Elevation of c-MYC disrupts HLA class II-mediated immune recognition of human B cell tumors

Journal of Immunology

Volumn 194, Issue 4, 2015, Pages 1434-1445

  God, Jason M ^a   Cameron, Christine ^a   Figueroa, Janette ^a   Amria, Shereen ^a   Hossain, Azim ^a   Kempkes, Bettina ^b   Bornkamm, Georg W ^c   Stuart, Robert K ^d   Blum, Janice S ^e   Haque, Azizul ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^e INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ENOLASE; ALPHA ENOLASE 1 LIKE PROTEIN; CELL SURFACE PROTEIN; GAMMA INTERFERON INDUCIBLE LYSOSOMAL THIOL REDUCTASE; HLA ANTIGEN CLASS 2; HLA DM ANTIGEN; HLA DO ANTIGEN; MYC PROTEIN; OXIDOREDUCTASE; PROTEIN CLIP; UNCLASSIFIED DRUG; MYC PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ARTICLE; B CELL LYMPHOMA; B CELL LYMPHOMA CELL; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; ONCOGENE C MYC; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR ESCAPE; FLOW CYTOMETRY; IMMUNOLOGY; MASS SPECTROMETRY; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANTIGEN PRESENTATION; BLOTTING, WESTERN; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; LYMPHOMA, B-CELL; MASS SPECTROMETRY; PROTO-ONCOGENE PROTEINS C-MYC; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TUMOR CELLS, CULTURED; TUMOR ESCAPE;

EID: 84922572142     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402382     Document Type: Article

References (92)

1. Vennstrom, B., D. Sheiness, J. Zabielski, and J. M. Bishop. 1982. Isolation and characterization of c-myc, a cellular homolog of the oncogene (v-myc) of avian myelocytomatosis virus strain 29. J. Virol. 42: 773-779.
2. Dang, C. V., K. A. O'Donnell, K. I. Zeller, T. Nguyen, R. C. Osthus, and F. Li. 2006. The c-Myc target gene network. Semin. Cancer Biol. 16: 253-264.
3. Lin, Z., Q. Yin, and E. Flemington. 2004. Identification of a negative regulatory element in the Epstein-Barr virus Zta transactivation domain that is regulated by the cell cycle control factors c-Myc and E2F1. J. Virol. 78: 11962-11971.
4. Allday, M. J. 2009. How does Epstein-Barr virus (EBV) complement the activation of Myc in the pathogenesis of Burkitt's lymphoma? Semin. Cancer Biol. 19: 366-376.
5. Slack, G. W., and R. D. Gascoyne. 2011. MYC and aggressive B-cell lymphomas. Adv. Anat. Pathol. 18: 219-228.
6. Larsson, L. G., and M. A. Henriksson. 2010. The Yin and Yang functions of the Myc oncoprotein in cancer development and as targets for therapy. Exp. Cell Res. 316: 1429-1437.
7. Grandori, C., S. M. Cowley, L. P. James, and R. N. Eisenman. 2000. The Myc/ Max/Mad network and the transcriptional control of cell behavior. Annu. Rev. Cell Dev. Biol. 16: 653-699.
8. Knoepfler, P. S., X. Y. Zhang, P. F. Cheng, P. R. Gafken, S. B. McMahon, and R. N. Eisenman. 2006. Myc influences global chromatin structure. EMBO J. 25: 2723-2734.
9. Meyer, N., and L. Z. Penn. 2008. Reflecting on 25 years with MYC. Nat. Rev. Cancer 8: 976-990.
10. Arabi, A., S. Wu, K. Ridderstråle, H. Bierhoff, C. Shiue, K. Fatyol, S. Fahlén, P. Hydbring, O. Söderberg, I. Grummt, et al. 2005. c-Myc associates with ri-bosomal DNA and activates RNA polymerase I transcription. Nat. Cell Biol. 7: 303-310.
