Home LiteratureArticle Details
PMID: 16203997 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Marek's disease virus Meq transforms chicken cells via the v-Jun transcriptional cascade: a converging transforming pathway for avian oncoviruses.

Levy AM, Gilad O, Xia L, Izumiya Y, Choi J, Tsalenko A, Yakhini Z, Witter R, Lee L, Cardona CJ, Kung HJ

Abstract

Marek's disease virus (MDV) is a highly pathogenic and oncogenic herpesvirus of chickens. MDV encodes a basic leucine zipper (bZIP) protein, Meq (MDV EcoQ). The bZIP domain of Meq shares homology with Jun/Fos, whereas the transactivation/repressor domain is entirely different. Increasing evidence suggests that Meq is the oncoprotein of MDV. Direct evidence that Meq transforms chicken cells and the underlying mechanism, however, remain completely unknown. Taking advantage of the DF-1 chicken embryo fibroblast transformation system, a well established model for studying avian sarcoma and leukemia oncogenes, we probed the transformation properties and pathways of Meq. We found that Meq transforms DF-1, with a cell morphology akin to v-Jun and v-Ski transformed cells, and protects DF-1 from apoptosis, and the transformed cells are tumorigenic in chorioallantoic membrane assay. Significantly, using microarray and RT-PCR analyses, we have identified up-regulated genes such as JTAP-1, JAC, and HB-EGF, which belong to the v-Jun transforming pathway. In addition, c-Jun was found to form stable dimers with Meq and colocalize with it in the transformed cells. RNA interference to Meq and c-Jun down-modulated the expression of these genes and reduced the growth of the transformed DF-1, suggesting that Meq transforms chicken cells by pirating the Jun pathway. These data suggest that avian herpesvirus and retrovirus oncogenes use a similar strategy in transformation and oncogenesis.

