Immunomodulatory action of SGI-110, a hypomethylating agent, in acute myeloid leukemia cells and xenografts

Leukemia Research

Volumn 38, Issue 11, 2014, Pages 1332-1341

  Srivastava, Pragya ^a   Paluch, Benjamin E ^a   Matsuzaki, Junko ^a   James, Smitha R ^a   Collamat Lai, Golda ^a   Karbach, Julia ^b   Nemeth, Michael J ^a   Taverna, Pietro ^c   Karpf, Adam R ^d   Griffiths, Elizabeth A ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b KRANKENHAUS NORDWEST   (Germany)

^c ASTEX PHARMACEUTICALS   (United Kingdom)

^d UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Acute myeloid leukemia; Cancer germline genes; Cancer testis antigens; DNA methylation; DNA methyltransferase inhibitors; Epigenetics; Immune modulation; SGI 110

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ANTILEUKEMIC AGENT; AZACITIDINE; CANCER TESTIS ANTIGEN; IMMUNOMODULATING AGENT; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MELANOMA ANTIGEN; NY ESO 1 ANTIGEN; SGI 110; UNCLASSIFIED DRUG; IMMUNOLOGIC FACTOR; SGI-110;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER MODEL; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXICITY; DRUG EXPOSURE; FEMALE; GENE EXPRESSION; GENETIC REGULATION; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; LEUKEMIA CELL LINE; MOUSE; MOUSE MODEL; NONHUMAN; TUMOR XENOGRAFT; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; DNA METHYLATION; DRUG SCREENING; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; TUMOR CELL LINE;

ANIMALS; AZACITIDINE; CELL LINE, TUMOR; DNA METHYLATION; FEMALE; HUMANS; IMMUNOLOGIC FACTORS; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, SCID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84910087763     PISSN: 01452126     EISSN: 18735835     Source Type: Journal    
DOI: 10.1016/j.leukres.2014.09.001     Document Type: Article

References (54)

