lu L Zsak DL Rock GF Kutish (2001) ArticleTitleThe genome of turkey herpesvirus. J Virol 85 1123–1135

    Google Scholar 

  • AS Anderson A Francesconi R Morgan (1992) ArticleTitleComplete nucleotide sequence of the Marek’s disease virus ICP4 gene. Virology 189 657–667 Occurrence Handle10.1016/0042-6822(92)90589-H Occurrence Handle1:CAS:528:DyaK3sXktVajt7g%3D Occurrence Handle1322594

    Article  CAS  PubMed  Google Scholar 

  • AS Anderson MS Parcells RW Morgan (1998) ArticleTitleThe glycoprotein D (US6) homolog is not essential for oncogenicity or horizontal transmission of Marek’s disease virus. J Virol 72 2548–2553 Occurrence Handle1:CAS:528:DyaK1cXhtFGgsLk%3D Occurrence Handle9499123

    CAS  PubMed  Google Scholar 

  • PM Biggs (1997) ArticleTitleThe Leeuwenhoek lecture. Marek’s disease herpesvirus: oncogenesis and prevention. Phil Trans R Soc Lond B 352 1951–1962 Occurrence Handle10.1098/rstb.1997.0181 Occurrence Handle1:STN:280:DyaK1c7htlOisA%3D%3D

    Article  CAS  Google Scholar 

  • PL Cortes CJ Cardona (2004) ArticleTitlePathogenesis of a Marek’s disease virus mutant lacking vIL-8 in resistant and susceptible chickens. Avian Dis 48 50–60 Occurrence Handle15077797

    PubMed  Google Scholar 

  • X Cui LF Lee WM Reed HJ Kung SM Reddy (2004) ArticleTitleMarek’s disease virus-encoded vIL-8 gene is involved in early cytolytic infection but dispensable for establishment of latency. J Virol 78 4753–4760 Occurrence Handle1:CAS:528:DC%2BD2cXjsVKisLs%3D Occurrence Handle15078957

    CAS  PubMed  Google Scholar 

  • H-J Delecluse W Hammerschmidt (1993) ArticleTitleStatus of Marek’s disease virus in established lymphoma cell lines: herpesvirus integration is common. J Virol 67 82–92 Occurrence Handle1:CAS:528:DyaK3sXns12kuw%3D%3D Occurrence Handle8380099

    CAS  PubMed  Google Scholar 

  • L Fragnet MA Blasco W Klapper D Rasschaert (2003) ArticleTitleThe RNA subunit of telomerase is encoded by Marek’s disease virus. J Virol 77 5985–5996 Occurrence Handle10.1128/JVI.77.10.5985-5996.2003 Occurrence Handle1:CAS:528:DC%2BD3sXjs1OksLY%3D Occurrence Handle12719590

    Article  CAS  PubMed  Google Scholar 

  • K Fukuchi K Sudo Y-S Lee A Tanaka M Nonoyama (1984) ArticleTitleStructure of Marek’s disease virus DNA: detailed restriction enzyme map. J Virol 51 102–109 Occurrence Handle1:CAS:528:DyaL2cXkvVCkt78%3D Occurrence Handle6328029

    CAS  PubMed  Google Scholar 

  • K Hirai K Ikuta S Kato (1981) ArticleTitleStructural changes of the DNA of Marek’s disease virus during serial passage in cultured cells. Virology 115 385–389 Occurrence Handle10.1016/0042-6822(81)90119-7 Occurrence Handle1:CAS:528:DyaL38XjtFehug%3D%3D Occurrence Handle6274089

    Article  CAS  PubMed  Google Scholar 

  • BC Horsburgh MM Hubinette D Qiang MLE MacDonald F Tufaro (1999) ArticleTitleAllele replacement: an application that permits rapid manipulation of herpes simplex virus type 1 genomes. Gene Ther 6 922–930 Occurrence Handle10.1038/sj.gt.3300887 Occurrence Handle1:CAS:528:DyaK1MXjtVKgtLg%3D Occurrence Handle10505118

