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Persistent measles virus infection enhances major histocompatibility complex class I expression and immunogenicity of murine neuroblastoma cells

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Abstract

The effect of persistent measles virus infection on the expression of major histocompatibility complex (MHC) class I antigens was studied. Mouse neuroblastoma cells C1300, clone NS20Y, were persistently infected with the Edmonston strain of measles virus. The persistently infected cell line, NS20Y/MS, expressed augmented levels of both H-2Kk and H-2Dd MHC class I glycoproteins. Activation of two interferon(IFN)-induced enzymes, known to be part of the IFN system: (2′–5′)oligoadenylate synthetase and double-stranded-RNA-activated protein kinase, was detected. Measles-virus-infected cells elicited cytotoxic T lymphocytes that recognized and lysed virus-infected and uninfected neuroblastoma cells in an H-2-restricted fashion. Furthermore, immunization of mice with persistently infected cells conferred resistance to tumor growth after challenge with the highly malignant NS20Y cells. The rationale for using measles virus for immunotherapy is that most patients develop lifelong immunity after recovery or vaccination from this infection. Patients developing cancer are likely to have memory cells. A secondary response induced by measles-virus-infected cells may therefore induce an efficient immune response against non-infected tumour cells.

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References

  1. Brodeur GM, Fong C (1989) Molecular biology and genetics of human neuroblastoma. Cancer Genet Cytogenet 41: 153

    PubMed  Google Scholar 

  2. Gopas J, Rager-Zisman B, Hammerling GJ, Bar-Eli M, Segal S (1989) The relationship between MHC gene expression and metastasis. Adv Cancer Res 53: 89

    PubMed  Google Scholar 

  3. Heath WR, Hurd ME, Carbone FR, Sherman LA (1989) Peptide-dependent recognition of H-2Kb by alloreactive cytotoxic T lymphocytes. Nature 341: 749

    PubMed  Google Scholar 

  4. Hect TT, Summers DF (1982) Effect of vesicular stomatitis virus infection on histocompatibility antigens of L cells. J Virol 10: 578

    Google Scholar 

  5. Hoon DSB, Banez M, Okun E, Morton DL, Irie RF (1991) Modulation of human melanoma cells by interleukin-4 in combination with gamma interferon or alpha tumor necrosis factor. Cancer Res 51: 2002

    PubMed  Google Scholar 

  6. Hovanessian AG (1989) The double stranded RNA-activated protein kinase induced by interferons: dsRNA-PK. J Interferon Res 9: 641

    PubMed  Google Scholar 

  7. Hunter WM, Greenwood FC (1962) Preparation of iodine human growth hormone of high specific activity. Nature 194: 495

    PubMed  Google Scholar 

  8. Ito T, Wang D-Q, Marus M, Nakagima K, Kato S, Kurimura T, Wakamiya R (1990) Antitumor efficacy of vaccinia virus modified tumor cell vaccine. Cancer Res 50: 6915

    PubMed  Google Scholar 

  9. Jacobson S, Sekaly RP, Jacobson CL, McFarland HR, Long EO (1989) HLA class II restricted presentation of cytoplasmic measles virus antigens to cytotoxic cells. J Virol 63: 1756

    PubMed  Google Scholar 

  10. Jennings SR, Rice PL, Kloszewski ED, Anderson RW, Thompson DL, Tevethia SS (1985) Effect of herpes simplex types 1 and 2 on surface expression of class I major histocompatibility complex antigens on infected cells. J Virol 55: 77

    Google Scholar 

  11. Ju G, Udem SA, Rager-Zisman B, Bloom BR (1978) Isolation of a heterogenous population of temperature sensitive mutants of measles virus from persistently infected human lymphoblastoid cell lines. J Exp Med 147: 1637

    PubMed  Google Scholar 

  12. Kast WM, Offringa R, Peter PJ, Voordouw AC, Meloen RH, van der Eb, Melief CJM (1989) Eradication of adenovirus E1-induced tumors by EIA specific cytotoxic T lymphocytes. Cell 59: 603

    PubMed  Google Scholar 

  13. Kerber B, Mermod N, Hood L, Stroynowski I (1988) Regulation of gene expression by interferons: control of H-2 promoter responses. Science 239: 130214

    Google Scholar 

  14. Kiessling R, Klein E, Wigzell H (1975) Natural killer cells in the mouse: 1. Cytotoxic cells with specificity for mouse Moloney leukemic cells. Eur J Immunol 5: 112

    PubMed  Google Scholar 

  15. Kronenberg M, Siu G, Hood LE, Shastri N (1986) The molecular genetics of the T-cell antigen receptor and T-cell antigen recognition. Annu Rev Immunol 4: 529

    PubMed  Google Scholar 

  16. Lampson L, Fisher CA (1984) Weak HLA and beta-2-microglobulin expression on neuronal cell lines can be modulated by interferon. Proc Natl Acad Sci USA 81: 6476

    PubMed  Google Scholar 

  17. Long EO (1989) Intracellular traffic and antigen processing. Immunol Today 10: 232

    PubMed  Google Scholar 

  18. Margulis DH (1989) Naked or peptide clothed MHC? Nature 342: 124

    PubMed  Google Scholar 

  19. Offerman MK, Faller DV (1989) Autocrine induction of major histocompatibility complex class I antigen expression results from induction of beta interferon in oncogene-transformed Balb/c-3T3 cells. Mol Cell Biol 9: 1989

    Google Scholar 

  20. Oldstone MBA, Blount P, Southern PJ, Lampert PW (1986) Cytoimmunotherapy for persistent virus infection reveals a unique clearance pattern from the central nervous system. Nature 321: 239

