Epigenetic screen identifies genotype-specific promoter DNA methylation and oncogenic potential of CHRNB4

Oncogene

Volumn 32, Issue 28, 2013, Pages 3329-3338

  Scherf, D B ^a   Sarkisyan, N ^a   Jacobsson, H ^a   Claus, R ^a   Bermejo, J L ^b   Peil, B ^b   Gu, L ^a   Muley, T ^c   Meister, M ^c   Dienemann, H ^c   Plass, C ^a   Risch, A ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

CHRNB4; DNA methylation; Non small cell lung cancer (NSCLC); Risk factors; TERT

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; DNA; RNA; TELOMERASE REVERSE TRANSCRIPTASE;

ADULT; AGED; ARTICLE; CANCER RISK; CARCINOGENICITY; CPG ISLAND; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC SCREENING; GENETIC SUSCEPTIBILITY; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LUNG CANCER; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; TOBACCO DEPENDENCE;

AZACITIDINE; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL PROLIFERATION; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HUMANS; LUNG NEOPLASMS; NERVE TISSUE PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; RECEPTORS, NICOTINIC;

EID: 84880263616     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.344     Document Type: Article

References (49)

1. Amos CI, Wu X, Broderick P, Gorlov IP, Gu J, Eisen T et al. Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1. Nat Genet 2008; 40: 616-622.
2. Hung RJ, McKay JD, Gaborieau V, Boffetta P, Hashibe M, Zaridze D et al. A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature 2008; 452: 633-637.
3. Thorgeirsson TE, Geller F, Sulem P, Rafnar T, Wiste A, Magnusson KP et al. A variant associated with nicotine dependence, lung cancer and peripheral arterial disease. Nature 2008; 452: 638-642.
4. McKay JD, Hung RJ, Gaborieau V, Boffetta P, Chabrier A, Byrnes G et al. Lung cancer susceptibility locus at 5p15.33. Nat Genet 2008; 40: 1404-1406.
5. Wang Y, Broderick P, Webb E, Wu X, Vijayakrishnan J, Matakidou A et al. Common 5p15.33 and 6p21.33 variants influence lung cancer risk. Nat Genet 2008; 40: 1407-1409.
6. Freedman ML, Monteiro AN, Gayther SA, Coetzee GA, Risch A, Plass C et al. Principles for the post-GWAs functional characterization of cancer risk loci. Nat Genet 2011; 43: 513-518.
7. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55: 74-108.
8. Coolen MW, Statham AL, Gardiner-Garden M, Clark SJ. Genomic profiling of CpG methylation and allelic specificity using quantitative high-throughput mass spectrometry: critical evaluation and improvements. Nucleic Acids Res 2007; 35: e119.
9. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003; 349: 2042-2054.
10. He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004; 5: 522-531.
11. Dai Z, Lakshmanan RR, Zhu WG, Smiraglia DJ, Rush LJ, Fruhwald MC et al. Global methylation profiling of lung cancer identifies novel methylated genes. Neoplasia 2001; 3: 314-323.
12. Shivapurkar N, Stastny V, Xie Y, Prinsen C, Frenkel E, Czerniak B et al. Differential methylation of a short CpG-rich sequence within exon 1 of TCF21 gene: a promising cancer biomarker assay. Cancer Epidemiol Biomarkers Prev 2008; 17: 995-1000.
13. Belinsky SA, Nikula KJ, Palmisano WA, Michels R, Saccomanno G, Gabrielson E et al. Aberrant methylation of p16(INK4a) is an early event in lung cancer and a potential biomarker for early diagnosis. Proc Natl Acad Sci USA 1998; 95: 11891-11896.
14. Belinsky SA, Liechty KC, Gentry FD, Wolf HJ, Rogers J, Vu K et al. Promoter hypermethylation of multiple genes in sputum precedes lung cancer incidence in a high-risk cohort. Cancer Res 2006; 66: 3338-3344.