    Article  CAS  PubMed  Google Scholar 

  • Izumiya Y, Janng H-K, Ono M, Mikami T (2001) A complete genome sequence of Marek’s disease virus type 2, strain HPRS24. In: Hirai K (ed) Marek’s disease virus. Springer, Berlin, Heidelberg, New York, pp 25–55 (Curr Topics Microbiol Immunol, vol 255)

  • M Kishi G Bradley J Jessip A Tanaka M Nonoyama (1991) ArticleTitleInverted repeat regions of Marek’s disease virus DNA possess a structure similar to that of the a sequence of herpes simplex virus DNA and contain host cell telomere sequences. J Virol 65 2791–2797 Occurrence Handle1:CAS:528:DyaK3MXkt1egsLo%3D Occurrence Handle1851854

    CAS  PubMed  Google Scholar 

  • LF Lee P Wu D Sui D Ren J Kamil H-J Kung RL Witter (2000) ArticleTitleThe complete unique long sequence and the overall genomic organization of the GA strain of Marek’s disease virus. Proc Natl Acad Sci USA 97 6091–6096 Occurrence Handle1:CAS:528:DC%2BD3cXjvFart7c%3D Occurrence Handle10823954

    CAS  PubMed  Google Scholar 

  • AJ Link D Philips G Church (1997) ArticleTitleMethods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J Bacteriol 179 6228–6237 Occurrence Handle1:CAS:528:DyaK2sXmslOmtr8%3D Occurrence Handle9335267

    CAS  PubMed  Google Scholar 

  • K Maotani A Kanamori K Ikuta S Ueda S Kato K Hirai (1986) ArticleTitleAmplification of a tandem repeat within inverted repeats of Marek’s disease virus DNA during serial in vitro passage. J Virol 58 657–660 Occurrence Handle1:CAS:528:DyaL28XktVWntb0%3D Occurrence Handle3009876

    CAS  PubMed  Google Scholar 

  • A McGregor MR Schleiss (2001) ArticleTitleRecent advances in herpesvirus genetics using bacterial artificial chromosomes. Mol Genet Metabol 72 8–14 Occurrence Handle1:CAS:528:DC%2BD3MXjt1yitw%3D%3D

    CAS  Google Scholar 

  • M Messerle I Crnkovic W Hammerschmidt H Ziegler (1997) ArticleTitleCloning and mutagenesis of a herpesvirus genome as an infectious bacterial artificial chromosome. Proc Natl Acad Sci USA 94 14759–14763 Occurrence Handle10.1073/pnas.94.26.14759 Occurrence Handle1:CAS:528:DyaK1cXis1yjug%3D%3D Occurrence Handle9405686

    Article  CAS  PubMed  Google Scholar 

  • K Narayanan R Williamson Y Zhang AF Stwewart PA Ioannou (1999) ArticleTitleEfficient and precise engineering of a 200 kb β-globin human/bacterial artificial chromosome in E. coli DH10B using an inducible homologous recombination system. Gene Ther 6 442–447 Occurrence Handle10.1038/sj.gt.3300901 Occurrence Handle1:CAS:528:DyaK1MXhs1ygtbo%3D Occurrence Handle10435094

    Article  CAS  PubMed  Google Scholar 

  • MS Parcells SF Lin RL Dienglewicz V Majerciak DR Robinson HC Chen Z Wu GR Dubyak P Brunovskis HD Hunt LF Lee HJ Kung (2001) ArticleTitleMarek’s disease virus (MDV) encodes an interleukin-8 homolog (vIL-8): characterization of the vIL-8 protein and a vIL-8 deletion mutant MDV. J Virol 75 5159–5173 Occurrence Handle10.1128/JVI.75.11.5159-5173.2001 Occurrence Handle1:CAS:528:DC%2BD3MXjs1Whtbs%3D Occurrence Handle11333897

    Article  CAS  PubMed  Google Scholar 

  • MS Parcells AS Anderson RW Morgan (1995) ArticleTitleRetention of oncogenicity by a Marek’s disease virus mutant lacking six unique short region genes. J Virol 69 7888–7898 Occurrence Handle1:CAS:528:DyaK2MXptlOku7Y%3D Occurrence Handle7494301

