H3K9 trimethylation silences fas expression to confer colon carcinoma immune escape and 5-fluorouracil chemoresistance

Journal of Immunology

Volumn 195, Issue 4, 2015, Pages 1868-1882

  Paschall, Amy V ^a,b   Yang, Dafeng ^a   Lu, Chunwan ^a   Choi, Jeong Hyeon ^a   Li, Xia ^c   Liu, Feiyan ^c   Figueroa, Mario ^d   Oberlies, Nicholas H ^d   Pearce, Cedric ^e   Bollag, Wendy B ^a   Nayak Kapoor, Asha ^a   Liu, Kebin ^a,b  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c ZHEJIANG UNIVERSITY   (China)

^d UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

^e Mycosynthetix Inc ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEATH RECEPTOR 5; DECITABINE; DROZITUMAB; FAS ANTIGEN; FAS LIGAND; FLUOROURACIL; HISTONE H3; LYSINE; METHYLTRANSFERASE INHIBITOR; UNCLASSIFIED DRUG; VERTICILLIN A; VORINOSTAT; EHMT2 PROTEIN, HUMAN; HISTOCOMPATIBILITY ANTIGEN; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; HISTONE METHYLTRANSFERASE; INDOLE DERIVATIVE; METHYLTRANSFERASE; REPRESSOR PROTEIN; SUV39H1 PROTEIN, HUMAN; SUV39H2 PROTEIN, HUMAN; VERTICILLINS;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER RESISTANCE; CHROMATIN IMMUNOPRECIPITATION; COLON CARCINOMA; COLORECTAL CARCINOMA; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DRUG MECHANISM; DRUG SAFETY; FAS GENE; GENE EXPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; IMMUNOSURVEILLANCE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN METHYLATION; TUMOR ESCAPE; ANIMAL; ANTAGONISTS AND INHIBITORS; COLONIC NEOPLASMS; DISEASE MODEL; DNA METHYLATION; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETICS; IC50; IMMUNOLOGY; LIVER; METABOLISM; METHYLATION; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; CELL LINE, TUMOR; COLONIC NEOPLASMS; DISEASE MODELS, ANIMAL; DNA METHYLATION; DRUG RESISTANCE, NEOPLASM; FAS LIGAND PROTEIN; FLUOROURACIL; GENE EXPRESSION PROFILING; GENE SILENCING; GENOME-WIDE ASSOCIATION STUDY; HISTOCOMPATIBILITY ANTIGENS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; INDOLES; INHIBITORY CONCENTRATION 50; LIVER; METHYLATION; METHYLTRANSFERASES; MICE; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; TUMOR ESCAPE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84938930600     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402243     Document Type: Article

References (66)

1. Cai, Z., F. Yang, L. Yu, Z. Yu, L. Jiang, Q. Wang, Y. Yang, L. Wang, X. Cao, and J. Wang. 2012. Activated T cell exosomes promote tumor invasion via Fas signaling pathway. J. Immunol. 188: 5954-5961.
2. Koncz, G., A. Hancz, K. Chakrabandhu, P. Gogolák, K. Kerekes, E. Rajnavölgyi, and A. O. Hueber. 2012. Vesicles released by activated T cells induce both Fasmediated RIP-dependent apoptotic and Fas-independent nonapoptotic cell deaths. J. Immunol. 189: 2815-2823.
3. Li, J., S. K. Figueira, A. C. Vrazo, B. F. Binkowski, B. L. Butler, Y. Tabata, A. Filipovich, M. B. Jordan, and K. A. Risma. 2014. Real-time detection of CTL function reveals distinct patterns of caspase activation mediated by Fas versus granzyme B. J. Immunol. 193: 519-528.
4. Ghare, S. S., S. Joshi-Barve, A. Moghe, M. Patil, D. F. Barker, L. Gobejishvili, G. N. Brock, M. Cave, C. J. McClain, and S. S. Barve. 2014. Coordinated histone H3 methylation and acetylation regulate physiologic and pathologic fas ligand gene expression in human CD4+ T cells. J. Immunol. 193: 412-421.
5. Weiss, J. M., J. J. Subleski, T. Back, X. Chen, S. K. Watkins, H. Yagita, T. J. Sayers, W. J. Murphy, and R. H. Wiltrout. 2014. Regulatory T cells and myeloid-derived suppressor cells in the tumor microenvironment undergo Fasdependent cell death during IL-2/aCD40 therapy. J. Immunol. 192: 5821-5829.
