1887

Abstract

MicroRNAs (miRNAs) are increasingly recognized to play crucial roles in regulation of gene expression in different biological events, including many sporadic forms of cancer. However, despite the involvement of several viruses in inducing cancer, only a limited number of studies have been carried out to examine the miRNA expression signatures in virus-induced neoplasia, particularly in herpesvirus-induced tumours where virus-encoded miRNAs also contribute significantly to the miRNome of the tumour cell. Marek's disease (MD) is a naturally occurring, rapid-onset CD4 T-cell lymphoma of poultry, induced by the highly contagious Marek's disease virus (MDV). High levels of expression of virus-encoded miRNAs and altered expression of several host-encoded miRNAs were demonstrated in the MDV-transformed lymphoblastoid cell line MSB-1. In order to identify the miRNA expression signature specific to MDV-transformed cells, we examined the global miRNA expression profiles in seven distinct MDV-transformed cell lines by microarray analysis. This study revealed that, in addition to the high levels of MDV-encoded miRNAs, these MD tumour-derived lymphoblastoid cell lines showed altered expression of several host-encoded miRNAs. Comparison of the miRNA expression profiles of these cell lines with the MDV-negative, retrovirus-transformed AVOL-1 cell line showed that miR-150 and miR-223 are downregulated irrespective of the viral aetiology, whereas downregulation of miR-155 was specific for MDV-transformed tumour cells. Thus, increased expression of MDV-encoded miRNAs with specific downregulation of miR-155 can be considered as unique expression signatures for MD tumour cells. Analysis of the functional targets of these miRNAs would contribute to the understanding of the molecular pathways of MD oncogenicity.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.009902-0
2009-07-01
2020-01-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/7/1551.html?itemId=/content/journal/jgv/10.1099/vir.0.009902-0&mimeType=html&fmt=ahah

