Genome-wide unmasking of epigenetically silenced genes in lung adenocarcinoma from smokers and never smokers

Carcinogenesis

Volumn 35, Issue 6, 2014, Pages 1248-1257

  Tessema, Mathewos ^a   Yingling, Christin M ^a   Liu, Yushi ^a   Tellez, Carmen S ^a   Van Neste, Leander ^b,c   Baylin, Stephen S ^d   Belinsky, Steven A ^a  

^a LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^b MDxHealth   (Belgium)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DECITABINE; SMALL INTERFERING RNA; TRICHOSTATIN A; 5 AZA 2' DEOXYCYTIDINE; AZACITIDINE; DRUG DERIVATIVE;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CPEB1 GENE; CPG ISLAND; CST6 GENE; DEACETYLATION; DISEASE COURSE; DNA METHYLATION; EMILIN2 GENE; EPIGENETICS; GENE; GENE EXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; LAYN GENE; LUNG ADENOCARCINOMA; LUNG CANCER CELL LINE; MAJOR CLINICAL STUDY; MARVELD3 GENE; NON SMALL CELL LUNG CANCER; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROMOTER REGION; SMOKING; ADENOCARCINOMA; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; LUNG TUMOR; MORTALITY; PATHOLOGY; REPRODUCIBILITY; TUMOR CELL LINE;

ADENOCARCINOMA; AZACITIDINE; CELL LINE, TUMOR; CPG ISLANDS; DISEASE PROGRESSION; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LUNG NEOPLASMS; PROMOTER REGIONS, GENETIC; REPRODUCIBILITY OF RESULTS; SMOKING;

EID: 84905370287     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgt494     Document Type: Article

References (43)