MeSH Terms
Animals Apoptosis/physiology Blotting, Western Cell Line Cell Transformation, Neoplastic/metabolism Chick Embryo Chorioallantoic Membrane/cytology Fluorescent Antibody Technique Gene Expression Regulation, Neoplastic Herpesvirus 2, Gallid/genetics,metabolism Immunoprecipitation JNK Mitogen-Activated Protein Kinases/metabolism Luciferases Microarray Analysis Oncogene Proteins, Viral/metabolism RNA Interference RNA, Small Interfering/genetics Reverse Transcriptase Polymerase Chain Reaction Signal Transduction/physiology
Chemicals
Eco-Q protein, Gallid herpesvirus 2 Oncogene Proteins, Viral RNA, Small Interfering Luciferases JNK Mitogen-Activated Protein Kinases
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Levy Alon M
Department of Biological Chemistry, School of Medicine, University of California, Davis, CA 95616, USA.
Gilad Oren
Xia Liang
Izumiya Yoshihiro
Choi Jonathan
Tsalenko Anya
Yakhini Zohar
Witter Richard
Lee Lucy
Cardona Carol J
Kung Hsing-Jien
References (32)
32 references, click to expand
  1. The complete unique long sequence and the overall genomic organization of the GA strain of Marek's disease virus.
    Proc Natl Acad Sci U S A. 2000 May 23;97(11):6091-6 PMID: 10823954
  2. The DF-1 chicken fibroblast cell line: transformation induced by diverse oncogenes and cell death resulting from infection by avian leukosis viruses.
    Virology. 1998 Sep 1;248(2):295-304 PMID: 9721238
  3. Meq: an MDV-specific bZIP transactivator with transforming properties.
    Curr Top Microbiol Immunol. 2001;255:245-60 PMID: 11217425
  4. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells.
    Nature. 2001 May 24;411(6836):494-8 PMID: 11373684
  5. Analysis of gene expression during myc oncogene-induced lymphomagenesis in the bursa of Fabricius.
    Proc Natl Acad Sci U S A. 2001 May 22;98(11):6378-83 PMID: 11353853
  6. Jun, the oncoprotein.
    Oncogene. 2001 Apr 30;20(19):2365-77 PMID: 11402333
  7. TOJ3, a target of the v-Jun transcription factor, encodes a protein with transforming activity related to human microspherule protein 1 (MCRS1).
    Oncogene. 2001 Nov 8;20(51):7524-35 PMID: 11709724
  8. JAC, a direct target of oncogenic transcription factor Jun, is involved in cell transformation and tumorigenesis.
    Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13601-6 PMID: 11698665
  9. c-Jun associates with the oncoprotein Ski and suppresses Smad2 transcriptional activity.
    J Biol Chem. 2002 Aug 9;277(32):29094-100 PMID: 12034730
  10. Role for a Drosophila Myb-containing protein complex in site-specific DNA replication.
    Nature. 2002 Dec 19-26;420(6917):833-7 PMID: 12490953
  11. Oncogenic effect of delta deletion in v-Jun does not result from uncoupling Jun from JNK signaling.
    Oncogene. 2003 Jan 30;22(4):498-506 PMID: 12555063
  12. Artificial oncoproteins: modified versions of the yeast bZip protein GCN4 induce cellular transformation.
    Oncogene. 2003 Sep 11;22(39):7931-41 PMID: 12970741
  13. Novel role for the potent endogenous inotrope apelin in human cardiac dysfunction.
    Circulation. 2003 Sep 23;108(12):1432-9 PMID: 12963638
  14. Characterization of the chromosomal binding sites and dimerization partners of the viral oncoprotein Meq in Marek's disease virus-transformed T cells.
    J Virol. 2003 Dec;77(23):12841-51 PMID: 14610205
  15. Microarray analysis identifies Autotaxin, a tumour cell motility and angiogenic factor with lysophospholipase D activity, as a specific target of cell transformation by v-Jun.
    Oncogene. 2004 Mar 25;23(13):2357-66 PMID: 14691447
  16. Marek's disease virus-encoded Meq gene is involved in transformation of lymphocytes but is dispensable for replication.
    Proc Natl Acad Sci U S A. 2004 Aug 10;101(32):11815-20 PMID: 15289599
  17. Generation of transforming viruses in cultures of chicken fibroblasts infected with an avian leukosis virus.
    J Virol. 1981 Sep;39(3):920-34 PMID: 6169846
  18. The v-ski oncogene encodes a truncated set of c-ski coding exons with limited sequence and structural relatedness to v-myc.
    Mol Cell Biol. 1989 Sep;9(9):4038-45 PMID: 2674685
  19. Transformation suppressor activity of a Jun transcription factor lacking its activation domain.
    Nature. 1991 Aug 15;352(6336):635-8 PMID: 1907719
  20. Marek disease virus encodes a basic-leucine zipper gene resembling the fos/jun oncogenes that is highly expressed in lymphoblastoid tumors.
    Proc Natl Acad Sci U S A. 1992 May 1;89(9):4042-6 PMID: 1315048
  21. Targeted degradation of c-Fos, but not v-Fos, by a phosphorylation-dependent signal on c-Jun.
    Science. 1992 Dec 18;258(5090):1941-4 PMID: 1470918
  22. Angiogenesis induced by head and neck squamous cell carcinoma xenografts in the chick embryo chorioallantoic membrane model.
    Ann Otol Rhinol Laryngol. 1993 Mar;102(3 Pt 1):215-21 PMID: 7681273
  23. Marek's disease virus (MDV) ICP4, pp38, and meq genes are involved in the maintenance of transformation of MDCC-MSB1 MDV-transformed lymphoblastoid cells.
    J Virol. 1996 Feb;70(2):1125-31 PMID: 8551572
  24. Induction of anchorage independent growth by heparin-binding EGF-like growth factor (HB-EGF).
    Growth Factors. 1999;17(1):49-61 PMID: 10495962
  25. DAP5 and IRES-mediated translation during programmed cell death.
    Cell Death Differ. 2005 Jun;12(6):554-62 PMID: 15818401
  26. The v-Jun point mutation allows c-Jun to escape GSK3-dependent recognition and destruction by the Fbw7 ubiquitin ligase.
    Cancer Cell. 2005 Jul;8(1):25-33 PMID: 16023596
  27. Isolation and cloning of JTAP-1: a cathepsin like gene upregulated in response to V-Jun induced cell transformation.
    Oncogene. 1996 Jan 4;12(1):135-42 PMID: 8552384
  28. Nucleolar and nuclear localization properties of a herpesvirus bZIP oncoprotein, MEQ.
    J Virol. 1997 Apr;71(4):3188-96 PMID: 9060682
  29. Transforming potential of the herpesvirus oncoprotein MEQ: morphological transformation, serum-independent growth, and inhibition of apoptosis.
    J Virol. 1998 Jan;72(1):388-95 PMID: 9420237
  30. Transformation of primary chick embryo fibroblasts by Marek's disease virus.
    Virology. 1997 Dec 8;239(1):20-35 PMID: 9426443
  31. Functional roles of Fas and Bcl-2-regulated apoptosis of T lymphocytes.
    J Immunol. 1998 Mar 1;160(5):2065-71 PMID: 9498742
  32. Identification and characterization of genes upregulated in cells transformed by v-Jun.
    Oncogene. 2000 Jul 20;19(31):3537-45 PMID: 10918612
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2005-10-11
Epub
2005-00-03
Pages
14831-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1253582
Subset
IM
Grants
NCI NIH HHS · CA46613 · United States
NCI NIH HHS · CA91574 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com