ERK5 knockdown generates mouse leukemia cells with low MHC class I levels that activate NK cells and block tumorigenesis

Journal of Immunology

Volumn 182, Issue 6, 2009, Pages 3398-3405

  Charni, Seyma ^a   Aguilo, Juan Ignacio ^b   Garaude, Johan ^a   De Bettignies, Geoffroy ^a   Jacquet, Chantal ^a   Hipskind, Robert A ^a   Singer, Dinah ^c   Anel, Alberto ^b   Villalba, Martin ^a  

^a CNRS   (France)

^b UNIVERSITY OF ZARAGOZA   (Spain)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MITOGEN ACTIVATED PROTEIN KINASE 7; SHORT HAIRPIN RNA; TUMOR CELL VACCINE; CANCER VACCINE; HLA ANTIGEN CLASS 1; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL ACTIVATION; CELL MEMBRANE; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; ENGRAFTMENT; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOBLOTTING; LEUKEMIA CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PERITONEUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; TRANSIENT TRANSFECTION; TUMOR GROWTH; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; DRUG ANTAGONISM; ENZYMOLOGY; GENE SILENCING; GENETICS; HUMAN; IMMUNOLOGY; LEUKEMIA CELL LINE; LEUKEMIA L 1210; LYMPHOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CANCER VACCINES; CELL LINE, TUMOR; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; GENE KNOCKDOWN TECHNIQUES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; JURKAT CELLS; KILLER CELLS, NATURAL; LEUKEMIA L1210; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 7; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 65449148656     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803006     Document Type: Article

References (39)

