Potential role for epigenetic modulatory drugs in the enhancement of cancer/germ-line antigen vaccine efficacy

Epigenetics

Volumn 1, Issue 3, 2006, Pages 116-120

  Karpf, Adam R ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

5 aza 2 deoxycytidine; Cancer testis antigens; Cancer germ line antigens; DNA methylation; DNMTs; Epigenetics; HDAC inhibitors; Immune response; MAGE A1; NY ESO 1

Indexed keywords

EID: 34250634403     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.1.3.2988     Document Type: Review

References (46)

1. Simpson AJ, Caballero OL, Jungbluth A, Chen YT, Old LJ. Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer 2005; 5:615-25.
2. Chomez P, De Backer O, Bertrand M, De Plaen E, Boon T, Lucas S. An overview of the MAGE gene family with the identification of all human members of the family. Cancer Res 2001; 61:5544-51.
3. van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, Van den Eynde B, Knuth A, Boon T. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 1991; 254:1643-7.
4. Scanlan MJ, Simpson AJ, Old LJ. The cancer/testis genes: Review, standardization, and commentary. Cancer Immun 2004; 4:1.
5. Christman JK. 5-Azacytidine and 5-aza-2′-deoxycytidine as inhibitors of DNA methylation: Mechanistic studies and their implications for cancer therapy. Oncogene 2002; 21:5483-95.
6. Weber J, Salgaller M, Samid D, Johnson B, Herlyn M, Lassam N, Treisman J, Rosenberg SA. Expression of the MAGE-1 tumor antigen is upregulated by the demethylating agent 5-aza-2′-deoxycytidine. Cancer Res 1994; 54:1766-71.
7. Serrano A, Garcia A, Abril E, Garrido F, Ruiz-Cabello F. Methylated CpG points identified within MAGE-1 promoter are involved in gene repression. Int J Cancer 1996; 68:464-70.
8. De Smet C, De Backer O, Faraoni I, Lurquin C, Brasseur F, Boon T. The activation of human gene MAGE-1 in tumor cells is correlated with genome-wide demethylation. Proc Natl Acad Sci USA 1996; 93:7149-53.
9. Sigalotti L, Coral S, Nardi G, Spessotto A, Cortini E, Cattarossi I, Colizzi F, Altomonte M, Maio M. Promoter methylation controls the expression of MAGE2, 3 and 4 genes in human cutaneous melanoma. J Immunother 2002; 25:16-26.
10. De Smet C, Lurquin C, Lethe B, Martelange V, Boon T. DNA methylation is the primary silencing mechanism for a set of germ line-and tumor-specific genes with a CpG-rich promoter. Mol Cell Biol 1999; 19:7327-35.
11. Lim JH, Kim SP, Gabrielson E, Park YB, Park JW, Kwon TK. Activation of human cancer/ testis antigen gene, XAGE-1, in tumor cells is correlated with CpG island hypomethylation. Int J Cancer 2005; 116:200-6.
12. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002; 3:415-28.
13. Bird A. The essentials of DNA methylation. Cell 1992; 70:5-8.
14. Ehrlich M. DNA methylation in cancer: Too much, but also too little. Oncogene 2002; 21:5400-13.
15. Feinberg AP, Tycko B. The history of cancer epigenetics. Nat Rev Cancer 2004; 4:143-53.
16. Robertson KD. DNA methylation, methyltransferases, and cancer. Oncogene 2001; 20:3139-55.
17. Koslowski M, Bell C, Seitz G, Lehr HA, Roemer K, Muntefering H, Huber C, Sahin U, Tureci O. Frequent nonrandom activation of germ-line genes in human cancer. Cancer Res 2004; 64:5988-93.
18. Loriot A, De Plaen E, Boon T, De Smet C. Transient down-regulation of DNMT1 methyltransferase leads to activation and stable hypomethylation of MAGE-A1 in melanoma cells. J Biol Chem 2006; In press.
19. James SR, Link PA, Karpf AR. Epigenetic regulation of X-linked cancer/germline antigen genes by DNMT1 and DNMT3b. Oncogene 2006, (doi:10.1038/sj.onc.1209678).
20. Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, Fukuda M, Takeda N, Niida H, Kato H, Shinkai Y. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev 2002; 16:1779-91.
21. Tachibana M, Ueda J, Fukuda M, Takeda N, Ohta T, Iwanari H, Sakihama T, Kodama T, Hamakubo T, Shinkai Y. Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes Dev 2005; 19:815-26.
22. Vatolin S, Abdullaev Z, Pack SD, Flanagan PT, Custer M, Loukinov DI, Pugacheva E, Hong JA, Morse IIIrd H, Schrump DS, Risinger JI, Barrett JC, Lobanenkov VV. Conditional expression of the CTCF-paralogous transcriptional factor BORIS in normal cells results in demethylation and derepression of MAGE-A1 and reactivation of other cancer-testis genes. Cancer Res 2005; 65:7751-62.
23. Hong JA, Kang Y, Abdullaev Z, Flanagan PT, Pack SD, Fischette MR, Adnani MT, Loukinov DI, Vatolin S, Risinger JI, Custer M, Chen GA, Zhao M, Nguyen DM, Barrett JC, Lobanenkov VV, Schrump DS. Reciprocal binding of CTCF and BORIS to the NY-ESO-1 promoter coincides with derepression of this cancer-testis gene in lung cancer cells. Cancer Res 2005; 65:7763-74.
24. Loukinov DI, Pugacheva E, Vatolin S, Pack SD, Moon H, Chernukhin I, Mannan P, Larsson E, Kanduri C, Vostrov AA, Cui H, Niemitz EL, Rasko JE, Docquier FM, Kistler M, Breen JJ, Zhuang Z, Quitschke WW, Renkawitz R, Klenova EM, Feinberg AP, Ohlsson R, Morse IIIrd HC, Lobanenkov VV. BORIS, a novel male germ-line-specific protein associated with epigenetic reprogramming events, shares the same 11-zinc-finger domain with CTCF, the insulator protein involved in reading imprinting marks in the soma. Proc Natl Acad Sci USA 2002; 99:6806-11.
25. Klenova EM, Morse IIIrd HC, Ohlsson R, Lobanenkov VV. The novel BORIS + CTCF gene family is uniquely involved in the epigenetics of normal biology and cancer. Semin Cancer Biol 2002; 12:399-414.
26. Ohlsson R, Renkawitz R, Lobanenkov V. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet 2001; 17:520-7.
27. Karpf AR, Lasek AW, Ririe TO, Hanks AN, Grossman D, Jones DA. Limited gene activation in tumor and normal epithelial cell lines treated with the DNA methyltransferase inhibitor 5-aza-2′-deoxycytidine. Mol Pharmacol 2004; 65:18-27.
28. Cheng JC, Yoo CB, Weisenberger DJ, Chuang J, Wozniak C, Liang G, Marquez VE, Greer S, Orntoft TF, Thykjaer T, Jones PA. Preferential response of cancer cells to zebularine. Cancer Cell 2004; 6:151-8.
29. Weiser TS, Guo ZS, Ohnmacht GA, Parkhurst ML, Tong-On P, Marincola FM, Fischette MR, Yu X, Chen GA, Hong JA, Stewart JH, Nguyen DM, Rosenberg SA, Schrump DS. Sequential 5-Aza-2 deoxycytidine-depsipeptide FR901228 treatment induces apoptosis preferentially in cancer cells and facilitates their recognition by cytolytic T lymphocytes specific for NY-ESO-1. J Immunother 2001; 24:151-61.
30. Wischnewski F, Pantel K, Schwarzenbach H. Promoter demethylation and histone acetylation mediate gene expression of MAGE-A1,-A2,-A3, and-A12 in human cancer cells. Mol Cancer Res 2006; 4:339-49.
31. Gillespie AM, Coleman RE. The potential of melanoma antigen expression in cancer therapy. Cancer Treatment Reviews 1999; 25:219-27.
32. Karpf AR, Peterson PW, Rawlins JT, Dalley BK, Yang Q, Albertsen H, Jones DA. 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 1999; 96:14007-12.
33. Fonsatti E, Sigalotti L, Coral S, Colizzi F, Altomonte M, Maio M. Methylation-regulated expression of HLA class I antigens in melanoma. Int J Cancer 2003; 105:430-1, (author reply 432-3).