1. Estey E.H. Epigenetics in clinical practice: the examples of azacitidine and decitabine in myelodysplasia and acute myeloid leukemia. Leukemia 2013, 27(September (9)):1803-1812.
2. Jabbour E., Garcia-Manero G., Batty N., Shan J., O'Brien S., Cortes J., et al. Outcome of patients with myelodysplastic syndrome after failure of decitabine therapy. Cancer 2010, 116(August (16)):3830-3834.
3. Prebet T., Gore S.D., Esterni B., Gardin C., Itzykson R., Thepot S., et al. Outcome of high-risk myelodysplastic syndrome after azacitidine treatment failure. J Clin Oncol 2011, 29(August (24)):3322-3327.
4. Prebet T., Gore S.D., Thepot S., Esterni B., Quesnel B., Beyne Rauzy O., et al. Outcome of acute myeloid leukaemia following myelodysplastic syndrome after azacitidine treatment failure. Br J Haematol 2012, 157(June (6)):764-766.
5. Prebet T., Thepot S., Gore S.D., Dreyfus F., Fenaux P., Vey N. Outcome of patients with low-risk myelodysplasia after azacitidine treatment failure. Haematologica 2013, 98(February (2)):e18-e19.
6. Itzykson R., Fenaux P. Optimizing hypomethylating agents in myelodysplastic syndromes. Curr Opin Hematol 2012, 19(March (2)):65-70.
7. Fandy T.E., Herman J.G., Kerns P., Jiemjit A., Sugar E.A., Choi S.H., et al. Early epigenetic changes and DNA damage do not predict clinical response in an overlapping schedule of 5-azacytidine and entinostat in patients with myeloid malignancies. Blood 2009, 114(September (13)):2764-2773.
8. Fandy T.E., Jiemjit A., Thakar M., Rhoden P., Suarez L., Gore S.D. Decitabine induces delayed reactive oxygen species (ROS) accumulation in leukemia cells and induces the expression of ROS generating enzymes. Clin Cancer Res 2014, 20(March (5)):1249-1258.
9. Karpf A.R., Moore B.C., Ririe T.O., Jones D.A. Activation of the p53 DNA damage response pathway after inhibition of DNA methyltransferase by 5-aza-2'-deoxycytidine. Mol Pharmacol 2001, 59(April (4)):751-757.
10. Karpf A.R., Jones D.A. Reactivating the expression of methylation silenced genes in human cancer. Oncogene 2002, 21(August (35)):5496-5503.
11. Zeidan A.M., Linhares Y., Gore S.D. Current therapy of myelodysplastic syndromes. Blood Rev 2013, 27(September (5)):243-259.
12. Goodyear O., Agathanggelou A., Novitzky-Basso I., Siddique S., McSkeane T., Ryan G., et al. Induction of a CD8+ T-cell response to the MAGE cancer testis antigen by combined treatment with azacitidine and sodium valproate in patients with acute myeloid leukemia and myelodysplasia. Blood 2010, 116(September (11)):1908-1918.
13. Goodyear O.C., Dennis M., Jilani N.Y., Loke J., Siddique S., Ryan G., et al. Azacitidine augments expansion of regulatory T cells after allogeneic stem cell transplantation in patients with acute myeloid leukemia (AML). Blood 2012, 119(April (14)):3361-3369.
14. Karpf A.R., Lasek A.W., Ririe T.O., Hanks A.N., Grossman D., Jones D.A. Limited gene activation in tumor and normal epithelial cells treated with the DNA methyltransferase inhibitor 5-aza-2'-deoxycytidine. Mol Pharmacol 2004, 65(January (1)):18-27.
15. Braun T., Fenaux P. Myelodysplastic syndromes (MDS) and autoimmune disorders (AD): cause or consequence?. Best Pract Res Clin Haematol 2013, 26(December (4)):327-336.
16. Al Ustwani O., Ford L.A., Sait S.J., Block A.M., Barcos M., Vigil C.E., et al. Myelodysplastic syndromes and autoimmune diseases - case series and review of literature. Leuk Res 2013, 37(August (8)):894-899.
17. Olnes M.J., Sloand E.M. Targeting immune dysregulation in myelodysplastic syndromes. J Am Med Assoc 2011, 305(February (8)):814-819.
18. Almstedt M., Blagitko-Dorfs N., Duque-Afonso J., Karbach J., Pfeifer D., Jager E., et al. The DNA demethylating agent 5-aza-2'-deoxycytidine induces expression of NY-ESO-1 and other cancer/testis antigens in myeloid leukemia cells. Leuk Res 2010, 34(July (7)):899-905.