1. Jemal, A. et al. (2011) Global cancer statistics. CA. Cancer J. Clin., 61, 69-90.
2. Ferlay, J. et al. (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer, 127, 2893-2917.
3. Thun, M.J. et al. (2006) Lung cancer death rates in lifelong nonsmokers. J. Natl. Cancer Inst., 98, 691-699.
4. International Agency for Research on Cancer (2004). Tobacco smoke and involuntary smoking. In Mattock, H. (ed) IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans. Vol. 83. International Agency for Research on Cancer, Lyon, France, p. 1452.
5. U.S. Department of Health and Human Services (2006) The Health Consequences of Involuntary Exposure to Tobacco Smoke: A Report of the Surgeon General. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health, Atlanta, GA.
6. Sun, S. et al. (2007) Lung cancer in never smokers-a different disease. Nat. Rev. Cancer, 7, 778-790.
7. Pao, W. et al. (2011) New driver mutations in non-small-cell lung cancer. Lancet Oncol., 12, 175-180.
8. Thu, K.L. et al. (2012) Lung adenocarcinoma of never smokers and smokers harbor differential regions of genetic alteration and exhibit different levels of genomic instability. PLoS One, 7, e33003.
9. Toyooka, S. et al. (2006) Mutational and epigenetic evidence for independent pathways for lung adenocarcinomas arising in smokers and never smokers. Cancer Res., 66, 1371-1375.
10. Tessema, M. et al. (2009) Concomitant promoter methylation of multiple genes in lung adenocarcinomas from current, former and never smokers. Carcinogenesis, 30, 1132-1138.
11. Belinsky, S.A. et al. (2002) Aberrant promoter methylation in bronchial epithelium and sputum from current and former smokers. Cancer Res., 62, 2370-2377.
12. Ramirez, R.D. et al. (2004) Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res., 64, 9027-9034.
13. Tessema, M. et al. (2008) Promoter methylation of genes in and around the candidate lung cancer susceptibility locus 6q23-25. Cancer Res., 68, 1707-1714.
14. Tessema, M. et al. (2012) SULF2 methylation is prognostic for lung cancer survival and increases sensitivity to topoisomerase-I inhibitors via induction of ISG15. Oncogene, 31, 4107-4116.
15. Livak, K.J. et al. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25, 402-408.
16. Tessema, M. et al. (2012) Differential epigenetic regulation of TOX subfamily high mobility group box genes in lung and breast cancers. PLoS One, 7, e34850.
17. Takai, D. et al. (2002) Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc. Natl. Acad. Sci. U. S. A., 99, 3740-3745.
18. Herman, J.G. et al. (1996) Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc. Natl. Acad. Sci. U. S. A., 93, 9821-9826.
19. Kojima, T. et al. (2011) Downregulation of tight junction-associated MARVEL protein marvelD3 during epithelial-mesenchymal transition in human pancreatic cancer cells. Exp. Cell Res., 317, 2288-2298.
20. Belinsky, S.A. et al. (2007) Predicting gene promoter methylation in nonsmall-cell lung cancer by evaluating sputum and serum. Br. J. Cancer, 96, 1278-1283.
21. Belinsky, S.A. et al. (2006) Promoter hypermethylation of multiple genes in sputum precedes lung cancer incidence in a high-risk cohort. Cancer Res., 66, 3338-3344.
22. Leng, S. et al. (2012) Defining a gene promoter methylation signature in sputum for lung cancer risk assessment. Clin. Cancer Res., 18, 3387-3395.
23. Tessema, M. et al. (2010) Re-expression of CXCL14, a common target for epigenetic silencing in lung cancer, induces tumor necrosis. Oncogene, 29, 5159-5170.
24. Cameron, E.E. et al. (1999) Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat. Genet., 21, 103-107.
25. Suzuki, H. et al. (2002) A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat. Genet., 31, 141-149.
26. Mongiat, M. et al. (2007) Regulation of the extrinsic apoptotic pathway by the extracellular matrix glycoprotein EMILIN2. Mol. Cell. Biol., 27, 7176-7187.
27. Mongiat, M. et al. (2010) The extracellular matrix glycoprotein elastin microfibril interface located protein 2: a dual role in the tumor microenvironment. Neoplasia, 12, 294-304.
28. Hill, V.K. et al. (2010) Identification of 5 novel genes methylated in breast and other epithelial cancers. Mol. Cancer, 9, 51.
29. Narayan, G. et al. (2006) Promoter hypermethylation-mediated inactivation of multiple Slit-Robo pathway genes in cervical cancer progression. Mol. Cancer, 5, 16.
30. D'Ambrogio, A. et al. (2013) Translational control of cell growth and malignancy by the CPEBs. Nat. Rev. Cancer, 13, 283-290.
31. Groisman, I. et al. (2006) Control of cellular senescence by CPEB. Genes Dev., 20, 2701-2712.
32. Groppo, R. et al. (2011) CPEB control of NF-kappaB nuclear localization and interleukin-6 production mediates cellular senescence. Mol. Cell. Biol., 31, 2707-2714.
33. Burns, D.M. et al. (2008) CPEB regulation of human cellular senescence, energy metabolism, and p53 mRNA translation. Genes Dev., 22, 3449-3460.
34. Heller, G. et al. (2008) Genome-wide transcriptional response to 5-aza-2'-deoxycytidine and trichostatin a in multiple myeloma cells. Cancer Res., 68, 44-54.
35. Caldeira, J. et al. (2012) CPEB1, a novel gene silenced in gastric cancer: a Drosophila approach. Gut, 61, 1115-1123.
36. Ai, L. et al. (2006) Epigenetic silencing of the tumor suppressor cystatin M occurs during breast cancer progression. Cancer Res., 66, 7899-7909.
37. Morris, M.R. et al. (2010) Identification of candidate tumour suppressor genes frequently methylated in renal cell carcinoma. Oncogene, 29, 2104-2117.
38. Pulukuri, S.M. et al. (2009) Frequent loss of cystatin E/M expression implicated in the progression of prostate cancer. Oncogene, 28, 2829-2838.
39. Qiu, J. et al. (2008) Invasion suppressor cystatin E/M (CST6): high-level cell type-specific expression in normal brain and epigenetic silencing in gliomas. Lab. Invest., 88, 910-925.
40. Veena, M.S. et al. (2008) Inactivation of the cystatin E/M tumor suppressor gene in cervical cancer. Genes. Chromosomes Cancer, 47, 740-754.
41. Forteza, R.M. et al. (2012) Hyaluronan and layilin mediate loss of airway epithelial barrier function induced by cigarette smoke by decreasing E-cadherin. J. Biol. Chem., 287, 42288-42298.
42. Steed, E. et al. (2009) Identification of MarvelD3 as a tight junction-associated transmembrane protein of the occludin family. BMC Cell Biol., 10, 95.
43. Oyanagi, J. et al. (2012) Epithelial-mesenchymal transition stimulates human cancer cells to extend microtubule-based invasive protrusions and suppresses cell growth in collagen gel. PLoS One, 7, e53209.