DNA-Demethylating Agents Target Colorectal Cancer Cells by Inducing Viral Mimicry by Endogenous Transcripts

Cell

Volumn 162, Issue 5, 2015, Pages 961-973

  Roulois, David ^a   Loo Yau, Helen ^a,b   Singhania, Rajat ^a   Wang, Yadong ^a   Danesh, Arnavaz ^a   Shen, Shu Yi ^a   Han, Han ^c   Liang, Gangning ^c   Jones, Peter A ^c   Pugh, Trevor J ^a,b   O'Brien, Catherine ^a,b,d   De Carvalho, Daniel D ^a,b  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d TORONTO GENERAL HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CYTOSOL RECEPTOR; DECITABINE; GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; MAVS PROTEIN; MDA5 PROTEIN; MITOCHONDRIAL PROTEIN; PATTERN RECOGNITION RECEPTOR; PROTEIN; RETROVIRUS VECTOR; RUXOLITINIB; TOFACITINIB; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIMETABOLITE; AZACITIDINE; DEAD BOX PROTEIN; DOUBLE STRANDED RNA; IFIH1 PROTEIN, HUMAN; IRF7 PROTEIN, HUMAN; RARRES3 PROTEIN, HUMAN; RETINOIC ACID RECEPTOR; SIGNAL TRANSDUCING ADAPTOR PROTEIN; VISA PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOINFORMATICS; CANCER THERAPY; COLONY FORMATION; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; DNA METHYLATION; DOUBLE-STRANDED RNA VIRUS; DRUG MECHANISM; DRUG TARGETING; ENDOGENOUS RETROVIRUS; GENE ACTIVATION; GENE EXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LONG TERM CARE; LOW DRUG DOSE; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR GROWTH; ANALOGS AND DERIVATIVES; ANIMAL; CELL CULTURE; COLORECTAL NEOPLASMS; DRUG EFFECTS; IMMUNOLOGY; METABOLISM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; AZACITIDINE; CELLS, CULTURED; COLORECTAL NEOPLASMS; DEAD-BOX RNA HELICASES; DNA METHYLATION; ENDOGENOUS RETROVIRUSES; HUMANS; INTERFERON REGULATORY FACTOR-7; MICE; RECEPTORS, RETINOIC ACID; RNA, DOUBLE-STRANDED; SIGNAL TRANSDUCTION;

EID: 84940403834     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.07.056     Document Type: Article

References (37)