19. Griffiths E.A., James S.R., Ford L.A., Beck A.F., Wetzler M., Odunsi K., et al. Conventional dose hypomethylating agents induce CG antigen genes in vivo. Blood 2011, 118(21):2441.
20. Srivastava P., Collamat G., James S.R., Ford L.A., Wetzler M., Karpf A.R., et al. Decitabine treatment induces NY-ESO1 promoter hypomethylation, mRNA and protein expression in acute myeloid leukemia (AML) blasts harvested from peripheral blood. Leuk Res 2013, 37(Suppl. 1):S132.
21. Akers S.N., Odunsi K., Karpf A.R. Regulation of cancer germline antigen gene expression: implications for cancer immunotherapy. Future Oncol 2010, 6(May (5)):717-732.
22. Stockert E., Jager E., Chen Y.T., Scanlan M.J., Gout I., Karbach J., et al. A survey of the humoral immune response of cancer patients to a panel of human tumor antigens. J Exp Med 1998, 187(April (8)):1349-1354.
23. Grah J.J., Katalinic D., Juretic A., Santek F., Samarzija M. Clinical significance of immunohistochemical expression of cancer/testis tumor-associated antigens (MAGE-A1, MAGE-A3/4, NY-ESO-1) in patients with non-small cell lung cancer. Tumori 2014, 100(January-February (1)):60-68.
24. Odunsi K., Jungbluth A.A., Stockert E., Qian F., Gnjatic S., Tammela J., et al. NY-ESO-1 and LAGE-1 cancer-testis antigens are potential targets for immunotherapy in epithelial ovarian cancer. Cancer Res 2003, 63(September (18)):6076-6083.
25. Woloszynska-Read A., Mhawech-Fauceglia P., Yu J., Odunsi K., Karpf A.R. Intertumor and intratumor NY-ESO-1 expression heterogeneity is associated with promoter-specific and global DNA methylation status in ovarian cancer. Clin Cancer Res 2008, 14(June (11)):3283-3290.
26. Aranda F., Vacchelli E., Eggermont A., Galon J., Sautes-Fridman C., Tartour E., et al. Trial watch: peptide vaccines in cancer therapy. Oncoimmunology 2013, 2(December (12)):e26621.
27. Atanackovic D., Luetkens T., Kloth B., Fuchs G., Cao Y., Hildebrandt Y., et al. Cancer-testis antigen expression and its epigenetic modulation in acute myeloid leukemia. Am J Hematol 2011, 86(November (11)):918-922.
28. Griffiths E.A., Choy G., Redkar S., Taverna P., Azab M., Karpf A.R. S.G.I-110. DNA methyltransferase inhibitor, oncolytic. Drugs Fut 2013, 38(8):535.
29. Yoo C.B., Jeong S., Egger G., Liang G., Phiasivongsa P., Tang C., et al. Delivery of 5-aza-2'-deoxycytidine to cells using oligodeoxynucleotides. Cancer Res 2007, 67(July (13)):6400-6408.
30. Kantarjian H., Jabbour E., Yee K., Kropf P., O'Connell C., Stock W., et al. First clinical results of a randomized phase 2 study of SGI-110, a novel subcutaneous (SQ) hypomethylating agent (HMA), in adult patients with acute myeloid leukemia (AML). Blood 2013, 122(21):497.
31. Odunsi K., Matsuzaki J., Karbach J., Neumann A., Mhawech-Fauceglia P., Miller A., et al. Efficacy of vaccination with recombinant vaccinia and fowlpox vectors expressing NY-ESO-1 antigen in ovarian cancer and melanoma patients. Proc Natl Acad Sci U S A 2012, 109(April (15)):5797-5802.
32. Odunsi K., Matsuzaki J., James S.R., Mhawech-Fauceglia P., Tsuji T., Miller A., et al. Epigenetic potentiation of NY-ESO-1 vaccine therapy in human ovarian cancer. Cancer Immunol Res 2014, 2:37-49.
33. Coral S., Parisi G., Nicolay H.J., Colizzi F., Danielli R., Fratta E., et al. Immunomodulatory activity of SGI-110, a 5-aza-2'-deoxycytidine-containing demethylating dinucleotide. Cancer Immunol Immunother 2013, 62(March (3)):605-614.
34. Krishnadas D.K., Bao L., Bai F., Chencheri S.C., Lucas K. Decitabine facilitates immune recognition of sarcoma cells by upregulating CT antigens, MHC molecules, and ICAM-1. Tumour Biol 2014, 35(June (6)):5753-5762.
35. Covre A., Parisi G., Nicolay H.J., Fonsatti E., Fratta E., Sigalotti L., et al. In vivo immunomodulatory activity of SGI-110, a second generation hypomethylating agent, in hematologic malignancies. Cancer Res 2013, 73(Suppl. 8):680.