34. Coral S, Sigalotti L, Gasparollo A, Cattarossi I, Visintin A, Cattelan A, Altomonte M, Maio M. Prolonged upregulation of the expression of HLA class I antigens and costimulatory molecules on melanoma cells treated with 5-aza-2′-deoxycytidine (5-AZA-CdR). J Immunother 1999; 22:16-24.
35. Algarra I, Garcia-Lora A, Cabrera T, Ruiz-Cabello F, Garrido F. The selection of tumor variants with altered expression of classical and nonclassical MHC class I molecules: Implications for tumor immune escape. Cancer Immunol Immunother 2004; 53:904-10.
36. van den Elsen PJ, Holling TM, van der Stoep N, Boss JM. DNA methylation and expression of major histocompatibility complex class I and class II transactivator genes in human developmental tumor cells and in T cell malignancies. Clin Immunol 2003; 109:46-52.
37. Guo ZS, Hong JA, Irvine KR, Chen GA, Spiess PJ, Liu Y, Zeng G, Wunderlich JR, Nguyen DM, Restifo NP, Schrump DS. De novo induction of a cancer/testis antigen by 5-aza-2′-deoxycytidine augments adoptive immunotherapy in a murine tumor model. Cancer Res 2006; 66:1105-13.
38. Samlowski WE, Leachman SA, Wade M, Cassidy P, Porter-Gill P, Busby L, Wheeler R, Boucher K, Fitzpatrick F, Jones DA, Karpf AR. Evaluation of a 7-day continuous intravenous infusion of decitabine: Inhibition of promoter-specific and global genomic DNA methylation. J Clin Oncol 2005; 23:3897-905.
39. Sigalotti L, Altomonte M, Colizzi F, Degan M, Rupolo M, Zagonel V, Pinto A, Gattei V, Maio M. 5-Aza-2′-deoxycytidine (decitabine) treatment of hematopoietic malignancies: A multimechanism therapeutic approach? Blood 2003; 101:4644-4646, (discussion 4645-6).
40. Davis ID, Chen W, Jackson H, Parente P, Shackleton M, Hopkins W, Chen Q, Dimopoulos N, Luke T, Murphy R, Scott AM, Maraskovsky E, McArthur G, MacGregor D, Sturrock S, Tai TY, Green S, Cuthbertson A, Maher D, Miloradovic L, Mitchell SV, Ritter G, Jungbluth AA, Chen YT, Gnjatic S, Hoffman EW, Old LJ, Cebon JS. Recombinant NY-ESO-1 protein with ISCOMATRIX adjuvant induces broad integrated antibody and CD4(+) and CD8(+) T cell responses in humans. Proc Natl Acad Sci USA 2004; 101:10697-702.
41. Kaminskas E, Farrell A, Abraham S, Baird A, Hsieh LS, Lee SL, Leighton JK, Patel H, Rahman A, Sridhara R, Wang YC, Pazdur R. Approval summary: Azacitidine for treatment of myelodysplastic syndrome subtypes. Clin Cancer Res 2005; 11:3604-8.
42. Issa JP. Optimizing therapy with methylation inhibitors in myelodysplastic syndromes: Dose, duration, and patient selection. Nat Clin Pract Oncol 2005; 2(Suppl 1):S24-9.
43. Coral S, Sigalotti L, Altomonte M, Engelsberg A, Colizzi F, Cattarossi I, Maraskovsky E, Jager E, Seliger B, Maio M. 5-aza-2′-deoxycytidine-induced expression of functional cancer testis antigens in human renal cell carcinoma: Immunotherapeutic implications. Clin Cancer Res 2002; 8:2690-5.
44. Liang G, Gonzales FA, Jones PA, Orntoft TF, Thykjaer T. Analysis of gene induction in human fibroblasts and bladder cancer cells exposed to the methylation inhibitor b5-aza-2′-deoxycytidineb. Cancer Res 2002; 62:961-6.
45. Sigalotti L, Coral S, Altomonte M, Natali L, Gaudino G, Cacciotti P, Libener R, Colizzi F, Vianale G, Martini F, Tognon M, Jungbluth A, Cebon J, Maraskovsky E, Mutti L, Maio M. Cancer testis antigens expression in mesothelioma: Role of DNA methylation and bioimmunotherapeutic implications. Br J Cancer 2002; 86:979-82.
46. Sigalotti L, Fratta E, Coral S, Tanzarella S, Danielli R, Colizzi F, Fonsatti E, Traversari C, Altomonte M, Maio M. Intratumor heterogeneity of cancer/testis antigens expression in human cutaneous melanoma is methylation-regulated and functionally reverted by 5-aza-2′-deoxycytidine. Cancer Res 2004; 64:9167-71.