Acute Hypersensitivity of Pluripotent Testicular Cancer-Derived Embryonal Carcinoma to Low-Dose 5-Aza Deoxycytidine Is Associated with Global DNA Damage-Associated p53 Activation, Anti-Pluripotency and DNA Demethylation

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Biswal, Bijesh K ^a   Beyrouthy, Maroun J ^a   Hever Jardine, Mary P ^a   Armstrong, David ^a   Tomlinson, Craig R ^a   Christensen, Brock C ^a   Marsit, Carmen J ^a   Spinella, Michael J ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; G PROTEIN COUPLED RECEPTOR 30; GROWTH DIFFERENTIATION FACTOR 3; MYC PROTEIN; PROTEIN P53; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

APOPTOSIS; ARTICLE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEMETHYLATION; DNA DAMAGE; DNA METHYLATION; DOWN REGULATION; DRUG EFFICACY; DRUG SENSITIVITY; EMBRYO; EMBRYONAL CARCINOMA STEM CELL; GDF3 GENE; GENE; GENE EXPRESSION REGULATION; GENE REPRESSION; GPER GENE; HUMAN; HUMAN CELL; MALE; NANOG GENE; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN INDUCTION; RIN1 GENE; SOX15 GENE; SOX2 GENE; TESTIS CARCINOMA; TLR4 GENE; UPREGULATION;

ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; AZACITIDINE; CARCINOMA, EMBRYONAL; CELL LINE, TUMOR; DNA DAMAGE; DNA METHYLATION; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; TESTICULAR NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84871664401     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053003     Document Type: Article

References (56)

