Measles virus-induced modulation of host-cell gene expression Free

Abstract

The influence of measles virus (MV) infection on gene expression by human peripheral blood mononuclear cells (PBMCs) was examined with cDNA microarrays. The mRNA levels of more than 3000 cellular genes were compared between uninfected PBMCs and cells infected with either the Edmonston MV strain or a wild-type MV isolate. The MV-induced upregulation of individual genes identified by microarray analyses was confirmed by RT–PCR. In the present study, a total of 17 genes was found to be upregulated by MV infection. The Edmonston strain grew better in the PBMC cultures than the wild-type MV, and the Edmonston strain was a stronger inducer of the upregulated host cell genes than the wild-type virus. The anti-apoptotic B cell lymphoma 3 (Bcl-3) protein and the transcription factor NF-κB p52 subunit were upregulated in infected PBMCs both at the mRNA and at the protein level. Several genes of the interferon system including that for interferon regulatory factor 7 were upregulated by MV. The genes for a number of chaperones, transcription factors and other proteins of the endoplasmic reticulum stress response were also upregulated. These included the gene for the pro-apoptotic and growth arrest-inducing CHOP/GADD153 protein. Thus, the present study demonstrated the activation by MV of cellular mechanisms and pathways that may play a role in the pathogenesis of measles.

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2002-05-01
2024-03-28
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References

  1. Barone M. V., Crozat A., Tabaee A., Philipson L., Ron D. 1994; CHOP (GADD153) and its oncogenic variant, TLS-CHOP, have opposing effects on the induction of G1/S arrest. Genes & Development 8:453–464
    [Google Scholar]
  2. Bolt G. 2001; The measles virus (MV) glycoproteins interact with cellular chaperones in the endoplasmic reticulum and MV infection upregulates chaperone expression. Archives of Virology 146:2055–2068
    [Google Scholar]
  3. Borrow P., Oldstone M. B. A. 1995; Measles virus-mononuclear cell interactions. Current Topics in Microbiology and Immunology 191:85–100
    [Google Scholar]
  4. Bours V., Franzoso G., Azarenko V., Park S., Kanno T., Brown K., Siebenlist U. 1993; The oncoprotein Bcl-3 directly transactivates through κB motifs via association with DNA-binding p50B homodimers. Cell 72:729–739
    [Google Scholar]
  5. Cattaneo R., Rose J. K. 1993; Cell fusion by the envelope glycoproteins of persistent measles viruses which causes lethal human brain diseases. Journal of Virology 67:1493–1502
    [Google Scholar]
  6. Eisen M. B., Brown P. O. 1999; DNA arrays for analysis of gene expression. Methods in Enzymology 303:179–205
    [Google Scholar]
  7. Enders J. F., Peebles T. C. 1954; Propagation in tissue cultures of cytopathogenic agents from patients with measles. Proceedings of the Society for Experimental Biology and Medicine 86:277–286
    [Google Scholar]
  8. Esolen L. M., Park S. W., Hardwick J. M., Griffin D. E. 1995; Apoptosis as a cause of death in measles virus-infected cells. Journal of Virology 69:3955–3958
    [Google Scholar]
  9. Fawcett T. W., Martindale J. L., Guyton K. Z., Hai T., Holbrook N. J. 1999; Complexes containing activation transcription factor (ATF)/cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochemical Journal 339:135–141
    [Google Scholar]
  10. Franzoso G., Bours V., Park S., Tomita-Yamaguchi M., Kelly K., Siebenlist U. 1992; The candidate oncoprotein Bcl-3 is an antagonist of p50/NF-κB-mediated inhibition. Nature 359:339–342
    [Google Scholar]
  11. Fugier-Vivier I., Servet-Delprat C., Rivailler P., Rissoan M.-C., Liu Y.-J., Rabourdin-Combe C. 1997; Measles virus suppresses cell-mediated immunity by interfering with the survival and functions of dendritic and T cells. Journal of Experimental Medicine 186:813–823
    [Google Scholar]
  12. Ghosh S., May M. J., Kopp E. P. 1998; NF-κB and Rel proteins: evolutionary conserved mediators of immune responses. Annual Review of Immunology 16:225–260
    [Google Scholar]
  13. Griffin D. E., Ward B. J., Esolen L. M. 1994; Pathogenesis of measles virus infection: an hypothesis for altered immune responses. Journal of Infectious Diseases 170 (Suppl. 1):S24–S31