11. Eilers, M., and R. N. Eisenman. 2008. Myc's broad reach. Genes Dev. 22: 2755-2766.
12. Hoffman, B., and D. A. Liebermann. 2008. Apoptotic signaling by c-MYC. Oncogene 27: 6462-6472.
13. Wang, C., M. P. Lisanti, and D. J. Liao. 2011. Reviewing once more the c-myc and Ras collaboration: converging at the cyclin D1-CDK4 complex and challenging basic concepts of cancer biology. Cell Cycle 10: 57-67.
14. Egle, A., A. W. Harris, P. Bouillet, and S. Cory. 2004. Bim is a suppressor of Myc-induced mouse B cell leukemia. Proc. Natl. Acad. Sci. USA 101: 6164-6169.
15. Nesbit, C. E., J. M. Tersak, and E. V. Prochownik. 1999. MYC oncogenes and human neoplastic disease. Oncogene 18: 3004-3016.
16. Dang, C. V., L. M. Resar, E. Emison, S. Kim, Q. Li, J. E. Prescott, D. Wonsey, and K. Zeller. 1999. Function of the c-Myc oncogenic transcription factor. Exp. Cell Res. 253: 63-77.
17. Boxer, L. M., and C. V. Dang. 2001. Translocations involving c-myc and c-myc function. Oncogene 20: 5595-5610.
18. Gerbitz, A., J. Mautner, C. Geltinger, K. Hörtnagel, B. Christoph, H. Asenbauer, G. Klobeck, A. Polack, and G. W. Bornkamm. 1999. Deregulation of the proto-oncogene c-myc through t(8;22) translocation in Burkitt's lymphoma. Oncogene 18: 1745-1753.
19. Robbiani, D. F., and M. C. Nussenzweig. 2013. Chromosome translocation, B cell lymphoma, and activation-induced cytidine deaminase. Annu. Rev. Pathol. 8: 79-103.
20. Mutalima, N., E. Molyneux, H. Jaffe, S. Kamiza, E. Borgstein, N. Mkandawire, G. Liomba, M. Batumba, D. Lagos, F. Gratrix, et al. 2008. Associations between Burkitt lymphoma among children in Malawi and infection with HIV, EBV and malaria: results from a case-control study. PLoS One 3: e2505.
21. Rasti, N., K. I. Falk, D. Donati, B. A. Gyan, B. Q. Goka, M. Troye-Blomberg, B. D. Akanmori, J. A. Kurtzhals, D. Dodoo, R. Consolini, et al. 2005. Circulating epstein-barr virus in children living in malaria-endemic areas. Scand. J. Immunol. 61: 461-465.
22. Njie, R., A. I. Bell, H. Jia, D. Croom-Carter, S. Chaganti, A. D. Hislop, H. Whittle, and A. B. Rickinson. 2009. The effects of acute malaria on Epstein-Barr virus (EBV) load and EBV-specific T cell immunity in Gambian children. J. Infect. Dis. 199: 31-38.
23. Piriou, E., R. Kimmel, K. Chelimo, J. M. Middeldorp, P. S. Odada, R. Ploutz-Snyder, A. M. Moormann, and R. Rochford. 2009. Serological evidence for long-term Epstein-Barr virus reactivation in children living in a holoendemic malaria region of Kenya. J. Med. Virol. 81: 1088-1093.
24. Aldoss, I. T., D. D. Weisenburger, K. Fu, W. C. Chan, J. M. Vose, P. J. Bierman, R. G. Bociek, and J. O. Armitage. 2008. Adult Burkitt lymphoma: advances in diagnosis and treatment. Oncology 22: 1508-1517.
25. Sharipo, A., M. Imreh, A. Leonchiks, S. Imreh, and M. G. Masucci. 1998. A minimal glycine-alanine repeat prevents the interaction of ubiquitinated IκBα with the proteasome: a new mechanism for selective inhibition of proteolysis. Nat. Med. 4: 939-944.
26. + T cells in patients with Epstein-Barr virus-associated naso-pharyngeal carcinoma. Proc. Natl. Acad. Sci. USA 106: 3318-3323.