References

  1. Akiyama, Y. & Kato, S. ( 1974; ). Two cell lines from lymphomas of Marek's disease. Biken J 17, 105–116.
    [Google Scholar]
  2. Baek, D., Villen, J., Shin, C., Camargo, F. D., Gygi, S. P. & Bartel, D. P. ( 2008; ). The impact of microRNAs on protein output. Nature 455, 64–71.[CrossRef]
    [Google Scholar]
  3. Benjamini, Y. & Hochberg, Y. ( 1995; ). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57, 289–300.
    [Google Scholar]
  4. Bornkamm, G. W., Berens, C., Kuklik-Roos, C., Bechet, J. M., Laux, G., Bachl, J., Korndoerfer, M., Schlee, M., Holzel, M. & other authors ( 2005; ). Stringent doxycycline-dependent control of gene activities using an episomal one-vector system. Nucleic Acids Res 33, e137 [CrossRef]
    [Google Scholar]
  5. Burnside, J. & Morgan, R. W. ( 2007; ). Genomics and Marek's disease virus. Cytogenet Genome Res 117, 376–387.[CrossRef]
    [Google Scholar]
  6. Burnside, J., Bernberg, E., Anderson, A., Lu, C., Meyers, B. C., Green, P. J., Jain, N., Isaacs, G. & Morgan, R. W. ( 2006; ). Marek's disease virus encodes microRNAs that map to meq and the latency-associated transcript. J Virol 80, 8778–8786.[CrossRef]
    [Google Scholar]
  7. Burnside, J., Ouyang, M., Anderson, A., Bernberg, E., Lu, C., Meyers, B. C., Green, P. J., Markis, M., Isaacs, G. K. & other authors ( 2008; ). Deep sequencing of chicken microRNAs. BMC Genomics 9, 185 [CrossRef]
    [Google Scholar]
  8. Cai, X., Lu, S., Zhang, Z., Gonzalez, C. M., Damania, B. & Cullen, B. R. ( 2005; ). Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. Proc Natl Acad Sci U S A 102, 5570–5575.[CrossRef]
    [Google Scholar]
  9. Calin, G. A. & Croce, C. M. ( 2006; ). MicroRNA signatures in human cancers. Nat Rev Cancer 6, 857–866.[CrossRef]
    [Google Scholar]
  10. Calin, G. A. & Croce, C. M. ( 2007; ). Investigation of microRNA alterations in leukemias and lymphomas. Methods Enzymol 427, 193–213.
    [Google Scholar]
  11. Calnek, B. W. ( 1986; ). Marek's disease: a model for herpesvirus oncology. Crit Rev Microbiol 12, 293–320.
    [Google Scholar]
  12. Chan, M. M., Chen, C. L., Ager, L. L. & Cooper, M. D. ( 1988; ). Identification of the avian homologues of mammalian CD4 and CD8 antigens. J Immunol 140, 2133–2138.
    [Google Scholar]
  13. Cosmopoulos, K., Pegtel, M., Hawkins, J., Moffett, H., Novina, C., Middeldorp, J. & Thorley-Lawson, D. A. ( 2008; ). Comprehensive profiling of EBV microRNAs in nasopharyngeal carcinoma. J Virol 83, 2357–2367.
    [Google Scholar]
  14. Cullen, B. R. ( 2006; ). Viruses and microRNAs. Nat Genet 38 (Suppl.), S25–S30.[CrossRef]
    [Google Scholar]
  15. Cullen, B. R. ( 2009; ). Viral and cellular messenger RNA targets of viral microRNAs. Nature 457, 421–425.[CrossRef]
    [Google Scholar]
  16. Fabbri, M., Garzon, R., Andreeff, M., Kantarjian, H. M., Garcia-Manero, G. & Calin, G. A. ( 2008; ). MicroRNAs and noncoding RNAs in hematological malignancies: molecular, clinical and therapeutic implications. Leukemia 22, 1095–1105.[CrossRef]
    [Google Scholar]
  17. Garcia, P. & Frampton, J. ( 2008; ). Hematopoietic lineage commitment: miRNAs add specificity to a widely expressed transcription factor. Dev Cell 14, 815–816.[CrossRef]
    [Google Scholar]
  18. Garzon, R. & Croce, C. M. ( 2008; ). MicroRNAs in normal and malignant hematopoiesis. Curr Opin Hematol 15, 352–358.[CrossRef]
    [Google Scholar]
  19. Ghosh, Z., Mallick, B. & Chakrabarti, J. ( 2008; ). Cellular versus viral microRNAs in host–virus interaction. Nucleic Acids Res 37, 1035–1048.[CrossRef]
    [Google Scholar]
  20. Gottwein, E. & Cullen, B. R. ( 2008; ). Viral and cellular microRNAs as determinants of viral pathogenesis and immunity. Cell Host Microbe 3, 375–387.[CrossRef]
    [Google Scholar]
  21. Griffiths-Jones, S., Saini, H. K., van Dongen, S. & Enright, A. J. ( 2008; ). miRBase: tools for microRNA genomics. Nucleic Acids Res 36, D154–D158.[CrossRef]
    [Google Scholar]
  22. Javier, R. T. & Butel, J. S. ( 2008; ). The history of tumor virology. Cancer Res 68, 7693–7706.[CrossRef]
    [Google Scholar]
  23. Johnnidis, J. B., Harris, M. H., Wheeler, R. T., Stehling-Sun, S., Lam, M. H., Kirak, O., Brummelkamp, T. R., Fleming, M. D. & Camargo, F. D. ( 2008; ). Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 451, 1125–1129.[CrossRef]