    PubMed  Google Scholar 

  21. Rager-Zisman B, Ju G, Rajan TV, Bloom BR (1981) Decreased expression of H-2 antigens following acute measles virus infection. Cell Immunol 59: 319

    PubMed  Google Scholar 

  22. Rager-Zisman B, Egan J, Kress Y, Bloom BR (1984) Isolation of cold sensitive mutants of measles virus from persistently infected murine neuroblastoma cells. J Virol 51: 845

    PubMed  Google Scholar 

  23. Rotzschke O, Falk K, Deres K, Schild H, Norda M, Metzger J, Jung G, Rammensee HG (1990) Isolation and analysis of naturally processed viral peptides as recognized by cytotoxic T cells. Nature 348: 252

    PubMed  Google Scholar 

  24. Schirrmacher V, Hoegen VP, Schlag P, Liebrich W, Lehner B, Schumacher K, Ahlrert T, Bastert G (1989) Active specific immunotherapy with autologous tumor cell vaccines modified by Newcastle disease virus: experimental and clinical studies. In: Schirrmacher V, Schwartz-Albeiz R (eds) Cancer metastasis, Springer Berlin Heidelberg, pp 157

    Google Scholar 

  25. Sheil JM, Bevan MJ, Lefrancois L (1987) Characterization of dual reactive H-2Kb restricted antivesicular stomatitis virus and alloreactive cytotoxic T cells. J Immunol 138: 3654

    PubMed  Google Scholar 

  26. Shimizu Y, Hasumi K, Kazumasa M, Okudaira Y (1988) Immunotherapy of tumor-bearing mice utilizing virus help. Cancer Immunol Immunother 27: 223

    PubMed  Google Scholar 

  27. Staeheli P (1990) Interferon-induced proteins and the antiviral state. Adv Virus Res 38: 147

    PubMed  Google Scholar 

  28. Sugimoto T, Horii Y, Hino T, Kemshead JT, Kuroda H, Sawada T, Morioka H, Imanishi J, Inoko H (1988) Differential susceptibility of HLA class II antigens induced by gamma-interferon in human neuroblastoma cell lines. Cancer Res 49: 1824

    Google Scholar 

  29. Sweester MT, Morrison LA, Braciale LL, Braciale TJ (1989) Recognition of pre-processed endogenous antigen by class I but not class II restricted cells. Nature 342: 180

    PubMed  Google Scholar 

  30. Tanaka K, Isselbacher KJ, Khoury G, Jay G (1984) Reversal of oncogenesis by the expression of a major histocompatibility complex class I gene. Science 228: 26

    Google Scholar 

  31. Tanaka K, Yoshioka T, Bieberich C, Jay G (1988) Role of major histocompatibility complex class I in tumor growth and metastasis. Annu Rev Immunol 6: 359

    PubMed  Google Scholar 

  32. Taylor PM, Davey J, Howland K, Rothbard JB, Askonas BA (1987) Class I MHC molecules rather than other mouse genes dictate influenza epitope recognition by cytotoxic T cells. Immunogenetics 36: 267

    Google Scholar 

  33. Watanabe Y, Kuribayashi K, Miyatake S, Nishihara K, Nakayama E, Taniyama T, Sakala T (1989) Exogenous expression of mouse interferon gamma cDNA in mouse neuroblastoma C1300 results in reduced tumorigenicity by augmented anti-tumor immunity. Proc Natl Acad Sci USA 86: 9456

    PubMed  Google Scholar 

  34. Wolfson M, Karotza A, Segal S, Rager-Zisman B (1990) Effect of persistent measles virus infection on protein kinase C activity and c-fos protooncogene expression in neuroblastoma cells. FEBS Lett 250: 367

    Google Scholar 

  35. Wong GHW, Bartlett PF, Clark-Lewis I, McKiman-Breschkin JL, Schrader JW (1985) Interferon-gamma induces the expression of H-2 and Ia antigens on brain cells. J Neuroimmunol 7: 255

    PubMed  Google Scholar 

  36. Vaessen RT, Houwelling MJ, Israel A, Kourlisky P, van der Eb AJ (1986) Adenovirus EIA-mediated regulation of class I MHC expression. EMBO J 5: 335

    PubMed  Google Scholar 

  37. Van Bleek GM, Nathenson SG (1990) Isolation of an endogenously processed immunodominant viral peptide from the class I H-2Kb molecule. Nature 348: 213

    PubMed  Google Scholar 

  38. Vasmel WL, Sijts EJAL, Leupers CJM, Matthews EA, Melief CJM (1989) Primary virus induced lymphomas evade T cell immunity by failure to express viral antigens. J Exp Med 169: 1233

    PubMed  Google Scholar 

  39. Weber JS, Rosenberg SA (1988) Modification of murine tumor major histocompatibility antigens by cytokines in vivo and in vitro. Cancer Res 48: 5818

    PubMed  Google Scholar 

  40. Yewdell JW, Bennink JR, Eager KB, Ricciardi RP (1988) CTL recognition of adenovirus-transformed cells infected with influenza virus: lysis of anti-influenza CTL parallels adenovirus 2-induced suppression of class I MHC molecules. Virology 162: 236

    PubMed  Google Scholar 

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Gopas, J., Itzhaky, D., Segev, Y. et al. Persistent measles virus infection enhances major histocompatibility complex class I expression and immunogenicity of murine neuroblastoma cells. Cancer Immunol Immunother 34, 313–320 (1992). https://doi.org/10.1007/BF01741552

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