6. Oh, J., S. H. Kim, S. Ahn, and C. E. Lee. 2012. Suppressors of cytokine signaling promote Fas-induced apoptosis through downregulation of NF-kB and mitochondrial Bfl-1 in leukemic T cells. J. Immunol. 189: 5561-5571.
7. Wynes, M. W., B. L. Edelman, A. G. Kostyk, M. G. Edwards, C. Coldren, S. D. Groshong, G. P. Cosgrove, E. F. Redente, A. Bamberg, K. K. Brown, et al. 2011. Increased cell surface Fas expression is necessary and sufficient to sensitize lung fibroblasts to Fas ligation-induced apoptosis: implications for fibroblast accumulation in idiopathic pulmonary fibrosis. J. Immunol. 187: 527-537.
8. He, J. S., D. E. Gong, and H. L. Ostergaard. 2010. Stored Fas ligand, a mediator of rapid CTL-mediated killing, has a lower threshold for response than degranulation or newly synthesized Fas ligand. J. Immunol. 184: 555-563.
9. Straus, S. E., E. S. Jaffe, J. M. Puck, J. K. Dale, K. B. Elkon, A. Rösen-Wolff, A. M. Peters, M. C. Sneller, C. W. Hallahan, J. Wang, et al. 2001. The development of lymphomas in families with autoimmune lymphoproliferative syndrome with germline Fas mutations and defective lymphocyte apoptosis. Blood 98: 194-200.
10. Nikolov, N. P., M. Shimizu, S. Cleland, D. Bailey, J. Aoki, T. Strom, P. L. Schwartzberg, F. Candotti, and R. M. Siegel. 2010. Systemic autoimmunity and defective Fas ligand secretion in the absence of the Wiskott-Aldrich syndrome protein. Blood 116: 740-747.
11. Park, W. S., R. R. Oh, Y. S. Kim, J. Y. Park, S. H. Lee, M. S. Shin, S. Y. Kim, P. J. Kim, H. K. Lee, N. Y. Yoo, and J. Y. Lee. 2001. Somatic mutations in the death domain of the Fas (Apo-1/CD95) gene in gastric cancer. J. Pathol. 193: 162-168.
12. Lei, D., E. M. Sturgis, L. E. Wang, Z. Liu, M. E. Zafereo, Q. Wei, and G. Li. 2010. FAS and FASLG genetic variants and risk for second primary malignancy in patients with squamous cell carcinoma of the head and neck. Cancer Epidemiol. Biomarkers Prev. 19: 1484-1491.
13. Sunter, N. J., K. Scott, R. Hills, D. Grimwade, S. Taylor, L. J. Worrillow, S. E. Fordham, V. J. Forster, G. Jackson, S. Bomken, et al. 2012. A functional variant in the core promoter of the CD95 cell death receptor gene predicts prognosis in acute promyelocytic leukemia. Blood 119: 196-205.
14. Sung, W. W., Y. C. Wang, Y. W. Cheng, M. C. Lee, K. T. Yeh, L. Wang, J. Wang, C. Y. Chen, and H. Lee. 2011. A polymorphic 2844T/C in FasL promoter predicts survival and relapse in non-small cell lung cancer. Clin. Cancer Res. 17: 5991-5999.
15. Möller, P., K. Koretz, F. Leithäuser, S. Brüderlein, C. Henne, A. Quentmeier, and P. H. Krammer. 1994. Expression of APO-1 (CD95), a member of the NGF/TNF receptor superfamily, in normal and neoplastic colon epithelium. Int. J. Cancer 57: 371-377.
16. Krammer, P. H. 1999. CD95(APO-1/Fas)-mediated apoptosis: live and let die. Adv. Immunol. 71: 163-210.
17. Sträter, J., U. Hinz, C. Hasel, U. Bhanot, G. Mechtersheimer, T. Lehnert, and P. Möller. 2005. Impaired CD95 expression predisposes for recurrence in curatively resected colon carcinoma: clinical evidence for immunoselection and CD95L mediated control of minimal residual disease. Gut 54: 661-665.
18. Afshar-Sterle, S., D. Zotos, N. J. Bernard, A. K. Scherger, L. Rödling, A. E. Alsop, J. Walker, F. Masson, G. T. Belz, L. M. Corcoran, et al. 2014. Fas ligand-mediated immune surveillance by T cells is essential for the control of spontaneous B cell lymphomas. Nat. Med. 20: 283-290.