    [Google Scholar]
  24. Lambeth, L. S., Yao, Y., Smith, L. P., Zhao, Y. & Nair, V. ( 2009; ). MicroRNAs 221 and 222 target p27Kip1 in Marek's disease virus-transformed tumour cell line MSB-1. J Gen Virol 90, 1164–1171.[CrossRef]
    [Google Scholar]
  25. Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., Pfeffer, S., Rice, A., Kamphorst, A. O. & other authors ( 2007; ). A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129, 1401–1414.[CrossRef]
    [Google Scholar]
  26. Lawrie, C. H., Soneji, S., Marafioti, T., Cooper, C. D., Palazzo, S., Paterson, J. C., Cattan, H., Enver, T., Mager, R. & other authors ( 2007; ). MicroRNA expression distinguishes between germinal center B cell-like and activated B cell-like subtypes of diffuse large B cell lymphoma. Int J Cancer 121, 1156–1161.[CrossRef]
    [Google Scholar]
  27. Lawrie, C. H., Saunders, N. J., Soneji, S., Palazzo, S., Dunlop, H. M., Cooper, C. D., Brown, P. J., Troussard, X., Mossafa, H. & other authors ( 2008; ). MicroRNA expression in lymphocyte development and malignancy. Leukemia 22, 1440–1446.[CrossRef]
    [Google Scholar]
  28. Lee, Y. S. & Dutta, A. ( 2009; ). MicroRNAs in cancer. Annu Rev Pathol 4, 199–227.[CrossRef]
    [Google Scholar]
  29. Lin, Y. C., Kuo, M. W., Yu, J., Kuo, H. H., Lin, R. J., Lo, W. L. & Yu, A. L. ( 2008; ). c-Myb is an evolutionary conserved miR-150 target and miR-150/c-Myb interaction is important for embryonic development. Mol Biol Evol 25, 2189–2198.[CrossRef]
    [Google Scholar]
  30. Lowery, A. J., Miller, N., McNeill, R. E. & Kerin, M. J. ( 2008; ). MicroRNAs as prognostic indicators and therapeutic targets: potential effect on breast cancer management. Clin Cancer Res 14, 360–365.[CrossRef]
    [Google Scholar]
  31. Lu, J., Guo, S., Ebert, B. L., Zhang, H., Peng, X., Bosco, J., Pretz, J., Schlanger, R., Wang, J. Y. & other authors ( 2008; ). MicroRNA-mediated control of cell fate in megakaryocyte–erythrocyte progenitors. Dev Cell 14, 843–853.[CrossRef]
    [Google Scholar]
  32. Martinez, I., Gardiner, A. S., Board, K. F., Monzon, F. A., Edwards, R. P. & Khan, S. A. ( 2008; ). Human papillomavirus type 16 reduces the expression of microRNA-218 in cervical carcinoma cells. Oncogene 27, 2575–2582.[CrossRef]
    [Google Scholar]
  33. Merkerova, M., Belickova, M. & Bruchova, H. ( 2008; ). Differential expression of microRNAs in hematopoietic cell lineages. Eur J Haematol 81, 304–310.[CrossRef]
    [Google Scholar]
  34. Morgan, R., Anderson, A., Bernberg, E., Kamboj, S., Huang, E., Lagasse, G., Isaacs, G., Parcells, M., Meyers, B. C. & other authors ( 2008; ). Sequence conservation and differential expression of Marek's disease virus microRNAs. J Virol 82, 12213–12220.[CrossRef]
    [Google Scholar]
  35. Nazerian, K. ( 1987; ). An updated list of avian cell lines and transplantable tumours. Avian Pathol 16, 527–544.[CrossRef]
    [Google Scholar]
  36. Ozen, M., Creighton, C. J., Ozdemir, M. & Ittmann, M. ( 2008; ). Widespread deregulation of microRNA expression in human prostate cancer. Oncogene 27, 1788–1793.[CrossRef]
    [Google Scholar]
  37. Petherbridge, L., Brown, A. C., Baigent, S. J., Howes, K., Sacco, M. A., Osterrieder, N. & Nair, V. K. ( 2004; ). Oncogenicity of virulent Marek's disease virus cloned as bacterial artificial chromosomes. J Virol 78, 13376–13380.[CrossRef]
    [Google Scholar]
  38. Pfeffer, S., Zavolan, M., Grasser, F. A., Chien, M., Russo, J. J., Ju, J., John, B., Enright, A. J., Marks, D. & other authors ( 2004; ). Identification of virus-encoded microRNAs. Science 304, 734–736.[CrossRef]
    [Google Scholar]
  39. Pfeffer, S., Sewer, A., Lagos-Quintana, M., Sheridan, R., Sander, C., Grasser, F. A., van Dyk, L. F., Ho, C. K., Shuman, S. & other authors ( 2005; ). Identification of microRNAs of the herpesvirus family. Nat Methods 2, 269–276.[CrossRef]
    [Google Scholar]
  40. Pratt, Z. L., Kuzembayeva, M., Sengupta, S. & Sugden, B. ( 2009; ). The microRNAs of Epstein–Barr virus are expressed at dramatically differing levels among cell lines. Virology 386, 387–397.[CrossRef]
    [Google Scholar]
  41. Rosenfeld, N., Aharonov, R., Meiri, E., Rosenwald, S., Spector, Y., Zepeniuk, M., Benjamin, H., Shabes, N., Tabak, S. & other authors ( 2008; ). MicroRNAs accurately identify cancer tissue origin. Nat Biotechnol 26, 462–469.[CrossRef]
