Analysis of DNA methylation and gene expression in radiation-resistant head and neck tumors

Epigenetics

Volumn 10, Issue 6, 2015, Pages 545-561

  Chen, Xiaofei ^a   Liu, Liang ^a   Mims, Jade ^a   Punska, Elizabeth C ^b   Williams, Kristin E ^b   Zhao, Weiling ^a   Arcaro, Kathleen F ^b   Tsang, Allen W ^a   Zhou, Xiaobo ^a   Furdui, Cristina M ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

DNA methylation; Gene expression; Head and neck squamous cell cancer (HNSCC); Radiation resistance; The Cancer Genome Atlas (TCGA)

Indexed keywords

5 METHYLCYTOSINE; GLUCOCORTICOID RECEPTOR; INTEGRIN LINKED KINASE; AZACITIDINE; CCND2 PROTEIN, HUMAN; CYCLIN D2; DECITABINE;

ARTICLE; CELL CYCLE REGULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA EXTRACTION; DNA METHYLATION; DNA MICROARRAY; DOWN REGULATION; FATTY ACID OXIDATION; GENE EXPRESSION; HEAD AND NECK CANCER; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR SIGNALING; PROMOTER REGION; PYROSEQUENCING; RADIATION DOSE; RADIATION RESISTANT HEAD AND NECK TUMOR; RADIOSENSITIVITY; REGULATORY MECHANISM; SCORING SYSTEM; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; HEAD AND NECK NEOPLASMS; PATHOLOGY; RADIATION RESPONSE; RADIATION TOLERANCE; TUMOR CELL LINE;

AZACITIDINE; CELL LINE, TUMOR; CPG ISLANDS; CYCLIN D2; DNA METHYLATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HUMANS; PROMOTER REGIONS, GENETIC; RADIATION TOLERANCE;

EID: 84943782960     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.1080/15592294.2015.1048953     Document Type: Article

