Carcinogen-induced gene promoter hypermethylation is mediated by DNMT1 and causal for transformation of immortalized bronchial epithelial cells

Cancer Research

Volumn 68, Issue 21, 2008, Pages 9005-9014

  Damiani, Leah A ^a   Yingling, Christin M ^a   Leng, Shuguang ^a   Romo, Paul E ^a   Nakamura, Jun ^b   Belinsky, Steven A ^a  

^a LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^b IL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZO[A]PYRENE DERIVATIVE; BENZO[A]PYRENE DIOLEPOXIDE 1; CADHERIN; CARCINOGEN; DNA METHYLTRANSFERASE 1; METHYLNITROSOUREA; NITROBLUE TETRAZOLIUM; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BAGG ALBINO MOUSE; BRONCHUS MUCOSA; CANCER CELL CULTURE; CANCER PREVENTION; CELL TRANSFORMATION; CYTOTOXICITY; DEMETHYLATION; DNA REPAIR; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG CANCER; MALE; METHYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BLOOD LEVEL; REAL TIME POLYMERASE CHAIN REACTION; SMOKING; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING;

BRONCHI; CARCINOGENS; CELL TRANSFORMATION, NEOPLASTIC; CHROMATIN IMMUNOPRECIPITATION; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPITHELIAL CELLS; HUMANS; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 55349109940     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-1276     Document Type: Article

References (49)