1. Dunn, G. P., C. M. Koebel, and R. D. Schreiber. 2006. Interferons, immunity and cancer immunoediting. Nat. Rev. Immunol. 6: 836-848.
2. Nguyen van Binh, P., and H. T. Duc. 2006. Analyses and perspectives in cancer immunotherapy. Biomed. Pharmacother. 60: 621-628.
3. Berd, D., H. C. Maguire, Jr., P. McCue, and M. J. Mastrangelo. 1990. Treatment of metastatic melanoma with an autologous tumor-cell vaccine: clinical and immunologic results in 64 patients. J. Clin. Oncol. 8: 1858-1867.
4. Ronchetti, A., P. Rovere, G. Iezzi, G. Galati, S. Heltai, M. P. Protti, M. P. Garancini, A. A. Manfredi, C. Rugarli, and M. Bellone. 1999. Immunogenicity of apoptotic cells in vivo: role of antigen load, antigen-presenting cells, and cytokines. J. Immunol. 163: 130-136.
5. Dzik, W. H. 2003. Apoptosis, TGFβand transfusion-related immunosuppression: biologic versus clinical effects. Transfus. Apher. Sci. 29: 127-129.
6. Terme, M., E. Ullrich, N. F. Delahaye, N. Chaput, and L. Zitvogel. 2008. Natural killer cell-directed therapies: moving from unexpected results to successful strategies. Nat. Immunol. 9: 486-494.
7. Vivier, E., E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini. 2008. Functions of natural killer cells. Nat. Immunol. 9: 503-510.
8. Lanier, L. L. 2008. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 9: 495-502.
9. Glas, R., L. Franksson, C. Une, M. L. Eloranta, C. Ohlen, A. Orn, and K. Karre. 2000. Recruitment and activation of natural killer (NK) cells in vivo determined by the target cell phenotype: an adaptive component of NK cell-mediated responses. J. Exp. Med. 191: 129-138.
10. Hallett, W. H., and W. J. Murphy. 2006. Positive and negative regulation of natural killer cells: therapeutic implications. Semin. Cancer Biol. 16: 367-382.
11. Wodnar-Filipowicz, A., and C. P. Kalberer. 2006. Function of natural killer cells in immune defence against human leukaemia. Swiss Med. Wkly. 136: 359-364.
12. Bryceson, Y. T., M. E. March, H. G. Ljunggren, and E. O. Long. 2006. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 107: 159-166.
13. Wang, X., and C. Tournier. 2006. Regulation of cellular functions by the ERK5 signalling pathway. Cell. Signal. 18: 753-760.
14. Carvajal-Vergara, X., S. Tabera, J. C. Montero, A. Esparis-Ogando, R. Lopez-Perez, G. Mateo, N. Gutierrez, M. Parmo-Cabanas, J. Teixido, J. F. San Miguel, and A. Pandiella. 2005. Multifunctional role of Erk5 in multiple myeloma. Blood 105: 4492-4499.
15. Buschbeck, M., S. Hofbauer, L. D. Croce, G. Keri, and A. Ullrich. 2005. Ablkinase-sensitive levels of ERK5 and its intrinsic basal activity contribute to leukaemia cell survival. EMBO Rep. 6: 63-69.
16. Nagel, S., C. Burek, L. Venturini, M. Scherr, H. Quentmeier, C. Meyer, A. Rosenwald, H. G. Drexler, and R. A. Macleod. 2007. Comprehensive analysis of homeobox genes in Hodgkin lymphoma cell lines identifies dysregulated expression of HOXB9 mediated via ERK5 signaling and BMI1. Blood 109: 3015-3023.
17. Akao, Y., Y. Nakagawa, Y. Kitade, T. Kinoshita, and T. Naoe. 2007. Down-regulation of microRNAs-143 and -145 in B-cell malignancies. Cancer Sci. 98: 1914-1920.
18. Garaude, J., S. Cherni, S. Kaminski, E. Delepine, C. Chable-Bessia, M. Benkirane, J. Borges, A. Pandiella, M. A. Iniguez, M. Fresno, et al. 2006. ERK5 activates NF-κB in leukemic T cells and is essential for their growth in vivo. J. Immunol. 177: 7607-7617.
19. Howcroft, T. K., J. D. Weissman, A. Gegonne, and D. S. Singer. 2005. A T lymphocyte-specific transcription complex containing RUNX1 activates MHC class I expression. J. Immunol. 174: 2106-2115.
20. Pardo, J., S. Balkow, A. Anel, and M. M. Simon. 2002. Granzymes are essential for natural killer cell-mediated and perf-facilitated tumor control. Eur. J. Immunol. 32: 2881-2887.
21. Kasai, M., T. Yoneda, S. Habu, Y. Maruyama, K. Okumura, and T. Tokunaga. 1981. In vivo effect of anti-asialo GM1 antibody on natural killer activity. Nature 291: 334-335.
22. Wallin, R. P., V. Screpanti, J. Michaelsson, A. Grandien, and H. G. Ljunggren. 2003. Regulation of perforin-independent NK cell-mediated cytotoxicity. Eur. J. Immunol. 33: 2727-2735.
23. Simon, M. M., P. Waring, M. Lobigs, A. Nil, T. Tran, R. T. Hla, S. Chin, and A. Mullbacher. 2000. Cytotoxic T cells specifically induce Fas on target cells, thereby facilitating exocytosis-independent induction of apoptosis. J. Immunol. 165: 3663-3672.
24. Mullbacher, A., M. Lobigs, R. T. Hla, T. Tran, T. Stehle, and M. M. Simon. 2002. Antigen-dependent release of IFN-γ by cytotoxic T cells up-regulates Fas on target cells and facilitates exocytosis-independent specific target cell lysis. J. Immunol. 169: 145-150.
25. Esplugues, E., D. Sancho, J. Vega-Ramos, C. Martinez, U. Syrbe, A. Hamann, P. Engel, F. Sanchez-Madrid, and P. Lauzurica. 2003. Enhanced antitumor immunity in mice deficient in CD69. J. Exp. Med. 197: 1093-1106.
26. Diefenbach, A., E. R. Jensen, A. M. Jamieson, and D. H. Raulet. 2001. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 413: 165-171.
27. Aptsiauri, N., T. Cabrera, A. Garcia-Lora, M. A. Lopez-Nevot, F. Ruiz-Cabello, and F. Garrido. 2007. MHC class I antigens and immune surveillance in transformed cells. Int. Rev. Cytol. 256: 139-189.
28. Pardo, J., M. Buferne, M. J. Martinez-Lorenzo, J. Naval, A. M. Schmitt-Verhulst, C. Boyer, and A. Anel. 2003. Differential implication of protein kinase C isoforms in cytotoxic T lymphocyte degranulation and TCR-induced Fas ligand expression. Int. Immunol. 15: 1441-1450.
29. Kreuz, S., D. Siegmund, P. Scheurich, and H. Wajant. 2001. NF-κB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol. Cell. Biol. 21: 3964-3973.
30. Kelly, J. M., P. K. Darcy, J. L. Markby, D. I. Godfrey, K. Takeda, H. Yagita, and M. J. Smyth. 2002. Induction of tumor-specific T cell memory by NK cell-mediated tumor rejection. Nat. Immunol. 3: 83-90.
31. Suck, G. 2006. Novel approaches using natural killer cells in cancer therapy. Semin. Cancer Biol. 16: 412-418.
32. Ruggeri, L., A. Mancusi, E. Burchielli, F. Aversa, M. F. Martelli, and A. Velardi. 2007. Natural killer cell alloreactivity in allogeneic hematopoietic transplantation. Curr. Opin. Oncol. 19: 142-147.
33. Imai, K., S. Matsuyama, S. Miyake, K. Suga, and K. Nakachi. 2000. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 356: 1795-1799.
34. low targets prime dendritic cells to induce protective CD8 T cell responses. Immunity 19: 561-569.
35. Groh, V., J. Wu, C. Yee, and T. Spies. 2002. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419: 734-738.
36. Salih, H. R., H. Antropius, F. Gieseke, S. Z. Lutz, L. Kanz, H. G. Rammensee, and A. Steinle. 2003. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 102: 1389-1396.
37. Figueiredo, C., P. A. Horn, R. Blasczyk, and A. Seltsam. 2007. Regulating MHC expression for cellular therapeutics. Transfusion 47: 18-27.
38. Figueiredo, C., A. Seltsam, and R. Blasczyk. 2006. Class-, gene-, and group-specific HLA silencing by lentiviral shRNA delivery. J. Mol. Med. 84: 425-437.
39. Schowalter, D. B., J. C. Tubb, M. Liu, C. B. Wilson, and M. A. Kay. 1997. Heterologous expression of adenovirus E3-gp19K in an E1a-deleted adenovirus vector inhibits MHC I expression in vitro, but does not prolong transgene expression in vivo. Gene Ther. 4: 351-360.