1887

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Volume 84, Issue 1

Transcriptome profile of murine gammaherpesvirus-68 lytic infection Free

Abstract

The murine gammaherpesvirus-68 genome encodes 73 protein-coding open reading frames with extensive similarities to human γ herpesviruses, as well as unique genes and cellular homologues. We performed transcriptome analysis of stage-specific viral RNA during permissive infection using an oligonucleotide-based microarray. Using this approach, M4, K3, ORF38, ORF50, ORF57 and ORF73 were designated as immediate-early genes based on cycloheximide treatment. The microarray analysis also identified 10 transcripts with early expression kinetics, 32 transcripts with early-late expression kinetics and 29 transcripts with late expression kinetics. The latter group consisted mainly of structural proteins, and showed high expression levels relative to other viral transcripts. Moreover, we detected all eight tRNA-like transcripts in the presence of cycloheximide and phosphonoacetic acid. Lytic infection with MHV-68 also resulted in a significant reduction in the expression of cellular transcripts included in the DNA chip. This global approach to viral transcript analysis offers a powerful system for examining molecular transitions between lytic and latent virus infections associated with disease pathogenesis.

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2003-01-01
2024-04-19
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References

  1. Ahn W. A., Powell K. L., Kellam P., Alber D. G. 2002; Gammaherpesvirus lytic gene expression as characterized by DNA array. J Virol 76:6244–6256
     [Google Scholar]
  2. Albrecht J. C., Fleckenstein B. 1992; Nucleotide sequence of HSUR 6 and HSUR 7, two small RNAs of herpesvirus saimiri. Nucleic Acids Res 20:1810
     [Google Scholar]
  3. Bowden R. J., Simas J. P., Davis A. J., Efstathiou S. 1997; Murine gammaherpesvirus 68 encodes tRNA-like sequences which are expressed during latency. J Gen Virol 78:1675–1687
     [Google Scholar]
  4. Bridgeman A., Stevenson P. G., Simas J. P., Efstathiou S. 2001; A secreted chemokine binding protein encoded by murine gammaherpesvirus-68 is necessary for the establishment of a normal latent load. J Exp Med 194:301–312
     [Google Scholar]
  5. Chambers J., Angulo A., Amaratunga D. 9 other authors 1999; DNA microarrays of the complex human cytomegalovirus genome: profiling kinetic class with drug sensitivity of viral gene expression. J Virol 73:5757–5766
     [Google Scholar]
  6. Efstathiou S., Ho Y. M., Hall S., Styles C. J., Scott S. D., Gompels U. A. 1990a; Murine herpesvirus 68 is genetically related to the gammaherpesviruses Epstein–Barr virus and herpesvirus saimiri. J Gen Virol 71:1365–1372
     [Google Scholar]
  7. Efstathiou S., Ho Y. M., Minson A. C. 1990b; Cloning and molecular characterization of the murine herpesvirus 68 genome. J Gen Virol 71:1355–1364
     [Google Scholar]
  8. Eisen M. B., Brown P. O. 1999; DNA arrays for analysis of gene expression. Methods Enzymol 303:179–205
     [Google Scholar]
  9. Howe J. G., Shu M. D. 1989; Epstein–Barr virus small RNA (EBER) genes: unique transcription units that combine RNA polymerase II and III promoter elements. Cell 57:825–834
     [Google Scholar]
  10. Husain S. M., Usherwood E. J., Dyson H., Coleclough C., Coppola M. A., Woodland D. L., Blackman M. A., Stewart J. P., Sample J. T. 1999; Murine gammaherpesvirus M2 gene is latency-associated and its protein a target for CD8+ T lymphocytes. Proc Natl Acad Sci U S A 96:7508–7513
     [Google Scholar]
  11. Jenner R. G., Alba M. M., Boshoff C., Kellam P. 2001; Kaposi's sarcoma-associated herpesvirus latent and lytic gene expression as revealed by DNA arrays. J Virol 75:891–902
     [Google Scholar]
  12. Kapadia S. B., Molina H., van Berkel V., Speck S. H., Virgin H. W. IV 1999; Murine gammaherpesvirus 68 encodes a functional regulator of complement activation. J Virol 73:7658–7670
     [Google Scholar]
  13. Liu S., Pavlova I. V., Virgin H. W. IV., Speck S. H. 2000; Characterization of gammaherpesvirus 68 gene 50 transcription. J Virol 74:2029–2037
     [Google Scholar]
  14. Mackett M., Stewart J. P., Pepper S. de V., Chee M., Efstathiou S., Nash A. A., Arrand J. R. 1997; Genetic content and preliminary transcriptional analysis of a representative region of murine gammaherpesvirus 68. J Gen Virol 78:1425–1433
     [Google Scholar]
  15. Mathews M. B. 1995; Structure, function, and evolution of adenovirus virus-associated RNAs. Curr Top Microbiol Immunol 199:173–187
     [Google Scholar]
  16. Nash A. A., Dutia B. M., Stewart J. P., Davison A. J. 2001; Natural history of murine gamma-herpesvirus infection. Philos Trans R Soc Lond B Biol Sci 356:569–579
     [Google Scholar]