    [Google Scholar]
  14. Grosjean I., Caux C., Bella C., Berger I., Wild F., Banchereau J., Kaiserlian D. 1997; Measles virus infects human dendritic cells and blocks their allostimulatory properties for CD4+ T cells. Journal of Experimental Medicine 186:801–812
    [Google Scholar]
  15. Hu A., Kövamees J., Norrby E. 1994; Intracellular processing and antigenic maturation of measles virus hemagglutinin protein. Archives of Virology 136:239–253
    [Google Scholar]
  16. Kaufman R. J. 1999; Stress signalling from the lumen of the endoplasmic reticulum: coordination of gene transcription and translational controls. Genes & Development 13:1211–1233
    [Google Scholar]
  17. Khodarev N. N., Advani S. J., Gupta N., Roizman B., Weichselbaum R. R. 1999; Accumulation of specific RNAs encoding transcriptional factors and stress response proteins against a background of severe depletion of cellular RNAs in cells infected with herpes simplex virus 1. Proceedings of the National Academy of Sciences, USA 96:12062–12067
    [Google Scholar]
  18. Kokame K., Agarwala K. L., Kato H., Miyata T. 2000; Herp, a new ubiquitin-like membrane protein induced by endoplasmic reticulum stress. Journal of Biological Chemistry 275:32846–32853
    [Google Scholar]
  19. Mastroberadino K., Spindler B., Pfeiffer R., Skelly P. J., Loffings J., Shoemaker C. B., Verrey F. 1998; Amino-acid transport by heterodimers of 4F2hc/CD98 and members of a permease family. Nature 395:288–291
    [Google Scholar]
  20. McChesney M. B., Kehrl J. H., Valsamakis A., Fauci A. S., Oldstone M. B. A. 1987; Measles virus infection of B lymphocytes permits cellular activation but blocks progression through the cell cycle. Journal of Virology 61:3441–3447
    [Google Scholar]
  21. Mirchamsy H., Rapp F. 1969; Role of interferon in replication of virulent and attenuated strains of measles. Journal of General Virology 4:513–522
    [Google Scholar]
  22. Mitchell T. C., Hildeman D., Kedl R. M., Teague T. G., Schaefer B. C., White J., Zhu Y., Kappler J., Marrack P. 2001; Immunological adjuvants promote activated T cell survival via induction of Bcl-3. Nature Immunology 2:397–402
    [Google Scholar]
  23. Molinari M., Helenius A. 1999; Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells. Nature 402:90–93
    [Google Scholar]
  24. Nakaya T., Sato M., Hata N., Asagiri M., Suemori H., Noguchi S., Tanaka N., Taniguchi T. 2001; Gene induction pathways mediated by distinct IRFs during viral infection. Biochemical and Biophysical Research Communications 283:1150–1156
    [Google Scholar]
  25. Naniche D., Reed S. I., Oldstone M. B. A. 1999; Cell cycle arrest during measles virus infection: a G0-like block leads to suppression of retinoblastoma protein expression. Journal of Virology 73:1894–1901
    [Google Scholar]
  26. Naniche D., Yeh A., Eto D., Manchester M., Friedman R. M., Oldstone M. B. A. 2000; Evasion of host defences by measles virus: wild-type measles virus infection interferes with induction of alpha/beta interferon production. Journal of Virology 74:7478–7484
    [Google Scholar]
  27. Nees M., Geoghegan J. M., Hyman T., Frank S., Miller L., Woodworth C. L. 2001; Papillomavirus type 16 oncogenes downregulate expression of interferon-responsive genes and upregulate proliferation-associated and NF-κB-responsive genes in cervical keratinocytes. Journal of Virology 75:4283–4296
    [Google Scholar]
  28. Nielsen L., Blixenkrone-Møller M., Thylstrup M., Hansen N. J. V., Bolt G. 2001; Adaptation of wild-type measles virus to CD46 receptor usage. Archives of Virology 146:197–208
    [Google Scholar]
  29. Nolan G. P., Fujita T., Bhatia K., Huppi C., Liou H.-C., Scott M. L., Baltimore D. 1993; The bcl-3 proto-oncogene encodes a nuclear IκB-like molecule that preferentially interacts with NF-κB p50 and p52 in a phosphorylation-dependent manner. Molecular and Cellular Biology 13:3557–3566
    [Google Scholar]
  30. O’Brien V. 1998; Viruses and apoptosis. Journal of General Virology 79:1833–1845
    [Google Scholar]
  31. Ogura H., Sato H., Kamiya S., Nakamura S. 1991; Glycosylation of measles virus hemagglutinin protein in infected cells. Journal of General Virology 72:2679–2684