27. Lee, S. P., J. M. Brooks, H. Al-Jarrah, W. A. Thomas, T. A. Haigh, G. S. Taylor, S. Humme, A. Schepers, W. Hammerschmidt, J. L. Yates, et al. 2004. CD8 T cell recognition of endogenously expressed Epstein-Barr virus nuclear antigen 1. J. Exp. Med. 199: 1409-1420.
28. + T cells in HIV-infected patients progressing to AIDS-related non-Hodgkin lymphoma. Blood 106: 3166-3174.
29. Schlee, M., M. Schuhmacher, M. Hölzel, G. Laux, and G. W. Bornkamm. 2007. c-MYC impairs immunogenicity of human B cells. Adv. Cancer Res. 97: 167-188.
30. Aubert, R. D., A. O. Kamphorst, S. Sarkar, V. Vezys, S. J. Ha, D. L. Barber, L. Ye, A. H. Sharpe, G. J. Freeman, and R. Ahmed. 2011. Antigen-specific CD4 T-cell help rescues exhausted CD8 T cells during chronic viral infection. Proc. Natl. Acad. Sci. USA 108: 21182-21187.
31. + T cells in the control of mouse Burkitt lymphoma in vivo. J. Clin. Invest. 114: 542-550.
32. + cytotoxic T-cell responses during chronic viral infection. J. Virol. 68: 8056-8063.
33. + Th1 cells kill Burkitt's lymphoma cells. J. Immunol. 169: 1593-1603.
34. Khanna, R., S. R. Burrows, P. M. Steigerwald-Mullen, D. J. Moss, M. G. Kurilla, and L. Cooper. 1997. Targeting Epstein-Barr virus nuclear antigen 1 (EBNA1) through the class II pathway restores immune recognition by EBNA1-specific cytotoxic T lymphocytes: evidence for HLA-DM-independent processing. Int. Immunol. 9: 1537-1543.
35. + EBV-specific CTLs. J. Immunol. 158: 3619-3625.
36. + T-cell clones recognizing human lymphoma-associated antigens: generation by in vitro stimulation with autologous Epstein-Barr virus-transformed B cells. Blood 114: 807-815.
37. Saito, N., G. Courtois, A. Chiba, N. Yamamoto, T. Nitta, N. Hironaka, M. Rowe, N. Yamamoto, and S. Yamaoka. 2003. Two carboxyl-terminal activation regions of Epstein-Barr virus latent membrane protein 1 activate NF-κB through distinct signaling pathways in fibroblast cell lines. J. Biol. Chem. 278: 46565-46575.
38. Staege, M. S., S. P. Lee, T. Frisan, J. Mautner, S. Scholz, A. Pajic, A. B. Rickinson, M. G. Masucci, A. Polack, and G. W. Bornkamm. 2002. MYC overexpression imposes a nonimmunogenic phenotype on Epstein-Barr virus-infected B cells. Proc. Natl. Acad. Sci. USA 99: 4550-4555.
39. + invariant chain negative breast cancer cells present unique peptides that activate tumor-specific T cells from breast cancer patients. Mol. Cell. Proteomics 11: 1457-1467.
40. + T lymphocytes. Cancer Immunol. Immunother. 57: 389-398.
41. + T-cell recognition. Immunology 142: 492-505.
42. Kempkes, B., D. Spitkovsky, P. Jansen-Dürr, J. W. Ellwart, E. Kremmer, H. J. Delecluse, C. Rottenberger, G. W. Bornkamm, and W. Hammerschmidt. 1995. B-cell proliferation and induction of early G1-regulating proteins by Epstein-Barr virus mutants conditional for EBNA2. EMBO J. 14: 88-96.
43. Amria, S., C. Cameron, R. Stuart, and A. Haque. 2008. Defects in HLA class II antigen presentation in B-cell lymphomas. Leuk. Lymphoma 49: 353-355.
44. Balkan, W., A. F. Martinez, I. Fernandez, M. A. Rodriguez, M. Pang, and B. R. Troen. 2009. Identification of NFAT binding sites that mediate stimulation of cathepsin K promoter activity by RANK ligand. Gene 446: 90-98.