36. Herman J.G., Graff J.R., Myohanen S., Nelkin B.D., Baylin S.B. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci U S A 1996, 93(September (18)):9821-9826.
37. Li L.C., Dahiya R. MethPrimer. Designing primers for methylation PCRs. Bioinformatics 2002, 18(November (11)):1427-1431.
38. Srivastava P., Yadav N., Lella R., Schneider A., Jones A., Marlowe T., et al. Neem oil limonoids induces p53-independent apoptosis and autophagy. Carcinogenesis 2012, 33(November (11)):2199-2207.
39. Benlalam H., Linard B., Guilloux Y., Moreau-Aubry A., Derre L., Diez E., et al. Identification of five new HLA-B*3501-restricted epitopes derived from common melanoma-associated antigens, spontaneously recognized by tumor-infiltrating lymphocytes. J Immunol 2003, 171(December (11)):6283-6289.
40. Irish J.M., Hovland R., Krutzik P.O., Perez O.D., Bruserud O., Gjertsen B.T., et al. Single cell profiling of potentiated phospho-protein networks in cancer cells. Cell 2004, 118(July (2)):217-228.
41. Woloszynska-Read A., Zhang W., Yu J., Link P.A., Mhawech-Fauceglia P., Collamat G., et al. Coordinated cancer germline antigen promoter and global DNA hypomethylation in ovarian cancer: association with the BORIS/CTCF expression ratio and advanced stage. Clin Cancer Res 2011, 17(April (8)):2170-2180.
42. Betts M.R., Brenchley J.M., Price D.A., De Rosa S.C., Douek D.C., Roederer M., et al. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 2003, 281(October (1-2)):65-78.
43. Sandberg J.K., Fast N.M., Nixon D.F. Functional heterogeneity of cytokines and cytolytic effector molecules in human CD8+ T lymphocytes. J Immunol 2001, 167(July (1)):181-187.
44. Altmann D.M., Hogg N., Trowsdale J., Wilkinson D. Cotransfection of ICAM-1 and HLA-DR reconstitutes human antigen-presenting cell function in mouse L cells. Nature 1989, 338(April (6215)):512-514.
45. Tanaka Y., Fukudome K., Hayashi M., Takagi S., Yoshie O. Induction of ICAM-1 and LFA-3 by Tax1 of human T-cell leukemia virus type 1 and mechanism of down-regulation of ICAM-1 or LFA-1 in adult-T-cell-leukemia cell lines. Int J Cancer 1995, 60(February (4)):554-561.
46. Redkar S., Joshi R., Tang C., Sadikin S., Inloes R., Shi C., et al. Subcutaneous dosing of SGI-110, a second-generation hypomethylating agent, shows activity in mouse xenograft models. AACR Cancer Epigenet 2010.
47. De Plaen E., Arden K., Traversari C., Gaforio J.J., Szikora J.P., De Smet C., et al. Structure, chromosomal localization, and expression of 12 genes of the MAGE family. Immunogenetics 1994, 40(5):360-369.
48. Martinez A., Olarte I., Mergold M.A., Gutierrez M., Rozen E., Collazo J., et al. mRNA expression of MAGE-A3 gene in leukemia cells. Leuk Res 2007, 31(January (1)):33-37.
49. Shichijo S., Tsunosue R., Masuoka K., Natori H., Tamai M., Miyajima J., et al. Expression of the MAGE gene family in human lymphocytic leukemia. Cancer Immunol Immunother 1995, 41(August (2)):90-103.
50. Greiner J., Ringhoffer M., Simikopinko O., Szmaragowska A., Huebsch S., Maurer U., et al. Simultaneous expression of different immunogenic antigens in acute myeloid leukemia. Exp Hematol 2000, 28(December (12)):1413-1422.
51. Chambost H., van Baren N., Brasseur F., Olive D. MAGE-A genes are not expressed in human leukemias. Leukemia 2001, 15(November (11)):1769-1771.
52. Wrangle J., Wang W., Koch A., Easwaran H., Mohammad H.P., Vendetti F., et al. Alterations of immune response of non-small cell lung cancer with azacytidine. Oncotarget 2013, 4(November (11)):2067-2079.
53. Ahuja N., Easwaran H., Baylin S.B. Harnessing the potential of epigenetic therapy to target solid tumors. J Clin Invest 2014, 124(January (1)):56-63.
54. Li H., Chiappinelli K.B., Guzzetta A.A., Easwaran H., Yen R.W., Vatapalli R., et al. Immune regulation by low doses of the DNA methyltransferase inhibitor 5-azacitidine in common human epithelial cancers. Oncotarget 2014, 5(February (3)):587-598.