    [Google Scholar]
  32. Okada H., Kobune F., Sato T. A., Kohama T., Takeuchi Y., Abe T., Takayma N., Tsuchiya T., Tashiro M. 2000; Extensive lymphopenia due to apoptosis of uninfected lymphocytes in acute measles patients. Archives of Virology 145:905–920
    [Google Scholar]
  33. Okamoto K., Tsurudome M., Ohgimoto S., Kawano M., Nishio M., Komada H., Ito M., Sakakura Y., Ito Y. 1997; An anti-fusion regulatory protein-1 monoclonal antibody suppresses human parainfluenza virus type 2-induced cell fusion. Journal of General Virology 78:83–89
    [Google Scholar]
  34. Oliver J. D., Roderick H. L., Llewellyn D. H., High S. 1999; ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin. Molecular Biology of the Cell 10:2573–2582
    [Google Scholar]
  35. Parker R., Phan T., Baumeister P., Roy B., Cheriyath V., Roy A. L., Lee A. S. 2001; Identification of TFII-I as the endoplasmic reticulum stress response element binding factor ERSF: its autoregulation by stress and interaction with ATF6. Molecular and Cellular Biology 21:3220–3233
    [Google Scholar]
  36. Rebollo A., Dumoutier L., Renauld J.-C., Zaballos A., Ayllon V., Martineza C. 2000; Bcl-3 expression promotes cell survival following interleukin-4 deprivation and is controlled by AP1 and AP1-like transcription factors. Molecular and Cellular Biology 20:3407–3416
    [Google Scholar]
  37. Rota J. S., Wang Z.-D., Rota P. A., Bellini W. J. 1994; Comparison of sequences of the H, F, and N coding genes of measles virus vaccine strains. Virus Research 31:317–330
    [Google Scholar]
  38. Schmid A., Cattaneo R., Billeter M. A. 1987; A procedure for selective full length cDNA cloning of specific RNA species. Nucleic Acid Research 15:3987–3996
    [Google Scholar]
  39. Schneider-Schaulies S., ter Meulen V. 1999; Pathogenic aspects of measles virus infections. Archives of Virology Supplement 15:139–158
    [Google Scholar]
  40. Schneider-Schaulies J., Schneider-Schaulies S., ter Meulen V. 1993; Differential induction of cytokines by primary and persistent measles virus infections in human glial cells. Virology 195:219–228
    [Google Scholar]
  41. Schnorr J.-J., Seufert M., Schlender J., Borst J., Johnston I. C. D., ter Meulen V., Schneider-Schaulies S. 1997; Cell cycle arrest rather than apoptosis is associated with measles virus contact-mediated immunosuppression in vitro . Journal of General Virology 78:3217–3226
    [Google Scholar]
  42. Servant M. J., ten Oever B., LePage C., Conti L., Gessani S., Julkunen I., Lin R., Hiscott J. 2001; Identification of distinct signalling pathways leading to the phosphorylation of interferon regulatory factor 3. Journal of Biological Chemistry 276:355–363
    [Google Scholar]
  43. Sheshberadaran H., Chen S.-N., Norrby E. 1983; Monoclonal antibodies against five structural components of measles virus. Virology 128:341–353
    [Google Scholar]
  44. Soilu-Hänninen M., Hänninen A., Ilonen J., Salmi A., Salonen R. 1996; Measles virus hemagglutinin mediates monocyte aggregation and increased adherence to measles-infected endothelial cells. Medical Microbiology and Immunology 185:73–80
    [Google Scholar]
  45. Taylor L. A., Carthy C. M., Yang D., Saad K., Wong D., Schreiner G., Stanton L. W., McManus M. B. 2000; Host gene regulation during coxsackievirus B3 infection in mice. Circulation Research 87:328–334
    [Google Scholar]
  46. Tilles J. G., Balkville F., Davilla J. 1987; 2′,5′-oligoadenylate synthetase and interferon in peripheral blood after rubella, measles, or mumps live virus vaccine. Proceedings of the Society for Experimental Biology and Medicine 186:70–74
    [Google Scholar]
  47. Volckaert-Vervliet G., Heremans H., De Ley M., Billau A. 1978; Interferon induction and action in human lymphoblastoid cells infected with measles virus. Journal of General Virology 41:459–466
    [Google Scholar]
  48. World Health Organization 2000 The World Health Report Geneva: WHO;
    [Google Scholar]
  49. Zhu H., Cong J.-P., Mamtora G., Gingeras T., Shenk T. 1998; Cellular gene expression altered by human cytomegalovirus: global monitoring with oligonucleotide arrays. Proceedings of the National Academy of Sciences, USA 95:14470–14475
    [Google Scholar]
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