References (53)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014; 64: 9-29; PMID: 24399786; http://dx. doi. org/10. 3322/caac. 21208.
2. Delaney G, Jacob S, Featherstone C, Barton M. The role of radiotherapy in cancer treatment: estimating optimal utilization from a review of evidence-based clinical guidelines. Cancer 2005; 104: 1129-37; PMID: 16080176; http://dx. doi. org/10. 1002/cncr. 21324.
3. Begg AC, Stewart FA, Vens C. Strategies to improve radiotherapy with targeted drugs. Nat Rev Cancer 2011; 11: 239-53; PMID: 21430696; http://dx. doi. org/10. 1038/nrc3007.
4. Bansal N, Mims J, Kuremsky JG, Olex AL, Zhao W, Yin L, Wani R, Qian J, Center B, Marrs GS, et al. Broad phenotypic changes associated with gain of radiation resistance in head and neck squamous cell cancer. Antioxid Redox Signal 2014; 21: 221-36; PMID: 24597745; http://dx. doi. org/10. 1089/ars. 2013. 5690.
5. Esteller M. Epigenetics in cancer. N Engl J Med 2008; 358: 1148-59; PMID: 18337604; http://dx. doi. org/10. 1056/NEJMra072067.
6. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002; 3: 415-28; PMID: 12042769; http://dx. doi. org/10. 1038/nrg962.
7. Singal R, Ginder GD. DNA methylation. Blood 1999; 93: 4059-70; PMID: 10361102.
8. Das PM, Singal R. DNA methylation and cancer. J Clin Oncol 2004; 22: 4632-42; PMID: 15542813; http://dx. doi. org/10. 1200/JCO. 2004. 07. 151.
9. Bibikova M, Barnes B, Tsan C, Ho V, Klotzle B, Le JM, Delano D, Zhang L, Schroth GP, Gunderson KL, et al. High density DNA methylation array with single CpG site resolution. Genomics 2011; 98: 288-95; PMID: 21839163; http://dx. doi. org/10. 1016/j. ygeno. 2011. 07. 007.
10. Takano Y, Kato Y, van Diest PJ, Masuda M, Mitomi H, Okayasu I. Cyclin D2 overexpression and lack of p27 correlate positively and cyclin E inversely with a poor prognosis in gastric cancer cases. Amer J Pathol 2000; 156: 585-94; http://dx. doi. org/10. 1016/S0002-9440(10)64763-3.
11. Li R, Waga S, Hannon GJ, Beach D, Stillman B. Differential effects by the p21 CDK inhibitor on PCNAdependent DNA replication and repair. Nature 1994; 371: 534-7; PMID: 7935768; http://dx. doi. org/10. 1038/371534a0.
12. Rossig L, Jadidi AS, Urbich C, Badorff C, Zeiher AM, Dimmeler S. Akt-dependent phosphorylation of p21 (Cip1) regulates PCNA binding and proliferation of endothelial cells. Mol Cell Biol 2001; 21: 5644-57; PMID: 11463845; http://dx. doi. org/10. 1128/MCB. 21. 16. 5644-5657. 2001.
13. Brieger J, Mann SA, Pongsapich W, Koutsimpelas D, Fruth K, Mann WJ. Pharmacological genome demethylation increases radiosensitivity of head and neck squamous carcinoma cells. Int J Mol Med 2012; 29: 505-9; PMID: 22109647.
14. Hofstetter B, Niemierko A, Forrer C, Benhattar J, Albertini V, Pruschy M, Bosman FT, Catapano CV, Ciernik IF. Impact of genomic methylation on radiation sensitivity of colorectal carcinoma. Int J Radiat Oncol Biol Phys 2010; 76: 1512-9; PMID: 20338477; http://dx. doi. org/10. 1016/j. ijrobp. 2009. 10. 037.
15. Jiang W, Li YQ, Liu N, Sun Y, He QM, Jiang N, Xu YF, Chen L, Ma J. Five-Azacytidine enhances the radiosensitivity of CNE2 and SUNE1 cells in vitro and in vivo possibly by altering DNA methylation. PLoS One 2014; 9: e93273; PMID: 24691157; http://dx. doi. org/10. 1371/journal. pone. 0093273.
16. Li Y, Geng P, Jiang W, Wang Y, Yao J, Lin X, Liu J, Huang L, Su B, ChenH. Enhancement of radiosensitivity by 5-Aza-CdR through activation of G2/M checkpoint response and apoptosis in osteosarcoma cells. Tumour Biol 2014; 35: 4831-9; PMID: 24474250; http://dx. doi. org/10. 1007/s13277-014-1634-5.
17. Qiu H, Yashiro M, Shinto O, Matsuzaki T, Hirakawa K. DNA methyltransferase inhibitor 5-aza-CdR enhances the radiosensitivity of gastric cancer cells. Cancer Sci 2009; 100: 181-8; PMID: 19037991; http://dx. doi. org/10. 1111/j. 1349-7006. 2008. 01004. x.
18. Wang L, Zhang Y, Li R, Chen Y, Pan X, Li G, Dai F, Yang J. Five-aza-2'-Deoxycytidine enhances the radiosensitivity of breast cancer cells. Cancer Biother Radiopharm 2013; 28: 34-44; PMID: 22917213; http://dx. doi. org/10. 1089/cbr. 2012. 1170.