1. N. Ahuja, H. Easwaran, and S.B. Baylin Harnessing the potential of epigenetic therapy to target solid tumors J. Clin. Invest. 124 2014 56 63
2. R. Barbalat, S.E. Ewald, M.L. Mouchess, and G.M. Barton Nucleic acid recognition by the innate immune system Annu. Rev. Immunol. 29 2011 185 214
3. R. Besch, H. Poeck, T. Hohenauer, D. Senft, G. Häcker, C. Berking, V. Hornung, S. Endres, T. Ruzicka, S. Rothenfusser, and G. Hartmann Proapoptotic signaling induced by RIG-I and MDA-5 results in type I interferon-independent apoptosis in human melanoma cells J. Clin. Invest. 119 2009 2399 2411
4. P. Dalerba, S.J. Dylla, I.K. Park, R. Liu, X. Wang, R.W. Cho, T. Hoey, A. Gurney, E.H. Huang, D.M. Simeone, and et al. Phenotypic characterization of human colorectal cancer stem cells Proc. Natl. Acad. Sci. USA 104 2007 10158 10163
5. D.D. De Carvalho, S. Sharma, J.S. You, S.F. Su, P.C. Taberlay, T.K. Kelly, X. Yang, G. Liang, and P.A. Jones DNA methylation screening identifies driver epigenetic events of cancer cell survival Cancer Cell 21 2012 655 667
6. P. Duewell, A. Steger, H. Lohr, H. Bourhis, H. Hoelz, S.V. Kirchleitner, M.R. Stieg, S. Grassmann, S. Kobold, J.T. Siveke, and et al. RIG-I-like helicases induce immunogenic cell death of pancreatic cancer cells and sensitize tumors toward killing by CD8 T cells Cell Death Differ. 21 2014 1825 1837
7. R. Halfmann, and S. Lindquist Screening for amyloid aggregation by semi-denaturing detergent-agarose gel electrophoresis J. Vis. Exp. 17 2008 838
8. T. Hinoue, D.J. Weisenberger, C.P. Lange, H. Shen, H.M. Byun, D. Van Den Berg, S. Malik, F. Pan, H. Noushmehr, C.M. van Dijk, and et al. Genome-scale analysis of aberrant DNA methylation in colorectal cancer Genome Res. 22 2012 271 282
9. F. Hou, L. Sun, H. Zheng, B. Skaug, Q.X. Jiang, and Z.J. Chen MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response Cell 146 2011 448 461
10. Y. Hu, and G.K. Smyth ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays J. Immunol. Methods 347 2009 70 78
11. J.P. Issa, and H.M. Kantarjian Targeting DNA methylation Clin. Cancer Res. 15 2009 3938 3946
12. L.J. Jiang, N.N. Zhang, F. Ding, X.Y. Li, L. Chen, H.X. Zhang, W. Zhang, S.J. Chen, Z.G. Wang, J.M. Li, and et al. RA-inducible gene-I induction augments STAT1 activation to inhibit leukemia cell proliferation Proc. Natl. Acad. Sci. USA 108 2011 1897 1902
13. R.A. Juergens, J. Wrangle, F.P. Vendetti, S.C. Murphy, M. Zhao, B. Coleman, R. Sebree, K. Rodgers, C.M. Hooker, N. Franco, and et al. Combination epigenetic therapy has efficacy in patients with refractory advanced non-small cell lung cancer Cancer Discov. 1 2011 598 607
14. A.R. Karpf, P.W. Peterson, J.T. Rawlins, B.K. Dalley, Q. Yang, H. Albertsen, and D.A. Jones Inhibition of DNA methyltransferase stimulates the expression of signal transducer and activator of transcription 1, 2, and 3 genes in colon tumor cells Proc. Natl. Acad. Sci. USA 96 1999 14007 14012
15. A.R. Karpf, A.W. Lasek, T.O. Ririe, A.N. Hanks, D. Grossman, and D.A. Jones Limited gene activation in tumor and normal epithelial cells treated with the DNA methyltransferase inhibitor 5-aza-2′-deoxycytidine Mol. Pharmacol. 65 2004 18 27
16. H. Kato, O. Takeuchi, E. Mikamo-Satoh, R. Hirai, T. Kawai, K. Matsushita, A. Hiiragi, T.S. Dermody, T. Fujita, and S. Akira Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5 J. Exp. Med. 205 2008 1601 1610
17. T.K. Kelly, D.D. De Carvalho, and P.A. Jones Epigenetic modifications as therapeutic targets Nat. Biotechnol. 28 2010 1069 1078
18. A. Krämer, J. Green, J. Pollard Jr., and S. Tugendreich Causal analysis approaches in Ingenuity Pathway Analysis Bioinformatics 30 2014 523 530
19. A. Kreso, and J.E. Dick Evolution of the cancer stem cell model Cell Stem Cell 14 2014 275 291
