Journal of Microbiology

  • 제44권2호
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  • Pages.217-225
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  • 2006
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  • 1225-8873(pISSN)
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  • 1976-3794(eISSN)
한국미생물학회 (The Microbiological Society of Korea)
권호 표지

Notch Signal Transduction Induces a Novel Profile of Kaposi's Sarcoma-Associated Herpesvirus Gene Expression

  • Chang Hee-Soon (Department of Microbiology and Molecular Genetics and Tumor Virology Division, New England Primate Research Center, Harvard Medical School)
  • 발행 : 2006.04.01
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초록

Kaposi's sarcoma-associated herpesvirus (KSHV) RTA transcription factor is recruited to its responsive elements through interaction with RBP-Jk that is a downstream transcription factor of the Notch signaling pathway that is important in development and cell fate determination. This suggests that KSHV RTA mimics cellular Notch signal transduction to activate viral lytic gene expression. Here, I demonstrated that unlike other B lymphoma cells, KSHV -infected primary effusion lymphoma BCBL1 cells displayed the constitutive activation of ligand-mediated Notch signal transduction, evidenced by the Jagged ligand expression and the complete proteolytic process of Notch receptor I. In order to investigate the effect of Notch signal transduction on KSHV gene expression, human Notch intracellular (hNIC) domain that constitutively activates RBP-Jk transcription factor activity was expressed in BCBL1 cells, TRExBCBL1-hNIC, in a tetracycline inducible manner. Gene expression profiling showed that like RTA, hNIC robustly induced expression of a number of viral genes including KS immune modulatory gene resulting in downregulation of MHC I and CD54 surface expression. Finally, the genetic analysis of KSHV genome demonstrated that the hNIC-mediated expression of KS during viral latency consequently conferred the downregulation of MHC I and CD54 surface expression. These results indicate that cellular. Notch signal transduction provides a novel expression profiling of KSHV immune deregulatory gene that consequently confers the escape of host immune surveillance during viral latency.