    CAS  PubMed  Google Scholar 

  • L Petherbridge AC Brown SJ Baigent K Howes MA Sacco N Osterrieder VK Nair (2004) ArticleTitleOncogenicity of virulent Marek’s disease virus cloned as bacterial artificial chromosomes. J Virol 78 13376–13380 Occurrence Handle10.1128/JVI.78.23.13376-13380.2004 Occurrence Handle1:CAS:528:DC%2BD2cXhtVaqur%2FP Occurrence Handle15542691

    Article  CAS  PubMed  Google Scholar 

  • L Petherbridge K Howes SJ Baigent MA Sacco S Evans N Osterrieder V Nair (2003) ArticleTitleReplication-competent bacterial artificial chromosomes of Marek’s disease virus: novel tools for generation of molecularly defined herpesvirus vaccines. J Virol 77 8712–8718 Occurrence Handle10.1128/JVI.77.16.8712-8718.2003 Occurrence Handle1:CAS:528:DC%2BD3sXmt1Sitrk%3D Occurrence Handle12885890

    Article  CAS  PubMed  Google Scholar 

  • Roizman B, Knipe DM (2001) Herpes simplex viruses and their replication. In: Knipe DM, Howley PM (eds) Fields Virology, 4th edn. Lippincott Williams & Wilkins, Philadelphia, pp 2399–2459

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY

  • D Schumacher BK Tischer W Fuchs N Osterrieder (2000) ArticleTitleReconstitution of Marek’s disease virus serotype 1 (MDV-1) from DNA cloned as a bacterial artificial chromosome and characterization of a glycoprotein B-negative MDV-1 mutant. J Virol 74 11088–11098 Occurrence Handle10.1128/JVI.74.23.11088-11098.2000 Occurrence Handle1:CAS:528:DC%2BD3MXitFWmtLg%3D Occurrence Handle11070004

    Article  CAS  PubMed  Google Scholar 

  • H Shizuya B Birren U-J Kim V Mancino T Slepak Y Tachiiri M Simon (1992) ArticleTitleCloning and stable maintenance of 300-kilobase-pair fragments of human DNA in Escherichia coli using an F-factor-based vector. Proc Natl Acad Sci USA 89 8794–8797 Occurrence Handle1:CAS:528:DyaK38XmtVKju7w%3D Occurrence Handle1528894

    CAS  PubMed  Google Scholar 

  • RF Silva JC Barnett (1991) ArticleTitleRestriction endonuclease analysis of Marek’s disease virus DNA: differentiation of viral strains and determination of passage history. Avian Dis 35 487–495 Occurrence Handle1:STN:280:By2D287osFw%3D Occurrence Handle1659367

    CAS  PubMed  Google Scholar 

  • ER Tulman CL Afonso Z Lu L Zsak DL Rock GF Kutish (2000) ArticleTitleThe genome of a very virulent Marek’s disease virus. J Virol 74 7980–7988 Occurrence Handle10.1128/JVI.74.17.7980-7988.2000 Occurrence Handle1:CAS:528:DC%2BD3cXlsl2gu7Y%3D Occurrence Handle10933706

    Article  CAS  PubMed  Google Scholar 

  • RL Witter JM Sharma AM Fadly (1980) ArticleTitlePathogenicity of variant Marek’s disease virus isolates in vaccinated and unvaccinated chickens. Avian Dis 24 210–231

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, U.S.A.

    M. Niikura & J. Dodgson

  2. USDA-ARS Avian Disease and Oncology Laboratory, East Lansing, Michigan, U.S.A.

    M. Niikura & H. Cheng

Authors
  1. M. Niikura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Dodgson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Niikura, M., Dodgson, J. & Cheng, H. Direct evidence of host genome acquisition by the alphaherpesvirus Marek’s disease virus. Arch Virol 151, 537–549 (2006). https://doi.org/10.1007/s00705-005-0633-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-005-0633-7

Keywords

Search

Navigation