15. Brena RM, Morrison C, Liyanarachchi S, Jarjoura D, Davuluri RV, Otterson GA et al. Aberrant DNA methylation of OLIG1, a novel prognostic factor in non-small cell lung cancer. PLoS Med 2007; 4: e108.
16. Brena RM, Costello JF. Genome-epigenome interactions in cancer. Hum Mol Genet 2007; 1: R96-R10516 Spec No.
17. Esteller M, Garcia A, Martinez Palones JM, Xercavins J, Reventos J. Germ line polymorphisms in cytochrome-P450 1A1 (C4887 CYP1A1) and methylenetetrahydrofolate reductase (MTHFR) genes and endometrial cancer susceptibility. Carcinogenesis 1997; 18: 2307-2311.
18. Shames DS, Girard L, Gao B, Sato M, Lewis CM, Shivapurkar N et al. A genomewide screen for promoter methylation in lung cancer identifies novel methylation markers for multiple malignancies. PLoS Med 2006; 3: e486.
19. Laird PW. Principles and challenges of genome-wide DNA methylation analysis. Nat Rev Genet 2010; 11: 191-203.
20. Park JC, Chae YK, Son CH, Kim MS, Lee J, Ostrow K et al. Epigenetic silencing of human T (brachyury homologue) gene in non-small-cell lung cancer. Biochem Biophys Res Commun 2008; 365: 221-226.
21. Hitchins MP, Rapkins RW, Kwok CT, Srivastava S, Wong JJ, Khachigian LM et al. Dominantly inherited constitutional epigenetic silencing of MLH1 in a canceraffected family is linked to a single nucleotide variant within the 50UTR. Cancer Cell 2011; 20: 200-213.
22. Paliwal A, Vaissiere T, Krais A, Cuenin C, Cros MP, Zaridze D et al. Aberrant DNA methylation links cancer susceptibility locus 15q25.1 to apoptotic regulation and lung cancer. Cancer Res 2010; 70: 2779-2788.
23. Renaud S, Loukinov D, Abdullaev Z, Guilleret I, Bosman FT, Lobanenkov V et al. Dual role of DNA methylation inside and outside of CTCF-binding regions in the transcriptional regulation of the telomerase hTERT gene. Nucleic Acids Res 2007; 35: 1245-1256.
24. Schalkwyk LC, Meaburn EL, Smith R, Dempster EL, Jeffries AR, Davies MN et al. Allelic skewing of DNA methylation is widespread across the genome. Am J Hum Genet 2010; 86: 196-212.
25. Kerkel K, Spadola A, Yuan E, Kosek J, Jiang L, Hod E et al. Genomic surveys by methylation-sensitive SNP analysis identify sequence-dependent allele-specific DNA methylation. Nat Genet 2008; 40: 904-908.
26. Zhang Y, Rohde C, Reinhardt R, Voelcker-Rehage C, Jeltsch A. Non-imprinted allele-specific DNA methylation on human autosomes. Genome Biol 2009; 10: R138.
27. Amos CI, Gorlov IP, Dong Q, Wu X, Zhang H, Lu EY et al. Nicotinic acetylcholine receptor region on chromosome 15q25 and lung cancer risk among African Americans: a case-control study. J Natl Cancer Inst 2011; 102: 1199-1205.
28. Schlaepfer IR, Hoft NR, Collins AC, Corley RP, Hewitt JK, Hopfer CJ et al. The CHRNA5/A3/B4 gene cluster variability as an important determinant of early alcohol and tobacco initiation in young adults. Biol Psychiatry 2008; 63: 1039-1046.
29. Stephens SH, Hoft NR, Schlaepfer IR, Young SE, Corley RC, McQueen MB et al. Externalizing behaviors are associated with SNPs in the CHRNA5/CHRNA3/CHRNB4 gene cluster. Behav Genet 2011; 42: 402-414.
30. Erlich PM, Hoffman SN, Rukstalis M, Han JJ, Chu X, Linda Kao WH et al. Nicotinic acetylcholine receptor genes on chromosome 15q25.1 are associated with nicotine and opioid dependence severity. Hum Genet 2010; 128: 491-499.
31. Improgo MR, Schlichting NA, Cortes RY, Zhao-Shea R, Tapper AR, Gardner PD. ASCL1 regulates the expression of the CHRNA5/A3/B4 lung cancer susceptibility locus. Mol Cancer Res 8: 194-203.