  17. Parry C. M., Simas J. P., Smith V. P., Stewart C. A., Minson A. C., Efstathiou S., Alcami A. 2000; A broad spectrum secreted chemokine-binding protein encoded by a herpesvirus. J Exp Med 191:573–578
     [Google Scholar]
  18. Paulose-Murphy M., Ha N. K., Xiang C., Chen Y., Gillim L., Yarchoan R., Meltzer P., Bittner M., Trent J., Zeichner S. 2001; Transcription program of human herpesvirus 8 (Kaposi's sarcoma-associated herpesvirus). J Virol 75:4843–4853
     [Google Scholar]
  19. Rochford R., Lutzke M. L., Alfinito R. S., Clavo A., Cardin R. D. 2001; Kinetics of murine gammaherpesvirus 68 gene expression following infection of murine cells in culture and in mice. J Virol 75:4955–4963
     [Google Scholar]
  20. Roy D. J., Ebrahimi B., Dutia B. M., Nash A. A., Stewart J. P. 2000; Murine gammaherpesvirus M11 gene product inhibits apoptosis and is expressed during virus persistence. Arch Virol 145:2411–2420
     [Google Scholar]
  21. Sarid R., Flore O., Bohenzky R. A., Chang Y., Moore P. S. 1998; Transcription mapping of the Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) genome in a body cavity-based lymphoma cell line (BC-1). J Virol 72:1005–1012
     [Google Scholar]
  22. Schek N., Bachenheimer S. L. 1985; Degradation of cellular mRNA induced by a virion-associated factor during herpes simplex virus infection of Vero cells. J Virol 55:601–610
     [Google Scholar]
  23. Simas J. P., Bowden R. J., Paige V., Efstathiou S. 1998; Four tRNA-like sequences and a serpin homologue encoded by murine gammaherpesvirus 68 are dispensable for lytic replication in vitro and latency in vivo. J Gen Virol 79:149–153
     [Google Scholar]
  24. Stevenson P. G., Efstathiou S., Doherty P. C., Lehner P. J. 2000; Inhibition of MHC class I-restricted antigen presentation by gamma 2-herpesviruses. Proc Natl Acad Sci U S A 97:8455–8460
     [Google Scholar]
  25. Stewart J. P., Janjua N. J., Sunil-Chandra N. P., Nash A. A., Arrand J. R. 1994; Characterization of murine gammaherpesvirus 68 glycoprotein B (gB) homolog: similarity to Epstein–Barr virus gB (gp110). J Virol 68:6496–6504
     [Google Scholar]
  26. Stewart J. P., Janjua N. J., Pepper S. de V., Bennion G., Mackett M., Allen T., Nash A. A., Arrand J. R. 1996; Identification and characterization of murine gammaherpesvirus 68 gp 150: a virion membrane glycoprotein. J Virol 70:3528–3535
     [Google Scholar]
  27. Stingley S. W., Ramirez J. J., Aguilar S. A., Simmen K., Sandri-Goldin R. M., Ghazal P., Wagner E. K. 2000; Global analysis of herpes simplex virus type 1 transcription using an oligonucleotide-based DNA microarray. J Virol 74:9916–9927
     [Google Scholar]
  28. Sun R., Lin S. F., Staskus K., Gradoville L., Grogan E., Haase A., Miller G. 1999; Kinetics of Kaposi's sarcoma-associated herpesvirus gene expression. J Virol 73:2232–2242
     [Google Scholar]
  29. van Berkel V., Preiter K., Virgin H. W. IV., Speck S. H. 1999; Identification and initial characterization of the murine gammaherpesvirus 68 gene M3, encoding an abundantly secreted protein. J. Virol 73:4524–4529
     [Google Scholar]
  30. van Dyk L. F., Hess J. L., Katz J. D., Jacoby M., Speck S. H., Virgin H. W. IV 1999; The murine gammaherpesvirus 68 v-cyclin gene is an oncogene that promotes cell cycle progression in primary lymphocytes. J Virol 73:5110–5122
     [Google Scholar]
  31. Virgin H. W. IV, Latreille P., Wamsley P., Hallsworth K., Weck K. E., Dal Canto A. J., Speck S. H. 1997; Complete sequence and genomic analysis of murine gammaherpesvirus 68. J Virol 71:5894–5904
     [Google Scholar]
  32. Virgin H. W. IV, Presti R. M., Li X. Y., Liu C., Speck S. H. 1999; Three distinct regions of the murine gammaherpesvirus 68 genome are transcriptionally active in latently infected mice. J Virol 73:2321–2332
     [Google Scholar]
  33. Wakeling M. N., Roy D. J., Nash A. A., Stewart J. P. 2001; Characterization of the murine gammaherpesvirus 68 ORF74 product: a novel oncogenic G protein-coupled receptor. J Gen Virol 82:1187–1197
     [Google Scholar]
  34. Wang G.-H., Garvey T. L., Cohen J. I. 1999; The murine gammaherpesvirus-68 M11 protein inhibits Fas- and TNF-induced apoptosis. J Gen Virol 80:2737–2740
     [Google Scholar]
  35. Wu T. T., Usherwood E. J., Stewart J. P., Nash A. A., Sun R. 2000; Rta of murine gammaherpesvirus 68 reactivates the complete lytic cycle from latency. J Virol 74:3659–3667
     [Google Scholar]
  36. Wu T. T., Tong L., Rickabaugh T., Speck S., Sun R. 2001; Function of Rta is essential for lytic replication of murine gammaherpesvirus 68. J Virol 75:9262–9273
     [Google Scholar]
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Transcriptome profile of murine gammaherpesvirus-68 lytic infection
J. Gen. Virol. 84, 99 (2003); https://doi.org/10.1099/vir.0.18639-0
/content/journal/jgv/10.1099/vir.0.18639-0
/content/journal/jgv/10.1099/vir.0.18639-0
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