45. Polack, A., K. Hörtnagel, A. Pajic, B. Christoph, B. Baier, M. Falk, J. Mautner, C. Geltinger, G. W. Bornkamm, and B. Kempkes. 1996. c-myc activation renders proliferation of Epstein-Barr virus (EBV)-transformed cells independent of EBV nuclear antigen 2 and latent membrane protein 1. Proc. Natl. Acad. Sci. USA 93: 10411-10416.
46. + T cell recognition of human B-cell lymphoma by resveratrol. Leuk. Lymphoma 53: 305-314.
47. Haque, M. A., P. Li, S. K. Jackson, H. M. Zarour, J. W. Hawes, U. T. Phan, M. Maric, P. Cresswell, and J. S. Blum. 2002. Absence of γ-interferon-inducible lysosomal thiol reductase in melanomas disrupts T cell recognition of select immunodominant epitopes. J. Exp. Med. 195: 1267-1277.
48. Ma, C., P. E. Whiteley, P. M. Cameron, D. C. Freed, A. Pressey, S. L. Chen, B. Garni-Wagner, C. Fang, D. M. Zaller, L. S. Wicker, and J. S. Blum. 1999. Role of APC in the selection of immunodominant T cell epitopes. J. Immunol. 163: 6413-6423.
49. Pathak, S. S., and J. S. Blum. 2000. Endocytic recycling is required for the presentation of an exogenous peptide via MHC class II molecules. Traffic 1: 561-569.
50. + T-cell recognition. Clin. Dev. Immunol. 2011: 780839.
51. Li, P., M. A. Haque, and J. S. Blum. 2002. Role of disulfide bonds in regulating antigen processing and epitope selection. J. Immunol. 169: 2444-2450.
52. + T cell recognition of human melanoma cells following treatment with bryostatin-1. Cell. Immunol. 271: 392-400.
53. Hossain, A., F. F. Radwan, B. P. Doonan, J. M. God, L. Zhang, P. D. Bell, and A. Haque. 2012. A possible cross-talk between autophagy and apoptosis in generating an immune response in melanoma. Apoptosis 17: 1066-1078.
54. Younger, A. R., S. Amria, W. A. Jeffrey, A. E. Mahdy, O. G. Goldstein, J. S. Norris, and A. Haque. 2008. HLA class II antigen presentation by prostate cancer cells. Prostate Cancer Prostatic Dis. 11: 334-341.
55. Haque, A., A. Das, L. M. Hajiaghamohseni, A. Younger, N. L. Banik, and S. K. Ray. 2007. Induction of apoptosis and immune response by all-trans ret-inoic acid plus interferon-gamma in human malignant glioblastoma T98G and U87MG cells. Cancer Immunol. Immunother. 56: 615-625.
56. Goldstein, O. G., L. M. Hajiaghamohseni, S. Amria, K. Sundaram, S. V. Reddy, and A. Haque. 2008. γ-IFN-inducible-lysosomal thiol reductase modulates acidic proteases and HLA class II antigen processing in melanoma. Cancer Immunol. Immunother. 57: 1461-1470.
57. Amria, S., L. M. Hajiaghamohseni, C. Harbeson, D. Zhao, O. Goldstein, J. S. Blum, and A. Haque. 2008. HLA-DM negatively regulates HLA-DR4-restricted collagen pathogenic peptide presentation and T cell recognition. Eur. J. Immunol. 38: 1961-1970.
58. Rothbard, J. B., R. Busch, K. Howland, V. Bal, C. Fenton, W. R. Taylor, and J. R. Lamb. 1989. Structural analysis of a peptide - HLA class II complex: identification of critical interactions for its formation and recognition by T cell receptor. Int. Immunol. 1: 479-486.
59. Zhang, S., H. Zhang, and J. Zhao. 2009. The role of CD4 T cell help for CD8 CTL activation. Biochem. Biophys. Res. Commun. 384: 405-408.