1. Einhorn LH, (2002) Curing metastatic testicular cancer. Proc Natl Acad Sci USA 99: 4592-4595.
2. Koychev D, Oechsle K, Bokemeyer C, Honecker F, (2011) Treatment of patients with relapsed and/or cisplatin-refractory metastatic germ cell tumours: an update. Int J Androl 34: e266-273.
3. Efstathiou E, Logothetis CJ, (2006) Review of late complications of treatment and late relapse in testicular cancer. J Natl Compr Canc Netw 4: 1059-1070.
4. Kristensen DM, Sonne SB, Ottesen AM, Perrett RM, Nielsen JE, et al. (2008) Origin of pluripotent germ cell tumours: the role of microenvironment during embryonic development. Mol Cell Endocrinol 288: 111-118.
5. Clark AT, (2007) The stem cell identity of testicular cancer. Stem Cell Rev 3: 49-59.
6. Wong DJ, Liu H, Ridky TW, Cassarino D, Segal E, et al. (2008) Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2: 333-344.
7. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, et al. (2008) An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 40: 499-507.
8. Müller FJ, Laurent LC, Kostka D, Ulitsky I, Williams R, et al. (2008) Regulatory networks define phenotypic classes of human stem cell lines. Nature 455: 401-405.
9. Kim J, Woo AJ, Chu J, Snow JW, Fujiwara Y, et al. (2010) A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 143: 313-324.
10. Baylin SB, Jones PA, (2011) A decade of exploring the cancer epigenome - biological and translational implications. Nat Rev Cancer 11: 726-734.
11. Sperger JM, Chen X, Draper JS, Antosiewicz JE, Chon CH, et al. (2003) Gene expression patterns in human embryonic stem cells and human pluripotent germ cell tumors. Proc Natl Acad Sci USA 100: 13350-13355.
12. Fouse SD, Shen Y, Pellegrini M, Cole S, Meissner A, et al. (2008) Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation. Cell Stem Cell 2: 160-169.
13. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, et al. (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315-322.
14. Hawkins RD, Hon GC, Lee LK, Ngo Q, Lister R, et al. (2010) Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 6: 479-491.
15. Okamoto K, (2012) Epigenetics: A way to understand the origin and biology of testicular germ cell tumors. Int J Urol 19: 504-511.
16. Cheung HH, Lee TL, Davis AJ, Taft DH, Rennert OM, et al. (2010) Genome-wide DNA methylation profiling reveals novel epigenetically regulated genes and non-coding RNAs in human testicular cancer. Br J Cancer 102: 419-427.
17. Yang X, Lay F, Han H, Jones PA, (2010) Targeting DNA methylation for epigenetic therapy. Trends Pharmacol Sci 31: 536-546.
18. Baylin SB, Chen WY, (2005) Aberrant gene silencing in tumor progression: implications for control of cancer. Cold Spring Harb Symp Quant Biol 70: 427-433.
19. Jüttermann R, Li E, Jaenisch R, (1994) Toxicity of 5-aza-2′-deoxycytidine to mammalian cells is mediated primarily by covalent trapping of DNA methyltransferase rather than DNA demethylation. Proc Natl Acad Sci USA 91: 11797-11801.
20. Palii SS, Van Emburgh BO, Sankpal UT, Brown KD, Robertson KD, (2008) DNA methylation inhibitor 5-Aza-2′-deoxycytidine induces reversible genome-wide DNA damage that is distinctly influenced by DNA methyltransferases 1 and 3B. Mol Cell Biol 28: 752-771.
21. Beyrouthy MJ, Garner KM, Hever MP, Freemantle SJ, Eastman A, et al. (2009) High DNA methyltransferase 3B expression mediates 5-aza-deoxycytidine hypersensitivity in testicular germ cell tumors. Cancer Res 69: 9360-9366.
22. Issa JP, (2007) DNA methylation as a therapeutic target in cancer. Clin Cancer Res 13: 1634-1637.
23. Juergens RA, Wrangle J, Vendetti FP, Murphy SC, Zhao M, et al. (2011) Combination epigenetic therapy has efficacy in patients with refractory advanced non-small cell lung cancer. Cancer Discov 1: 598-607.
24. Tsai HC, Li H, Van Neste L, Cai Y, Robert C, et al. (2012) Transient low doses of DNA-demethylating agents exert durable antitumor effects on hematological and epithelial tumor cells. Cancer Cell 21: 430-446.
25. Kerley-Hamilton JS, Pike AM, Li N, DiRenzo J, Spinella MJ, (2005) A p53-dominant transcriptional response to cisplatin in testicular germ cell tumor-derived human embryonal carcinoma. Oncogene 24: 6090-60100.
26. Schlosser I, Hölzel M, Hoffmann R, Burtscher H, Kohlhuber F, et al. (2005) Dissection of transcriptional programmes in response to serum and c-Myc in a human B-cell line. Oncogene 24: 520-524.
27. Schuhmacher M, Kohlhuber F, Hölzel M, Kaiser C, Burtscher H, et al. (2001) The transcriptional program of a human B cell line in response to Myc. Nucleic Acids Res 29: 397-406.
28. Missiaglia E, Donadelli M, Palmieri M, Crnogorac-Jurcevic T, Scarpa A, et al. (2005) Growth delay of human pancreatic cancer cells by methylase inhibitor 5-aza-2′-deoxycytidine treatment is associated with activation of the interferon signalling pathway. Oncogene 24: 199-211.
29. Mueller W, Nutt CL, Ehrich M, Riemenschneider MJ, von Deimling A, et al. (2007) Downregulation of RUNX3 and TES by hypermethylation in glioblastoma. Oncogene 26: 583-593.