19. Liu, F., K. Bardhan, D. Yang, M. Thangaraju, V. Ganapathy, J. L. Waller, G. B. Liles, J. R. Lee, and K. Liu. 2012. NF-kB directly regulates Fas transcription to modulate Fas-mediated apoptosis and tumor suppression. J. Biol. Chem. 287: 25530-25540.
20. Maecker, H. L., Z. Yun, H. T. Maecker, and A. J. Giaccia. 2002. Epigenetic changes in tumor Fas levels determine immune escape and response to therapy. Cancer Cell 2: 139-148.
21. Yang, D., C. M. Torres, K. Bardhan, M. Zimmerman, T. L. McGaha, and K. Liu. 2012. Decitabine and vorinostat cooperate to sensitize colon carcinoma cells to Fas ligand-induced apoptosis in vitro and tumor suppression in vivo. J. Immunol. 188: 4441-4449.
22. Borralho, P. M., I. B. Moreira da Silva, M. M. Aranha, C. Albuquerque, C. Nobre Leitão, C. J. Steer, and C. M. Rodrigues. 2007. Inhibition of Fas expression by RNAi modulates 5-fluorouracil-induced apoptosis in HCT116 cells expressing wild-type p53. Biochim. Biophys. Acta 1772: 40-47.
23. Tillman, D. M., I. Petak, and J. A. Houghton. 1999. A Fas-dependent component in 5-fluorouracil/leucovorin-induced cytotoxicity in colon carcinoma cells. Clin. Cancer Res. 5: 425-430.
24. Longley, D. B., D. P. Harkin, and P. G. Johnston. 2003. 5-Fluorouracil: mechanisms of action and clinical strategies. Nat. Rev. Cancer 3: 330-338.
25. Greer, E. L., and Y. Shi. 2012. Histone methylation: a dynamic mark in health, disease and inheritance. Nat. Rev. Genet. 13: 343-357.
26. Spannhoff, A., A. T. Hauser, R. Heinke, W. Sippl, and M. Jung. 2009. The emerging therapeutic potential of histone methyltransferase and demethylase inhibitors. ChemMedChem 4: 1568-1582.
27. Crea, F., S. Nobili, E. Paolicchi, G. Perrone, C. Napoli, I. Landini, R. Danesi, and E. Mini. 2011. Epigenetics and chemoresistance in colorectal cancer: an opportunity for treatment tailoring and novel therapeutic strategies. Drug Resist. Updat. 14: 280-296.
28. Nebbioso, A., V. Carafa, R. Benedetti, and L. Altucci. 2012. Trials with "epigenetic" drugs: an update. Mol. Oncol. 6: 657-682.
29. Juergens, R. A., J. Wrangle, F. P. Vendetti, S. C. Murphy, M. Zhao, B. Coleman, R. Sebree, K. Rodgers, C. M. Hooker, N. Franco, et al. 2011. Combination epigenetic therapy has efficacy in patients with refractory advanced non-small cell lung cancer. Cancer Discov 1: 598-607.
30. Subramaniam, D., R. Thombre, A. Dhar, and S. Anant. 2014. DNA methyltransferases: a novel target for prevention and therapy. Front.Oncol.4: 80
31. Vedadi, M., D. Barsyte-Lovejoy, F. Liu, S. Rival-Gervier, A. Allali-Hassani, V. Labrie, T. J. Wigle, P. A. Dimaggio, G. A. Wasney, A. Siarheyeva, et al. 2011. A chemical probe selectively inhibits G9a and GLP methyltransferase activity in cells. Nat. Chem. Biol. 7: 566-574.
32. Daigle, S. R., E. J. Olhava, C. A. Therkelsen, C. R. Majer, C. J. Sneeringer, J. Song, L. D. Johnston, M. P. Scott, J. J. Smith, Y. Xiao, et al. 2011. Selective killing of mixed lineage leukemia cells by a potent small-molecule DOT1L inhibitor. Cancer Cell 20: 53-65.
33. Ferguson, A. D., N. A. Larsen, T. Howard, H. Pollard, I. Green, C. Grande, T. Cheung, R. Garcia-Arenas, S. Cowen, J. Wu, et al. 2011. Structural basis of substrate methylation and inhibition of SMYD2. Structure 19: 1262-1273.
34. Figueroa, M., T. N. Graf, S. Ayers, A. F. Adcock, D. J. Kroll, J. Yang, S. M. Swanson, U. Munoz-Acuna, E. J. Carcache de Blanco, R. Agrawal, et al. 2012. Cytotoxic epipolythiodioxopiperazine alkaloids from filamentous fungi of the Bionectriaceae. J. Antibiot. 65: 559-564.