19. Fuso A, Nicolia V, Pasqualato A, Fiorenza MT, Cavallaro RA, Scarpa S. Changes in Presenilin 1 gene methylation pattern in diet-induced B vitamin deficiency. Neurobiol Aging 2011; 32: 187-99; PMID: 19329227; http://dx. doi. org/10. 1016/j. neurobiolaging. 2009. 02. 013.
20. Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol 2010; 28: 1057-68; PMID: 20944598; http://dx. doi. org/10. 1038/nbt. 1685.
21. Chaudhry MA, Omaruddin RA. Differential DNA methylation alterations in radiation-sensitive and-resistant cells. DNA Cell Biol 2012; 31: 908-16; PMID: 22185261; http://dx. doi. org/10. 1089/dna. 2011. 1509.
22. Antwih DA, Gabbara KM, Lancaster WD, Ruden DM, Zielske SP. Radiation-induced epigenetic DNA methylation modification of radiation-response pathways. Epigenetics 2013; 8: 839-48; PMID: 23880508; http://dx. doi. org/10. 4161/epi. 25498.
23. Pogribny I, Raiche J, Slovack M, Kovalchuk O. Dosedependence, sex-and tissue-specificity, and persistence of radiation-induced genomic DNA methylation changes. Biochem Biophys Res Commun 2004; 320: 1253-61; PMID: 15249225; http://dx. doi. org/10. 1016/j. bbrc. 2004. 06. 081.
24. Kuhmann C, WeichenhanD, Rehli M, PlassC, Schmezer P, PopandaO. DNA methylation changes in cells regrowing after fractioned ionizing radiation. Radiother Oncol 2011; 101: 116-21; PMID: 21704414; http://dx. doi. org/10. 1016/j. radonc. 2011. 05. 048.
25. Loree J, Koturbash I, Kutanzi K, Baker M, Pogribny I, Kovalchuk O. Radiation-induced molecular changes in rat mammary tissue: possible implications for radiation-induced carcinogenesis. Int J Radiat Biol 2006; 82: 805-15; PMID: 17148264; http://dx. doi. org/10. 1080/09553000600960027.
26. Kim EH, Park AK, Dong SM, Ahn JH, Park WY. Global analysis of CpG methylation reveals epigenetic control of the radiosensitivity in lung cancer cell lines. Oncogene 2010; 29: 4725-31; PMID: 20531302; http://dx. doi. org/10. 1038/onc. 2010. 223.
27. Wang KY, Chen CC, Shen CK. Active DNA demethylation of the vertebrate genomes by DNA methyltransferases: deaminase, dehydroxymethylase or demethylase? Epigenomics 2014; 6: 353-63; PMID: 25111488; http://dx. doi. org/10. 2217/epi. 14. 21.
28. Chen CC, Wang KY, Shen CK. The mammalian de novo DNA methyltransferases DNMT3A and DNMT3B are also DNA 5-hydroxymethylcytosine dehydroxymethylases. J Biol Chem 2012; 287: 33116-21; PMID: 22898819; http://dx. doi. org/10. 1074/jbc. C112. 406975.
29. Turk PW, Laayoun A, Smith SS, Weitzman SA. DNA adduct 8-hydroxyl-2'-deoxyguanosine (8-hydroxyguanine) affects function of human DNA methyltransferase. Carcinogenesis 1995; 16: 1253-5; PMID: 7767994; http://dx. doi. org/10. 1093/carcin/16. 5. 1253.
30. Doi A, Park IH, Wen B, Murakami P, Aryee MJ, Irizarry R, Herb B, Ladd-Acosta C, Rho J, Loewer S, et al. Differential methylation of tissue-and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet 2009; 41: 1350-3; PMID: 19881528; http://dx. doi. org/10. 1038/ng. 471.
31. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M, et al. The human colon cancer methylome shows similar hypo-and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 2009; 41: 178-86; PMID: 19151715; http://dx. doi. org/10. 1038/ng. 298.
32. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012; 13: 484-92; PMID: 22641018; http://dx. doi. org/10. 1038/nrg3230.
33. Pawlik TM, Keyomarsi K. Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys 2004; 59: 928-42; PMID: 15234026; http://dx. doi. org/10. 1016/j. ijrobp. 2004. 03. 005.
34. Edwards PA, Kennedy MA, Mak PA. LXRs; oxysterolactivated nuclear receptors that regulate genes controlling lipid homeostasis. Vascul Pharmacol 2002; 38: 249-56; PMID: 12449021; http://dx. doi. org/10. 1016/S1537-1891(02)00175-1.
35. Stresemann C, Lyko F. Modes of action of the DNA methyltransferase inhibitors azacytidine and decitabine. Int J Cancer 2008; 123: 8-13; PMID: 18425818; http://dx. doi. org/10. 1002/ijc. 23607.
36. Christman JK. Five-Azacytidine and 5-aza-2'-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene 2002; 21: 5483-95; PMID: 12154409; http://dx. doi. org/10. 1038/sj. onc. 1205699.