30. Giuliano CJ, Kerley-Hamilton JS, Bee T, Freemantle SJ, Manickaratnam R, et al. (2005) Retinoic acid represses a cassette of candidate pluripotency chromosome 12p genes during induced loss of human embryonal carcinoma tumorigenicity. Biochim Biophys Acta 1731: 48-56.
31. Korkola JE, Houldsworth J, Chadalavada RS, Olshen AB, Dobrzynski D, et al. (2006) Down-regulation of stem cell genes, including those in a 200-kb gene cluster at 12p13.31, is associated with in vivo differentiation of human male germ cell tumors. Cancer Res 66: 820-827.
32. Jiemjit A, Fandy TE, Carraway H, Bailey KA, Baylin S, et al. (2008) p21(WAF1/CIP1) induction by 5-azacytosine nucleosides requires DNA damage. Oncogene 27: 3615-3623.
33. Maslov AY, Lee M, Gundry M, Gravina S, Strogonova N, et al. (2012) 5-Aza-2′-deoxycytidine-induced genome rearrangements are mediated by DNMT1. Oncogene e-pub ahead of print doi: 10.1038/onc.2012.9.
34. Gutekunst M, Oren M, Weilbacher A, Dengler MA, Markwardt C, et al. (2011) p53 hypersensitivity is the predominant mechanism of the unique responsiveness of testicular germ cell tumor (TGCT) cells to cisplatin. PLoS One 6: e19198.
35. Duale N, Lindeman B, Komada M, Olsen AK, Andreassen A, et al. (2007) Molecular portrait of cisplatin induced response in human testis cancer cell lines based on gene expression profiles. Mol Cancer 6: 53.
36. Koster R, Timmer-Bosscha H, Bishoff R, Gietema JA, de Jong S, (2011) Disruption of the MDM2-p53 interaction strongly potentiates p53-dependent apoptosis in cisplatin-resistant human testicular carcinoma cells via the Fas/FasL pathway. Cell Death Dis 2: e148.
37. Kawamura T, Suzuki J, Wang YV, Menendez S, Morera LB, et al. (2009) Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 460: 1140-1144.
38. Li H, Collado M, Villasante A, Strati K, Ortega S, et al. (2009) The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 460: 1136-1139.
39. Marión RM, Strati K, Li H, Murga M, Blanco R, et al. (2009) A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 460: 1149-1153.
40. Curtin JC, Dragnev KH, Sekula D, Christie AJ, Dmitrovsky E, et al. (2001) Retinoic acid activates p53 in human embryonal carcinoma through retinoid receptor-dependent stimulation of p53 transactivation function. Oncogene 20: 2559-2569.
41. Lin T, Chao C, Saito S, Mazur SJ, Murphy ME, et al. (2005) p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat Cell Biol 7: 165-171.
42. Li M, He Y, Dubois W, Wu X, Shi J, et al. (2012) Distinct regulatory mechanisms and functions for p53-activated and p53-repressed DNA damage response genes in embryonic stem cells. Mol Cell 46: 30-42.
43. Doi A, Park IH, Wen B, Murakami P, Aryee MJ, et al. (2009) Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet 41: 1350-1353.
44. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, et al. (2001) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480: 490-495.
45. Huang K, Fan G, (2010) DNA methylation in cell differentiation and reprogramming: an emerging systematic view. Regen Med 5: 531-544.
46. Heyn H, Vidal E, Sayols S, Sanchez-Mut JV, Moran S, et al. (2012) Whole-genome bisulfite DNA sequencing of a DNMT3B mutant patient. Epigenetics 7: 542-550.
47. Ziller MJ, Müller F, Liao J, Zhang Y, Gu H, et al. (2011) Genomic distribution and inter-sample variation of non-CpG methylation across human cell types. PLoS Genet 7: e1002389.
48. Oka M, Meacham AM, Hamazaki T, Rodić N, Chang LJ, et al. (2005) De novo DNA methyltransferases Dnmt3a and Dnmt3b primarily mediate the cytotoxic effect of 5-aza-2′-deoxycytidine. Oncogene 24: 3091-3099.
49. Bachman KE, Rountree MR, Baylin SB, (2001) Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J Biol Chem 276: 32282-32287.
50. Jurkowska RZ, Jurkowski TP, Jeltsch A, (2011) Structure and function of mammalian DNA methyltransferases. Chembiochem 12: 206-222.
51. Jin B, Yao B, Li JL, Fields CR, Delmas AL, et al. (2009) DNMT1 and DNMT3B modulate distinct polycomb-mediated histone modifications in colon cancer. Cancer Res 69: 7412-7421.
52. Gopalakrishnan S, Sullivan BA, Trazzi S, Della Valle G, Robertson KD, (2009) DNMT3B interacts with constitutive centromere protein CENP-C to modulate DNA methylation and the histone code at centromeric regions. Hum Mol Genet 18: 3178-3193.
53. Geiman TM, Sankpal UT, Robertson AK, Chen Y, Mazumdar M, et al. (2004) Isolation and characterization of a novel DNA methyltransferase complex linking DNMT3B with components of the mitotic chromosome condensation machinery. Nucleic Acids Res 32: 2716-29.
54. Weisenberger DJ, Velicescu M, Cheng JC, Gonzales FA, Liang G, et al. (2004) Role of the DNA methyltransferase variant DNMT3b3 in DNA methylation. Mol Cancer Res 2: 62-72.
55. Kashiwagi K, Nimura K, Ura K, Kaneda Y, (2011) DNA methyltransferase 3B preferentially associates with condensed chromatin. Nucleic Acids Res 39: 874-888.
56. Wilhelm CS, Kelsey KT, Butler R, Plaza S, Gagne L, et al. (2010) Implications of LINE1 methylation for bladder cancer risk in women. Clin Cancer Res 2010 16: 1682-1689.