60. + T cells: when, where, and how. Annu. Rev. Immunol. 24: 519-540.
61. Khanolkar, A., V. P. Badovinac, and J. T. Harty. 2007. CD8 T cell memory development: CD4 T cell help is appreciated. Immunol. Res. 39: 94-104.
62. Pajic, A., M. S. Staege, D. Dudziak, M. Schuhmacher, D. Spitkovsky, G. Eissner, M. Brielmeier, A. Polack, and G. W. Bornkamm. 2001. Antagonistic effects of c-myc and Epstein-Barr virus latent genes on the phenotype of human B cells. Int. J. Cancer 93: 810-816.
63. Pajic, A., A. Polack, M. S. Staege, D. Spitkovsky, B. Baier, G. W. Bornkamm, and G. Laux. 2001. Elevated expression of c-myc in lymphoblastoid cells does not support an Epstein-Barr virus latency III-to-I switch. J. Gen. Virol. 82: 3051-3055.
64. Schlee, M., M. Holzel, S. Bernard, R. Mailhammer, M. Schuhmacher, J. Reschke, D. Eick, D. Marinkovic, T. Wirth, A. Rosenwald, et al. 2007. C-myc activation impairs the NF-κB and the interferon response: implications for the pathogenesis of Burkitt's lymphoma. Int. J. Cancer 120: 1387-1395.
65. Huang, M. J., Y. C. Cheng, C. R. Liu, S. Lin, and H. E. Liu. 2006. A small-molecule c-Myc inhibitor, 10058-F4, induces cell-cycle arrest, apoptosis, and myeloid differentiation of human acute myeloid leukemia. Exp. Hematol. 34: 1480-1489.
66. Rocha, N., and J. Neefjes. 2008. MHC class II molecules on the move for successful antigen presentation. EMBO J. 27: 1-5.
67. Haque, A., and J. S. Blum. 2005. New insights in antigen processing and epitope selection: development of novel immunotherapeutic strategies for cancer, auto-immunity and infectious diseases. J. Biol. Regul. Homeost. Agents 19: 93-104.
68. Blum, J. S., P. A. Wearsch, and P. Cresswell. 2013. Pathways of antigen processing. Annu. Rev. Immunol. 31: 443-473.
69. Gras, S., S. R. Burrows, S. J. Turner, A. K. Sewell, J. McCluskey, and J. Rossjohn. 2012. A structural voyage toward an understanding of the MHC-I-restricted immune response: lessons learned and much to be learned. Immunol. Rev. 250: 61-81.
70. West, L. C., and P. Cresswell. 2013. Expanding roles for GILT in immunity. Curr. Opin. Immunol. 25: 103-108.
71. Norton, D. L., and A. Haque. 2009. Insights into the role of GILT in HLA class II antigen processing and presentation by melanoma. J. Oncol. 2009: 142959.
72. Stern, L. J., I. Potolicchio, and L. Santambrogio. 2006. MHC class II compartment subtypes: structure and function. Curr. Opin. Immunol. 18: 64-69.
73. Landsverk, O. J., O. Bakke, and T. F. Gregers. 2009. MHC II and the endocytic pathway: regulation by invariant chain. Scand. J. Immunol. 70: 184-193.
74. Chen, X., and P. E. Jensen. 2008. MHC class II antigen presentation and im-munological abnormalities due to deficiency of MHC class II and its associated genes. Exp. Mol. Pathol. 85: 40-44.
75. Painter, C. A., and L. J. Stern. 2012. Conformational variation in structures of classical and non-classical MHCII proteins and functional implications. Immunol. Rev. 250: 144-157.
76. Denzin, L. K., J. L. Fallas, M. Prendes, and W. Yi. 2005. Right place, right time, right peptide: DO keeps DM focused. Immunol. Rev. 207: 279-292.
77. Martín, R., M. Olivares, M. Pérez, J. Xaus, C. Torre, L. Fernández, and J. M. Rodríguez. 2010. Identification and evaluation of the probiotic potential of lactobacilli isolated from canine milk. Vet. J. 185: 193-198.