35. Liu, F., Q. Liu, D. Yang, W. B. Bollag, K. Robertson, P. Wu, and K. Liu. 2011. Verticillin A overcomes apoptosis resistance in human colon carcinoma through DNA methylation-dependent upregulation of BNIP3. Cancer Res. 71: 6807-6816.
36. Zhang, Y., T. Liu, C. A. Meyer, J. Eeckhoute, D. S. Johnson, B. E. Bernstein, C. Nusbaum, R. M. Myers, M. Brown, W. Li, and X. S. Liu. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9: R137.
37. Bacon, A. L., S. Fox, H. Turley, and A. L. Harris. 2007. Selective silencing of the hypoxia-inducible factor 1 target gene BNIP3 by histone deacetylation and methylation in colorectal cancer. Oncogene 26: 132-141.
38. O'Carroll, D., H. Scherthan, A. H. Peters, S. Opravil, A. R. Haynes, G. Laible, S. Rea, M. Schmid, A. Lebersorger, M. Jerratsch, et al. 2000. Isolation and characterization of Suv39h2, a second histone H3 methyltransferase gene that displays testis-specific expression. Mol. Cell. Biol. 20: 9423-9433.
39. Rice, J. C., S. D. Briggs, B. Ueberheide, C. M. Barber, J. Shabanowitz, D. F. Hunt, Y. Shinkai, and C. D. Allis. 2003. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol. Cell 12: 1591-1598.
40. Hewitt, R. E., A. McMarlin, D. Kleiner, R. Wersto, P. Martin, M. Tsokos, G. W. Stamp, and W. G. Stetler-Stevenson. 2000. Validation of a model of colon cancer progression. J. Pathol. 192: 446-454.
41. Jin, Q., L. R. Yu, L. Wang, Z. Zhang, L. H. Kasper, J. E. Lee, C. Wang, P. K. Brindle, S. Y. Dent, and K. Ge. 2011. Distinct roles of GCN5/PCAFmediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J. 30: 249-262.
42. O' Reilly, L. A., L. Tai, L. Lee, E. A. Kruse, S. Grabow, W. D. Fairlie, N. M. Haynes, D. M. Tarlinton, J. G. Zhang, G. T. Belz, et al. 2009. Membranebound Fas ligand only is essential for Fas-induced apoptosis. Nature 461: 659-663.
43. Hanahan, D., and R. A. Weinberg. 2000. The hallmarks of cancer. Cell 100: 57-70.
44. Ashkenazi, A. 2008. Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat. Rev. Drug Discov. 7: 1001-1012.
45. Almasan, A., and A. Ashkenazi. 2003. Apo2L/TRAIL: apoptosis signaling, biology, and potential for cancer therapy. Cytokine Growth Factor Rev. 14: 337-348.
46. Ashkenazi, A. 2002. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat. Rev. Cancer 2: 420-430.
47. Grosse-Wilde, A., O. Voloshanenko, S. L. Bailey, G. M. Longton, U. Schaefer, A. I. Csernok, G. Schütz, E. F. Greiner, C. J. Kemp, and H. Walczak. 2008. TRAIL-R deficiency in mice enhances lymph node metastasis without affecting primary tumor development. J. Clin. Invest. 118: 100-110.
48. Rocha Lima, C. M., S. Bayraktar, A. M. Flores, J. Macintyre, A. Montero, J. C. Baranda, J. Wallmark, C. Portera, R. Raja, H. Stern, et al. 2012. Phase Ib study of drozitumab combined with first-line mFOLFOX6 plus bevacizumab in patients with metastatic colorectal cancer. Cancer Invest. 30: 727-731.
49. Wilson, N. S., B. Yang, A. Yang, S. Loeser, S. Marsters, D. Lawrence, Y. Li, R. Pitti, K. Totpal, S. Yee, et al. 2011. An Fcg receptor-dependent mechanism drives antibody-mediated target-receptor signaling in cancer cells. Cancer Cell 19: 101-113.
50. Yokoyama, Y., M. Hieda, Y. Nishioka, A. Matsumoto, S. Higashi, H. Kimura, H. Yamamoto, M. Mori, S. Matsuura, and N. Matsuura. 2013. Cancer-associated upregulation of histone H3 lysine 9 trimethylation promotes cell motility in vitro and drives tumor formation in vivo. Cancer Sci. 104: 889-895.