    [Google Scholar]
  42. Ruike, Y., Ichimura, A., Tsuchiya, S., Shimizu, K., Kunimoto, R., Okuno, Y. & Tsujimoto, G. ( 2008; ). Global correlation analysis for micro-RNA and mRNA expression profiles in human cell lines. J Hum Genet 53, 515–523.[CrossRef]
    [Google Scholar]
  43. Schotte, D., Chau, J. C., Sylvester, G., Liu, G., Chen, C., van der Velden, V. H., Broekhuis, M. J., Peters, T. C., Pieters, R. & Boer, M. L. ( 2008; ). Identification of new microRNA genes and aberrant microRNA profiles in childhood acute lymphoblastic leukemia. Leukemia 23, 313–322.
    [Google Scholar]
  44. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N., Palmer, A. E. & Tsien, R. Y. ( 2004; ). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22, 1567–1572.[CrossRef]
    [Google Scholar]
  45. Skalsky, R. L., Samols, M. A., Plaisance, K. B., Boss, I. W., Riva, A., Lopez, M. C., Baker, H. V. & Renne, R. ( 2007; ). Kaposi's sarcoma-associated herpesvirus encodes an ortholog of miR-155. J Virol 81, 12836–12845.[CrossRef]
    [Google Scholar]
  46. Smyth, G. K. ( 2005; ). limma: linear models for microarray data. In Bioinformatics and Computational Biology Solutions using r and Bioconductor, pp. 397–420. Edited by R. Gentleman, V. J. Carey, W. Huber, R. A. Irizarry & S. Dudoit. New York: Springer.
  47. Sullivan, C. S. & Grundhoff, A. ( 2007; ). Identification of viral microRNAs. Methods Enzymol 427, 3–23.
    [Google Scholar]
  48. Wiemer, E. A. ( 2007; ). The role of microRNAs in cancer: no small matter. Eur J Cancer 43, 1529–1544.[CrossRef]
    [Google Scholar]
  49. Xiao, C., Calado, D. P., Galler, G., Thai, T. H., Patterson, H. C., Wang, J., Rajewsky, N., Bender, T. P. & Rajewsky, K. ( 2007; ). MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 131, 146–159.[CrossRef]
    [Google Scholar]
  50. Xu, H., Yao, Y., Zhao, Y., Smith, L. P., Baigent, S. J. & Nair, V. ( 2008; ). Analysis of the expression profiles of Marek's disease virus-encoded microRNAs by real-time quantitative PCR. J Virol Methods 149, 201–208.[CrossRef]
    [Google Scholar]
  51. Yao, Y., Zhao, Y., Xu, H., Smith, L. P., Lawrie, C. H., Sewer, A., Zavolan, M. & Nair, V. ( 2007; ). Marek's disease virus type 2 (MDV-2)-encoded microRNAs show no sequence conservation with those encoded by MDV-1. J Virol 81, 7164–7170.[CrossRef]
    [Google Scholar]
  52. Yao, Y., Zhao, Y., Xu, H., Smith, L. P., Lawrie, C. H., Watson, M. & Nair, V. ( 2008; ). MicroRNA profile of Marek's disease virus-transformed T-cell line MSB-1: predominance of virus-encoded microRNAs. J Virol 82, 4007–4015.[CrossRef]
    [Google Scholar]
  53. Yeung, M. L., Yassunaga, J., Bennasser, Y., Dusetti, N., Harris, D., Ahmad, N., Matsuoka, M. & Jeang, K. T. ( 2008; ). Roles for microRNAs, miR-93 and miR-130b, and tumor protein 53-induced nuclear protein 1 tumor suppressor in cell growth dysregulation by human T-cell lymphotrophic virus 1. Cancer Res 68, 8976–8985.[CrossRef]
    [Google Scholar]
  54. Zhao, Y., Yao, Y., Xu, H., Lambeth, L., Smith, L. P., Kgosana, L., Wang, X. & Nair, V. ( 2009; ). A functional MicroRNA-155 ortholog encoded by the oncogenic Marek's disease virus. J Virol 83, 489–492.[CrossRef]
    [Google Scholar]
  55. Zhou, B., Wang, S., Mayr, C., Bartel, D. P. & Lodish, H. F. ( 2007; ). miR-150, a microRNA expressed in mature B and T cells, blocks early B cell development when expressed prematurely. Proc Natl Acad Sci U S A 104, 7080–7085.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.009902-0
Loading
/content/journal/jgv/10.1099/vir.0.009902-0
Loading

Data & Media loading...

Supplements

Microarray expression levels of miRNAs (normalized against normal splenocytes) differentially expressed (adjusted <0.05) in each of the seven MDV-transformed cell lines compared with the expression profile in each other cell line. [ PDF] (5.8 MB)

PDF

Microarray expression levels of miRNAs (normalized against CD4 cells) differentially expressed (adjusted <0.05) in each of the four MDV-transformed cell lines compared with the expression profile in each other cell line. [ PDF] (1.9 MB)

PDF

[ Single PDF file] (75 KB)

PDF

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error