20. A. Kreso, P. van Galen, N.M. Pedley, E. Lima-Fernandes, C. Frelin, T. Davis, L. Cao, R. Baiazitov, W. Du, N. Sydorenko, and et al. Self-renewal as a therapeutic target in human colorectal cancer Nat. Med. 20 2014 29 36
21. K.I. Leonova, L. Brodsky, B. Lipchick, M. Pal, L. Novototskaya, A.A. Chenchik, G.C. Sen, E.A. Komarova, and A.V. Gudkov p53 cooperates with DNA methylation and a suicidal interferon response to maintain epigenetic silencing of repeats and noncoding RNAs Proc. Natl. Acad. Sci. USA 110 2013 E89 E98
22. H. Li, K.B. Chiappinelli, A.A. Guzzetta, H. Easwaran, R.W. Yen, R. Vatapalli, M.J. Topper, J. Luo, R.M. Connolly, N.S. Azad, and et al. Immune regulation by low doses of the DNA methyltransferase inhibitor 5-azacitidine in common human epithelial cancers Oncotarget 5 2014 587 598
23. S.C. Mack, H. Witt, R.M. Piro, L. Gu, S. Zuyderduyn, A.M. Stütz, X. Wang, M. Gallo, L. Garzia, K. Zayne, and et al. Epigenomic alterations define lethal CIMP-positive ependymomas of infancy Nature 506 2014 445 450
24. A. Merlos-Suárez, F.M. Barriga, P. Jung, M. Iglesias, M.V. Céspedes, D. Rossell, M. Sevillano, X. Hernando-Momblona, V. da Silva-Diz, P. Muñoz, and et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse Cell Stem Cell 8 2011 511 524
25. S.C. Navada, J. Steinmann, M. Lübbert, and L.R. Silverman Clinical development of demethylating agents in hematology J. Clin. Invest. 124 2014 40 46
26. C.A. O'Brien, A. Pollett, S. Gallinger, and J.E. Dick A human colon cancer cell capable of initiating tumour growth in immunodeficient mice Nature 445 2007 106 110
27. C.A. O'Brien, A. Kreso, P. Ryan, K.G. Hermans, L. Gibson, Y. Wang, A. Tsatsanis, S. Gallinger, and J.E. Dick ID1 and ID3 regulate the self-renewal capacity of human colon cancer-initiating cells through p21 Cancer Cell 21 2012 777 792
28. C. Odendall, E. Dixit, F. Stavru, H. Bierne, K.M. Franz, A.F. Durbin, S. Boulant, L. Gehrke, P. Cossart, and J.C. Kagan Diverse intracellular pathogens activate type III interferon expression from peroxisomes Nat. Immunol. 15 2014 717 726
29. L. Ricci-Vitiani, D.G. Lombardi, E. Pilozzi, M. Biffoni, M. Todaro, C. Peschle, and R. De Maria Identification and expansion of human colon-cancer-initiating cells Nature 445 2007 111 115
30. R.B. Seth, L. Sun, C.K. Ea, and Z.J. Chen Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3 Cell 122 2005 669 682
31. M.B. Treppendahl, L.S. Kristensen, and K. Grønbæk Predicting response to epigenetic therapy J. Clin. Invest. 124 2014 47 55
32. H.C. Tsai, H. Li, L. Van Neste, Y. Cai, C. Robert, F.V. Rassool, J.J. Shin, K.M. Harbom, R. Beaty, E. Pappou, and et al. Transient low doses of DNA-demethylating agents exert durable antitumor effects on hematological and epithelial tumor cells Cancer Cell 21 2012 430 446
33. F. Weber, V. Wagner, S.B. Rasmussen, R. Hartmann, and S.R. Paludan Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses J. Virol. 80 2006 5059 5064
34. M.S. Wicha Targeting self-renewal, an Achilles' heel of cancer stem cells Nat. Med. 20 2014 14 15
35. J. Wrangle, W. Wang, A. Koch, H. Easwaran, H.P. Mohammad, F. Vendetti, W. Vancriekinge, T. Demeyer, Z. Du, P. Parsana, and et al. Alterations of immune response of Non-Small Cell Lung Cancer with Azacytidine Oncotarget 4 2013 2067 2079
36. X. Yang, H. Han, D.D. De Carvalho, F.D. Lay, P.A. Jones, and G. Liang Gene body methylation can alter gene expression and is a therapeutic target in cancer Cancer Cell 26 2014 577 590
37. M. Zeng, Z. Hu, X. Shi, X. Li, X. Zhan, X.D. Li, J. Wang, J.H. Choi, K.W. Wang, T. Purrington, and et al. MAVS, cGAS, and endogenous retroviruses in T-independent B cell responses Science 346 2014 1486 1492