51. Ceol, C. J., Y. Houvras, J. Jane-Valbuena, S. Bilodeau, D. A. Orlando, V. Battisti, L. Fritsch, W. M. Lin, T. J. Hollmann, F. Ferré, et al. 2011. The histone methyltransferase SETDB1 is recurrently amplified in melanoma and accelerates its onset. Nature 471: 513-517.
52. Marteau, J. B., O. Rigaud, T. Brugat, N. Gault, L. Vallat, M. Kruhoffer, T. F. Orntoft, F. Nguyen-Khac, S. Chevillard, H. Merle-Beral, and J. Delic. 2010. Concomitant heterochromatinisation and down-regulation of gene expression unveils epigenetic silencing of RELB in an aggressive subset of chronic lymphocytic leukemia in males. BMC Med. Genomics 3: 53.
53. Park, Y. S., M. Y. Jin, Y. J. Kim, J. H. Yook, B. S. Kim, and S. J. Jang. 2008. The global histone modification pattern correlates with cancer recurrence and overall survival in gastric adenocarcinoma. Ann. Surg. Oncol. 15: 1968-1976.
54. Jin, B., Y. Li, and K. D. Robertson. 2011. DNA methylation: superior or subordinate in the epigenetic hierarchy? Genes Cancer 2: 607-617.
55. Petak, I., R. P. Danam, D. M. Tillman, R. Vernes, S. R. Howell, L. Berczi, L. Kopper, T. P. Brent, and J. A. Houghton. 2003. Hypermethylation of the gene promoter and enhancer region can regulate Fas expression and sensitivity in colon carcinoma. Cell Death Differ. 10: 211-217.
56. Morachis, J. M., C. M. Murawsky, and B. M. Emerson. 2010. Regulation of the p53 transcriptional response by structurally diverse core promoters. Genes Dev. 24: 135-147.
57. Pagès, F., A. Berger, M. Camus, F. Sanchez-Cabo, A. Costes, R. Molidor, B. Mlecnik, A. Kirilovsky, M. Nilsson, D. Damotte, et al. 2005. Effector memory T cells, early metastasis, and survival in colorectal cancer. N. Engl. J. Med. 353: 2654-2666.
58. Galon, J., A. Costes, F. Sanchez-Cabo, A. Kirilovsky, B. Mlecnik, C. Lagorce-Pagès, M. Tosolini, M. Camus, A. Berger, P. Wind, et al. 2006. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313: 1960-1964.
59. Chen, M. L., M. J. Pittet, L. Gorelik, R. A. Flavell, R. Weissleder, H. von Boehmer, and K. Khazaie. 2005. Regulatory T cells suppress tumor-specific CD8 T cell cytotoxicity through TGF-b signals in vivo. Proc. Natl. Acad. Sci. USA 102: 419-424.
60. Mempel, T. R., M. J. Pittet, K. Khazaie, W. Weninger, R. Weissleder, H. von Boehmer, and U. H. von Andrian. 2006. Regulatory T cells reversibly suppress cytotoxic T cell function independent of effector differentiation. Immunity 25: 129-141.
61. Glover, A. B., B. R. Leyland-Jones, H. G. Chun, B. Davies, and D. F. Hoth. 1987. Azacitidine: 10 years later. Cancer Treat. Rep. 71: 737-746.
62. Hanahan, D., and R. A. Weinberg. 2011. Hallmarks of cancer: the next generation. Cell 144: 646-674.
63. Graves, J. D., J. J. Kordich, T. H. Huang, J. Piasecki, T. L. Bush, T. Sullivan, I. N. Foltz,W. Chang, H. Douangpanya, T. Dang, et al. 2014. Apo2L/TRAIL and the death receptor 5 agonist antibody AMG 655 cooperate to promote receptor clustering and antitumor activity. Cancer Cell 26: 177-189.
64. Holohan, C., S. Van Schaeybroeck, D. B. Longley, and P. G. Johnston. 2013. Cancer drug resistance: an evolving paradigm. Nat. Rev. Cancer 13: 714-726.
65. Fakih, M. G., A. Groman, J. McMahon, G. Wilding, and J. R. Muindi. 2012. A randomized phase II study of two doses of vorinostat in combination with 5-FU/LV in patients with refractory colorectal cancer. Cancer Chemother. Pharmacol. 69: 743-751.
66. Fisher, G. A., T. Kuo, M. Ramsey, E. Schwartz, R. V. Rouse, C. D. Cho, J. Halsey, and B. I. Sikic. 2008. A phase II study of gefitinib, 5-fluorouracil, leucovorin, and oxaliplatin in previously untreated patients with metastatic colorectal cancer. Clin. Cancer Res. 14: 7074-7079.