1. Parkin DM. Global cancer statistics in the year 2000. Lancet Oncol 2001;9:533-43.
2. Belinsky SA. Gene-promoter hypermethylation as a biomarker in lung cancer. Nat Rev Cancer 2004;9:707-17.
3. Belinsky SA, Liechty KC, Gentry FD, et al. Promoter hypermethylation of multiple genes in sputum precedes lung cancer incidence in a high-risk cohort. Cancer Res 2006;6:3338-44.
4. 6-methylguanine-DNA methyltransferase gene: more common in lung adenocarcinomas from never-smokers than smokers and associatedwith tumor progression. Cancer Res 2003;16:4842-8.
5. Hirano T, Franzen B, Kato H, Ebihara Y, Auer G. Genesis of squamous cell lung carcinoma. Sequential changes of proliferation, DNA ploidy, and p53 expression. Am J Pathol 1994;2:296-302.
6. Okano M, Bell DW, Habe, DA, Li E. DNA methyltransferases Dnmt3a andDnmt3 b are essential for de novo methylation andmammalian development. Cell 1999;3:247-57.
7. Pradhan S, Bacolla A, Wells RD, Roberts RJ. Recombinant human DNA (cytosine-5) methyltransferase2 Expression, purification, andcomparison of de novo and maintenance methylation. J Biol Chem 1999;46:3002-10.
8. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003;21:2042-54.
9. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002;6:415-28.
10. Rhee I, Jair KW, Yen RW, et al. CpG methylation is maintained in human cancer cells lacking DNMT1. Nature 2000;6781:1003-7.
11. Esteve PO, Chin HG, Smallwood A, et al. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev 2006;22:3089-103.
12. Smallwood, A, Esteve PO, Pradhan S, Carey M. Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes Dev 2007;10:1169-78.
13. Le Gac G, Esteve PO, Ferec C, Pradhan S. DNA damage-induced down-regulation of human Cdc25C and Cdc2 is mediated by cooperation between p53 and maintenance DNA (cytosine-5) methyltransferase 1. J Biol Chem 2006;281:24161-70.
14. Mortusewicz O, Schermelleh L, Walter J, Cardoso MC, Leonhardt H. Recruitment of DNA methyltransferase I to DNA repair sites. Proc Natl Acad Sci U S A 2005;25:8905-9.
15. Belinsky SA, Nikula KJ, Baylin SB, Issa JP. Increased cytosine DNA-methyltransferase activity is target-cell-specific andan early event in lung cancer. Proc Natl Acad Sci U S A 1996;9:4045-50.
16. Robertson KD, Uzvolgyi E, Liang G, et al. The human DNA methyltransferases (DNMTs) 1, 3a and3b: coordinate mRNA expression in normal tissues and overexpression in tumors. Nucleic Acids Res 1999;11:2291-8.
17. Kim G-D, Ni J, Kelesoglu N, Roberts RJ, Pradhan S. Co-operation andcommunicatio n between the human maintenance and de novo DNA (cytosine-5)methyltransferases. EMBO J 2002;21:4183-95.
18. Rhee I, Bachman KE, Park BH, et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 2002;6880:552-6.
19. Robert MF, Morin S, Beaulieu N, et al. DNMT1 is required to maintain CpG methylation and aberrant gene silencing in human cancer cells. Nat Genet 2003;1:61-5.
20. Suzuki M, Sunaga N, Shames DS, Toyooka S, Gazdar AF, Minna JD. RNA interference-mediated knockdown of DNA methyltransferase 1 leads to promoter demethylation and gene re-expression in human lung and breast cancer cells. Cancer Res 2004;9:3137-43.
21. Reddel RR, Ke Y, Gerwin BI, et al. Transformation of human bronchial epithelial cells by infection with SV40 or adenovirus-12 SV40 hybrid or transfection via strontium phosphate coprecipitation with a plasmid containing SV40 early region genes. Cancer Res 1988;48:1904-9.
22. Ramirez RD, Sheridan S, Girard L, et al. Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res 2004;24:9027-34.
23. Lehnerdt G, Fischer M. p16(INK4a)/exon 2 mutations in squamous cell carcinoma of the head and neck region. Acta Otolaryngol 2006;4:414-7.
24. Holmila R, Husgafvel-Pursiainen K. Analysis of TP53 gene mutations in human lung cancer: comparison of capillary electrophoresis single strand conformation polymorphism assay with denaturing gradient gel electrophoresis andd irect sequencing. Cancer Detect Prev 2006;1:1-6.
25. Chastain PD, Nakamura J, Swenberg J, Kaufman D. Nonrandom AP site distribution in highly proliferative cells. FASEB J 2006;14:2612-4.
26. Fenech M. In vitro micronucleus technique to predict chemosensitivity. Methods Mol Med 2005;111:3-32.
27. van Agen B, Maas LM, Zwingmann IH, Van Schooten FJ, Kleinjans JC. B[a]P-DNA adduct formation and induction of human epithelial lung cell transformation. Environ Mol Mutagen 1997;3:287-92.
28. You M, Wang Y, Lineen A. Activation of proto-oncogenes in mouse lung tumors. Exp Lung Res 1991;17:389-400.
29. Denissenko MF, Pao A, Tang M, Pfeifer GP. Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in p53. Science 1996;274:430-2.
30. Herzog CR, Soloff EV, McDoniels AL, et al. Homozygous codeletion and differential decreased expression of p15INK4b, p16INK4a-α and p16INK4a-β in mouse lung tumor cells. Oncogene 1996;13:1885-91.
31. Agoston AT, Argani P, De Marzo AM, Hicks JL, Nelson WG. Retinoblastoma pathway dysregulation causes DNA methyltransferase 1 overexpression in cancer via MAD2-mediated inhibition of the anaphase-promoting complex. Am J Pathol 2007;5:1585-93.
32. Peyton M, Stellrecht CM, Naya FJ, Huang HP, Samora PJ, Tsai MJ. β3, a novel helix-loop-helix, can act as a negative regulator of β3 and MyoD-responsive genes. Mol Cell Biol 1996;2:626-33.
33. Suzuki M, Shigematsu H, Takahashi T, et al. Aberrant methylation of Reprimo in lung cancer. Lung Cancer 2005;3:309-14.
34. Halmos B, Basseres DS, Monti S, et al. A transcriptional profiling study of CCAAT/enhancer binding protein targets identifies hepatocyte nuclear factor 3 β as a novel tumor suppressor in lung cancer. Cancer Res 2004;12:4137-47.
35. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 2001;6824:116-20.
36. Kassis, ES, Zhao M, Hong JA, Chen A, Nguyen DM, Schrump DS. Depletion of DNA methyltransferase 1 and/or DNA methyltransferase 3b mediates growth arrest andapoptosis in lung andesophageal cancer andmalignant pleural mesothelioma cells. J Thorac Cardiovasc Surg 2006;131:298-306.
37. Belinsky SA, Grimes MJ, Casas E, et al. Predicting gene promoter methylation in lung tumors by evaluating sputum andseru m. Br J Cancer 2007;96:1278-83.
38. Sato M, Vaughan MB, Girard L, et al. multiple oncogenic changes (K-RAS(V12), p53 knockdown, mutant EGFRs, p16 bypass, telomerase) are not sufficient to confer a full malignant phenotype on human bronchial epithelial cells. Cancer Res 2006;4:2116-28.
39. Sherr CJ. Divorcing ARF andp53: an unsettled case. Nat Rev Cancer 2006;6:663-73.
40. Klein-Szanto AJ, Iizasa T, Momiki S, et al. A tobacco-specific N-nitrosamine or cigarette smoke condensate causes neoplastic transformation of xenotransplanted human bronchial epithelial cells. Proc Natl Acad Sci U S A 1992;15:6693-97.
41. Lemjabbar-Alaoui H, Dasari V, Sidhu SS, et al. Wnt and hedgehog are critical mediators of cigarette smoke-induced lung cancer. Plos One 2006;1:e93.
42. Neumann AS, Sturgis EM, Wei Q. Nucleotide excision repair as a marker for susceptibility to tobacco-related cancers: A review of molecular epidemiology studies. Mol Carcinog 2004;42:65-92.
43. Gorgoulis VG, Vassiliou LV, Karakaidos P, et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005;434:907-13.
44. Graff JR, Gabrielson E, Fujii H, Baylin SB, Herman JG. Methylation patterns of the E-cadherin 5′CpG island are unstable and reflect the dynamic, heterogenous loss of E-cadherin expression during metastatic progression. J Biol Chem 2000;275:2727-32.
45. Kikuchi S, Yamada D, Fukami T, et al. Promoter methylation of DAL-1.4.1B predicts poor prognosis in non-small cell lung cancer. Clin Cancer Res 2005;11:2954-61.
46. Russo ALL, Thiagalingam A, Pan H, et al. Differential DNA hypermethylation of critical genes mediates the stage-specific tobacco smoke-induced neoplastic progression of lung cancer. Clin Cancer Res 2005;11:2466-70.
47. Palmisano WA, Crume KP, Winters SA, et al. Aberrant promoter methylation of the transcription factor genes PAX 5 a and h in human cancers. Cancer Res 2003;63:4620-25.
48. Esteve PO, Chin HG, Pradhan S. Human maintenance DNA (cytosine-5)- methyltransferase andp53 modulate expression of p53-repressed promoters. Proc Natl Acad Sci U S A 2005;102:1000-5.
49. Cuozzo C, Porcellini A, Angrisano T, et al. DNA damage, homology-directed repair, and DNA methylation. PLoS Genet 2007;3:e110.