32. Jones PA. The DNA methylation paradox. Trends Genet 1999; 15: 34-37.
33. Allemand E, Batsche E, Muchardt C. Splicing, transcription, and chromatin: a menage a trois. Curr Opin Genet Dev 2008; 18: 145-151.
34. Luco RF, Pan Q, Tominaga K, Blencowe BJ, Pereira-Smith OM, Misteli T. Regulation of alternative splicing by histone modifications. Science 2010; 327: 996-1000.
35. Chodavarapu RK, Feng S, Bernatavichute YV, Chen PY, Stroud H, Yu Y et al. Relationship between nucleosome positioning and DNA methylation. Nature 2010; 466: 388-392.
36. McCabe MT, Lee EK, Vertino PM. A multifactorial signature of DNA sequence and polycomb binding predicts aberrant CpG island methylation. Cancer Res 2009; 69: 282-291.
37. Gebhard C, Benner C, Ehrich M, Schwarzfischer L, Schilling E, Klug M et al. General transcription factor binding at CpG islands in normal cells correlates with resistance to de novo DNA methylation in cancer cells. Cancer Res 2010; 70: 1398-1407.
38. Herceg Z. Epigenetic information in chromatin and cancer. Eur J Cancer 2009; 45: 442-444.
39. Chen SS, Raval A, Johnson AJ, Hertlein E, Liu TH, Jin VX et al. Epigenetic changes during disease progression in a murine model of human chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2009; 106: 13433-13438.
40. Van den Berg RM, Brokx H, Vesin A, Field JK, Brambilla C, Meijer CJ et al. Prognostic value of hTERT mRNA expression in surgical samples of lung cancer patients: the European Early Lung Cancer Project. Int J Oncol 2010; 37: 455-461.
41. Schuller HM. Is cancer triggered by altered signalling of nicotinic acetylcholine receptors? Nat Rev Cancer 2009; 9: 195-205.
42. Schuller HM, Tithof PK, Williams M, Plummer 3rd H. The tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone is a beta-adrenergic agonist and stimulates DNA synthesis in lung adenocarcinoma via beta-adrenergic receptor-mediated release of arachidonic acid. Cancer Res 1999; 59: 4510-4515.
43. Kawai H, Berg DK. Nicotinic acetylcholine receptors containing alpha 7 subunits on rat cortical neurons do not undergo long-lasting inactivation even when upregulated by chronic nicotine exposure. J Neurochem 2001; 78: 1367-1378.
44. Joseph J, Niggemann B, Zaenker KS, Entschladen F. The neurotransmitter gammaaminobutyric acid is an inhibitory regulator for the migration of SW 480 colon carcinoma cells. Cancer Res 2002; 62: 6467-6469.
45. Shiraishi K, Kohno T, Kunitoh H, Watanabe S, Goto K, Nishiwaki Y et al. Contribution of nicotine acetylcholine receptor polymorphisms to lung cancer risk in a smoking-independent manner in the Japanese. Carcinogenesis 2009; 30: 65-70.
46. Liu Y, Liu P, Wen W, James MA, Wang Y, Bailey-Wilson JE et al. Haplotype and cell proliferation analyses of candidate lung cancer susceptibility genes on chromosome 15q24-25.1. Cancer Res 2009; 69: 7844-7850.
47. Ehrich M, Nelson MR, Stanssens P, Zabeau M, Liloglou T, Xinarianos G et al. Quantitative high-throughput analysis of DNA methylation patterns by basespecific cleavage and mass spectrometry. Proc Natl Acad Sci USA 2005; 102: 15785-15790.
48. Oeth P, del Mistro G, Marnellos G, Shi T, van den Boom D. Qualitative and quantitative genotyping using single base primer extension coupled with matrixassisted laser desorption/ionization time-of-flight mass spectrometry (MassARRAY). Methods Mol Biol 2009; 578: 307-343.
49. Franken NA, Rodermond HM, Stap J, Haveman J, van Bree C. Clonogenic assay of cells in vitro. Nat Protoc 2006; 1: 2315-2319.