37. Yuan BZ, Jefferson AM, Popescu NC, Reynolds SH. Aberrant gene expression in human non small cell lung carcinoma cells exposed to demethylating agent 5-aza-2'-deoxycytidine. Neoplasia 2004; 6: 412-9; PMID: 15256063; http://dx. doi. org/10. 1593/neo. 03490.
38. Menendez L, Walker D, Matyunina LV, Dickerson EB, Bowen NJ, Polavarapu N, Benigno BB, McDonald JF. Identification of candidate methylation-responsive genes in ovarian cancer. Mol Cancer 2007; 6: 10; PMID: 17254359; http://dx. doi. org/10. 1186/1476-4598-6-10.
39. Ando T, Nishimura M, Oka Y. Decitabine (5-Aza-2'-deoxycytidine) decreased DNA methylation and expression of MDR-1 gene in K562/ADM cells. Leukemia 2000; 14: 1915-20; PMID: 11069027; http://dx. doi. org/10. 1038/sj. leu. 2401914.
40. Kitagawa Y, Kyo S, Takakura M, Kanaya T, Koshida K, Namiki M, Inoue M. Demethylating reagent 5-azacytidine inhibits telomerase activity in human prostate cancer cells through transcriptional repression of hTERT. Clin Cancer Res 2000; 6: 2868-75; PMID: 10914736.
41. Wong J, Sia YY, Misso NL, Aggarwal S, Ng A, Bhoola KD. Effects of the demethylating agent, 5-azacytidine, on expression of the kallikrein-kinin genes in carcinoma cells of the lung and pleura. Patholog Res Int 2011; 2011: 167046; PMID: 21904690.
42. Liang K, Jin W, Knuefermann C, Schmidt M, Mills GB, Ang KK, Milas L, Fan Z. Targeting the phosphatidylinositol 3-kinase/Akt pathway for enhancing breast cancer cells to radiotherapy. Mol Cancer Ther 2003; 2: 353-60; PMID: 12700279.
43. Gupta AK, Cerniglia GJ, Mick R, Ahmed MS, Bakanauskas VJ, Muschel RJ, McKenna WG. Radiation sensitization of human cancer cells in vivo by inhibiting the activity of PI3K using LY294002. Int J Rad Oncol Biol Phys 2003; 56: 846-53; http://dx. doi. org/10. 1016/S0360-3016(03)00214-1.
44. Gupta AK, McKenna WG, Weber CN, Feldman MD, Goldsmith JD, Mick R, Machtay M, Rosenthal DI, Bakanauskas VJ, Cerniglia GJ, et al. Local recurrence in head and neck cancer: relationship to radiation resistance and signal transduction. Clin Cancer Res 2002; 8: 885-92; PMID: 11895923.
45. Bussink J, van der Kogel AJ, Kaanders JH. Activation of the PI3-K/AKT pathway and implications for radioresistance mechanisms in head and neck cancer. Lancet Oncol 2008; 9: 288-96; PMID: 18308254; http://dx. doi. org/10. 1016/S1470-2045(08)70073-1.
46. Huang KH, Huang SF, Chen IH, Liao CT, Wang HM, Hsieh LL. Methylation of RASSF1A, RASSF2A, and HIN-1 is associated with poor outcome after radiotherapy, but not surgery, in oral squamous cell carcinoma. Clin Cancer Res 2009; 15: 4174-80; PMID: 19509163; http://dx. doi. org/10. 1158/1078-0432. CCR-08-2929.
47. Mims J, Bansal N, Bharadwaj MS, Chen X, Molina AJ, Tsang AW, Furdui CM. Energy metabolism in a matched model of radiation resistance for head and neck squamous cell cancer. Radiat Res 2015; 183: 291-304; PMID: 25738895; http://dx. doi. org/10. 1667/RR13828. 1.
48. Reed MF, Liu VF, Ladha MH, Ando K, Griffin JD, Weaver DT, Ewen ME. Enforced CDK4 expression in a hematopoietic cell line confers resistance to the G1 arrest induced by ionizing radiation. Oncogene 1998; 17: 2961-71; PMID: 9881698; http://dx. doi. org/10. 1038/sj. onc. 1202450.
49. Kim HJ, Kim JH, Chie EK, Young PD, Kim IA, Kim IH. DNMT (DNA methyltransferase) inhibitors radiosensitize human cancer cells by suppressing DNA repair activity. Radiat Oncol 2012; 7: 39; PMID: 22429326; http://dx. doi. org/10. 1186/1748-717X-7-39.
50. Roy K, Wang L, Makrigiorgos GM, Price BD. Methylation of the ATM promoter in glioma cells alters ionizing radiation sensitivity. Biochem Biophys Res Commun 2006; 344: 821-6; PMID: 16631604; http://dx. doi. org/10. 1016/j. bbrc. 2006. 03. 222.
51. Karolchik D, Barber GP, Casper J, Clawson H, Cline MS, Diekhans M, Dreszer TR, Fujita PA, Guruvadoo L, Haeussler M, et al. The UCSC Genome Browser database: 2014 update. Nucleic Acids Res 2014; 42: D764-70; PMID: 24270787; http://dx. doi. org/10. 1093/nar/gkt1168.
52. Gardiner-Garden M, Frommer M. CpG islands in vertebrate genomes. J Mol Biol 1987; 196: 261-82; PMID: 3656447; http://dx. doi. org/10. 1016/0022-2836(87)90689-9.
53. Benjamini Y, Hochberg Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 1995; 57: 289-300.