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참고문헌

  1. Boshoff, C., T.F. Schulz, M.M. Kennedy, A.K. Graham, C. Fisher, A. Thomas, J.O. McGee, R.A. Weiss, and J.J. O'Leary. 1995. Kaposi's sarcoma-associated herpesvirus infects endothelial and spindle cells. Nat. Med. 1, 1274-1278 https://doi.org/10.1038/nm1295-1274
  2. Cesarman, E., Y. Chang, P.S. Moore, J.W. Said, and D.M. Knowles. 1995. Kaposi's sarcoma-associated herpesviruslike DNA sequences in AIDS-related body-cavity-based lymphomas. N. Engl. J. Med. 332, 1186-1191 https://doi.org/10.1056/NEJM199505043321802
  3. Chang, H., D.P. Dittmer, Y.C. Shin, Y. Hong, and J.U. Jung. 2005. Role of Notch signal transduction in Kaposi's sarcoma-associated herpesvirus gene expression. J. Virol. 79, 14371-14382 https://doi.org/10.1128/JVI.79.22.14371-14382.2005
  4. Chang, H., Y. Gwack, D. Kingston, J. Souvlis, X. Liang, R.E. Means, E. Cesarman, L. Hutt-Fletcher and, J.U. Jung. 2005. Activation of CD21 and CD23 gene expression by Kaposi's sarcoma-associated herpesvirus RTA. J. Virol. 79, 4651-4663 https://doi.org/10.1128/JVI.79.8.4651-4663.2005
  5. Chang, Y., E. Cesarman, M.S. Pessin, F. Lee, J. Culpepper, D. M. Knowles, and P.S. Moore. 1994. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266, 1865-1869 https://doi.org/10.1126/science.7997879
  6. Coscoy, L., and D. Ganem. 2000. Kaposi's sarcoma-associated herpesvirus encodes two proteins that block cell surface display of MHC class I chains by enhancing their endocytosis. Proc. Natl. Acad. Sci. USA 97, 8051-8056
  7. Coscoy, L., D.J. Sanchez, and D. Ganem. 2001. A novel class of herpesvirus-encoded membrane-bound E3 ubiquitin ligases regulates endocytosis of proteins involved in immune recognition. J. Cell Biol. 155, 1265-1273 https://doi.org/10.1083/jcb.200111010
  8. Curry, C.L., L.L. Reed, T.E. Golde, L. Miele, B.J. Nickoloff, and K.E. Foreman. 2005. Gamma secretase inhibitor blocks Notch activation and induces apoptosis in Kaposi's sarcoma tumor cells. Oncogene 24, 6333-6344 https://doi.org/10.1038/sj.onc.1208783
  9. Gradoville, L., J. Gerlach, E. Grogan, D. Shedd, S. Nikiforow, C. Metroka, and G. Miller. 2000. Kaposi's sarcoma-associated herpesvirus open reading frame 50/Rta protein activates the entire viral lytic cycle in the HH-B2 primary effusion lymphoma cell line. J. Virol. 74, 6207-6212 https://doi.org/10.1128/JVI.74.13.6207-6212.2000
  10. Hamaguchi, Y., Y. Yamamoto, H. Iwanari, S. Maruyama, T. Furukawa, N. Matsunami, and T. Honjo. 1992. Biochemical and immunological characterization of the DNA binding protein (RBP-J kappa) to mouse J kappa recombination signal sequence. J. Biochem. (Tokyo) 112, 314-320 https://doi.org/10.1093/oxfordjournals.jbchem.a123898
  11. Hayward, G.S. 2003. Initiation of angiogenic Kaposi's sarcoma lesions. Cancer Cell 3, 1-3 https://doi.org/10.1016/S1535-6108(03)00002-3
  12. Hsieh, J.J., and S.D. Hayward. 1995. Masking of the CBF1/ RBPJ kappa transcriptional repression domain by Epstein- Barr virus EBNA2. Science 268, 560-563 https://doi.org/10.1126/science.7725102
  13. Ishido, S., C. Wang, B.S. Lee, G.B. Cohen, and J.U. Jung. 2000. Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J. Virol. 74, 5300-5309 https://doi.org/10.1128/JVI.74.11.5300-5309.2000
  14. Kawaichi, M., C. Oka, S. Shibayama, A.E. Koromilas, N. Matsunami, Y. Hamaguchi, and T. Honjo. 1992. Genomic organization of mouse J kappa recombination signal binding protein (RBP-J kappa) gene. J. Biol. Chem. 267, 4016-4022
  15. Liang, Y., J. Chang, S.J. Lynch, D.M. Lukac, and D. Ganem. 2002. The lytic switch protein of KSHV activates gene expression via functional interaction with RBP-Jkappa (CSL), the target of the Notch signaling pathway. Genes Dev. 16, 1977-1989 https://doi.org/10.1101/gad.996502
  16. Liang, Y., and D. Ganem. 2003. Lytic but not latent infection by Kaposi's sarcoma-associated herpesvirus requires host CSL protein, the mediator of Notch signaling. Proc. Natl. Acad. Sci. USA 100, 8490-8495
  17. Liang, Y., and D. Ganem. 2004. RBP-J (CSL) is essential for activation of the K14/vGPCR promoter of Kaposi's sarcoma-associated herpesvirus by the lytic switch protein RTA. J. Virol. 78, 6818-6826 https://doi.org/10.1128/JVI.78.13.6818-6826.2004