78. Busch, R., C. H. Rinderknecht, S. Roh, A. W. Lee, J. J. Harding, T. Burster, T. M. Hornell, and E. D. Mellins. 2005. Achieving stability through editing and chaperoning: regulation of MHC class II peptide binding and expression. Immunol. Rev. 207: 242-260.
79. Morris, P., J. Shaman, M. Attaya, M. Amaya, S. Goodman, C. Bergman, J. J. Monaco, and E. Mellins. 1994. An essential role for HLA-DM in antigen presentation by class II major histocompatibility molecules. Nature 368: 551-554.
80. Guce, A. I., S. E. Mortimer, T. Yoon, C. A. Painter, W. Jiang, E. D. Mellins, and L. J. Stern. 2013. HLA-DO acts as a substrate mimic to inhibit HLA-DM by a competitive mechanism. Nat. Struct. Mol. Biol. 20: 90-98.
81. Chen, X., and P. E. Jensen. 2004. The expression of HLA-DO (H2-O) in B lymphocytes. Immunol. Res. 29: 19-28.
82. Xiu, F., M. H. Côté, M. C. Bourgeois-Daigneault, A. Brunet, M. E. Gauvreau, A. Shaw, and J. Thibodeau. 2011. Cutting edge: HLA-DO impairs the incorporation of HLA-DM into exosomes. J. Immunol. 187: 1547-1551.
83. Glazier, K. S., S. B. Hake, H. M. Tobin, A. Chadburn, E. J. Schattner, and L. K. Denzin. 2002. Germinal center B cells regulate their capability to present antigen by modulation of HLA-DO. J. Exp. Med. 195: 1063-1069.
84. Pathak, S. S., J. D. Lich, and J. S. Blum. 2001. Cutting edge: editing of recycling class II: peptide complexes by HLA-DM. J. Immunol. 167: 632-635.
85. Haque, M. A., J. W. Hawes, and J. S. Blum. 2001. Cysteinylation of MHC class II ligands: peptide endocytosis and reduction within APC influences T cell recognition. J. Immunol. 166: 4543-4551.
86. Yin, L., P. Trenh, A. Guce, M. Wieczorek, S. Lange, J. Sticht, W. Jiang, M. Bylsma, E. D. Mellins, C. Freund, and L. J. Stern. 2014. Susceptibility to HLA-DM protein is determined by a dynamic conformation of major histo-compatibility complex class II molecule bound with peptide. J. Biol. Chem. 289: 23449-23464.
87. Phipps-Yonas, H., V. Semik, and K. T. Hastings. 2013. GILT expression in B cells diminishes cathepsin S steady-state protein expression and activity. Eur. J. Immunol. 43: 65-74.
88. Maric, M., B. Arunachalam, U. T. Phan, C. Dong, W. S. Garrett, K. S. Cannon, C. Alfonso, L. Karlsson, R. A. Flavell, and P. Cresswell. 2001. Defective antigen processing in GILT-free mice. Science 294: 1361-1365.
89. O'Donnell, P. W., A. Haque, M. J. Klemsz, M. H. Kaplan, and J. S. Blum. 2004. Cutting edge: induction of the antigen-processing enzyme IFN-γ-inducible ly-sosomal thiol reductase in melanoma cells Is STAT1-dependent but CIITA-in-dependent. J. Immunol. 173: 731-735.
90. Denzin, L. K., and P. Cresswell. 2013. Sibling rivalry: competition between MHC class II family members inhibits immunity. Nat. Struct. Mol. Biol. 20: 7-10.
91. Subramanian, A., and D. M. Miller. 2000. Structural analysis of alpha-enolase. Mapping the functional domains involved in down-regulation of the c-myc protooncogene. J. Biol. Chem. 275: 5958-5965.
92. Sedoris, K. C., S. D. Thomas, and D. M. Miller. 2007. c-myc promoter binding protein regulates the cellular response to an altered glucose concentration. Biochemistry 46: 8659-8668.