  18. Ling, P.D., and S.D. Hayward. 1995. Contribution of conserved amino acids in mediating the interaction between EBNA2 and CBF1/RBPJk. J. Virol. 69, 1944-1950
  19. Lukac, D.M., R. Renne, J.R. Kirshner, and D. Ganem. 1998. Reactivation of Kaposi's sarcoma-associated herpesvirus infection from latency by expression of the ORF 50 transactivator, a homolog of the EBV R protein. Virology 252, 304-312 https://doi.org/10.1006/viro.1998.9486
  20. Means, R.E., S. Ishido, X. Alvarez, and J.U. Jung. 2002. Multiple endocytic trafficking pathways of MHC class I molecules induced by a Herpesvirus protein. EMBO J. 21, 1638-1649 https://doi.org/10.1093/emboj/21.7.1638
  21. Nakamura, H., M. Lu, Y. Gwack, J. Souvlis, S.L. Zeichner, and J.U. Jung. 2003. Global changes in Kaposi's sarcomaassociated virus gene expression patterns following expression of a tetracycline-inducible Rta transactivator. J. Virol. 77, 4205-4220 https://doi.org/10.1128/JVI.77.7.4205-4220.2003
  22. Neipel, F., J.C. Albrecht, and B. Fleckenstein. 1997. Cellhomologous genes in the Kaposi's sarcoma-associated rhadinovirus human herpesvirus 8: determinants of its pathogenicity? J. Virol. 71, 4187-4192
  23. Nicholas, J., V. Ruvolo, J. Zong, D. Ciufo, H.G. Guo, M. S. Reitz, and G.S. Hayward. 1997. A single 13-kilobase divergent locus in the Kaposi sarcoma-associated herpesvirus (human herpesvirus 8) genome contains nine open reading frames that are homologous to or related to cellular proteins. J. Virol. 71, 1963-1974
  24. Papin, J., W. Vahrson, R. Hines-Boykin, and D.P. Dittmer. 2005. Real-time quantitative PCR analysis of viral transcription. Methods Mol. Biol. 292, 449-480
  25. Radtke, F., and K. Raj. 2003. The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nat. Rev. Cancer 3, 756-767 https://doi.org/10.1038/nrc1186
  26. Russo, J.J., R.A. Bohenzky, M.C. Chien, J. Chen, M. Yan, J.P. Maddalena Parry, D. Peruzzi, I.S. Edelman, Y. Chang, and P.S. Moore. 1996. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc. Natl. Acad. Sci. USA 93, 14862-14867
  27. Sanchez, D.J., L. Coscoy, and D. Ganem. 2002. Functional organization of MIR2, a novel viral regulator of selective endocytosis. J. Biol. Chem. 277, 6124-6130 https://doi.org/10.1074/jbc.M110265200
  28. Song, M.J., X. Li, H.J. Brown, and R. Sun. 2002. Characterization of interactions between RTA and the promoter of polyadenylated nuclear RNA in Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8. J. Virol. 76, 5000-5013 https://doi.org/10.1128/JVI.76.10.5000-5013.2002
  29. Staudt, M.R., Y. Kanan, J.H. Jeong, J.F. Papin, R. Hines-Boykinand, and D.P. Dittmer. 2004. The tumor microenvironment controls primary effusion lymphoma growth in vivo. Cancer Res. 64, 4790-4799 https://doi.org/10.1158/0008-5472.CAN-03-3835
  30. Sun, R., S.F. Lin, L. Gradoville, Y. Yuan, F. Zhu, and G. Miller. 1998. A viral gene that activates lytic cycle expression of Kaposi's sarcoma-associated herpesvirus. Proc. Natl. Acad. Sci. USA 95, 10866-10871
  31. Sun, R., S.F. Lin, K. Staskus, L. Gradoville, E. Grogan, A. Haase, and G. Miller. 1999. Kinetics of Kaposi's sarcomaassociated herpesvirus gene expression. J. Virol. 73, 2232- 2242
  32. Tomescu, C., W.K. Law, and D.H. Kedes. 2003. Surface downregulation of major histocompatibility complex class I, PE-CAM, and ICAM-1 following de novo infection of endothelial cells with Kaposi's sarcoma-associated herpesvirus. J. Virol. 77, 9669-9684 https://doi.org/10.1128/JVI.77.17.9669-9684.2003
  33. Ye, F.C., F.C. Zhou, S.M. Yoo, J.P. Xie, P.J. Browning, and S.J. Gao. 2004. Disruption of Kaposi's sarcoma-associated herpesvirus latent nuclear antigen leads to abortive episome persistence. J. Virol. 78, 11121-11129 https://doi.org/10.1128/JVI.78.20.11121-11129.2004
  34. Zhou, F.C., Y.J. Zhang, J.H. Deng, X.P. Wang, H.Y. Pan, E. Hettler, and S.J. Gao. 2002. Efficient infection by a recombinant Kaposi's sarcoma-associated herpesvirus cloned in a bacterial artificial chromosome: application for genetic analysis. J. Virol. 76, 6185-6196 https://doi.org/10.1128/JVI.76.12.6185-6196.2002