Establishment of a strong link between smoking and cancer pathogenesis through DNA methylation analysis

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Ma, Yunlong ^a,b   Li, Ming D ^a,b,c  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c SETON HALL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; TRANSCRIPTOME;

BIOLOGICAL MODEL; BIOLOGY; DISEASE PREDISPOSITION; DNA METHYLATION; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; GENETIC EPIGENESIS; HUMAN; METABOLISM; NEOPLASM; PROCEDURES; SIGNAL TRANSDUCTION; SMOKING;

BIOMARKERS; COMPUTATIONAL BIOLOGY; DISEASE SUSCEPTIBILITY; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; HUMANS; MODELS, BIOLOGICAL; NEOPLASMS; SIGNAL TRANSDUCTION; SMOKING; TRANSCRIPTOME;

EID: 85019259153     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-01856-4     Document Type: Article

References (67)

1. Vineis, P., et al. Tobacco and cancer: recent epidemiological evidence. Journal of the National Cancer Institute 96, 99-106, doi: 10.1093/jnci/djh014 (2004
2. CDC. Racial/Ethnic disparities and geographic differences in lung cancer incidence - 38 States and the District of Columbia, 1998-2006. MMWR Morb Mortal Wkly Rep 59, 1434-1438 (2010
3. WHO. WHO Tobacco Fact sheet No339 (http://www.who.int/mediacentre/factsheets/fs339/en/) World Health Organization (2014
4. Hecht, S. S. Tobacco carcinogens, their biomarkers and tobacco-induced cancer. Nature reviews. Cancer 3, 733-744, doi: 10.1038/nrc1190 (2003
5. Pfeifer, G. P., et al. Tobacco smoke carcinogens, DNA damage and p53 mutations in smoking-associated cancers. Oncogene 21, 7435-7451, doi: 10.1038/sj.onc.1205803 (2002
6. Grando, S. A. Connections of nicotine to cancer. Nature reviews. Cancer 14, 419-429, doi: 10.1038/nrc3725 (2014
7. Amos, C. I., et al. Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1. Nature genetics 40, 616-622, doi: 10.1038/ng.109 (2008
8. Thorgeirsson, T. E., et al. A variant associated with nicotine dependence, lung cancer and peripheral arterial disease. Nature 452, 638-642, doi: 10.1038/nature06846 (2008
9. Hung, R. J., et al. A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature 452, 633-637, doi: 10.1038/nature06885 (2008
10. Wen, L., Jiang, K., Yuan, W., Cui, W., & Li, M. D. Contribution of Variants in CHRNA5/A3/B4 Gene Cluster on Chromosome 15 to Tobacco Smoking: From Genetic Association to Mechanism. Molecular neurobiology 53, 472-484, doi: 10.1007/s12035-014-8997-x (2016
11. Bell, J. T., et al. DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biol 12, R10, doi: 10.1186/gb-2011-12-1-r10 (2011
12. Laurent, L., et al. Dynamic changes in the human methylome during differentiation. Genome research 20, 320-331, doi: 10.1101/gr.101907.109 (2010
13. Law, J. A., & Jacobsen, S. E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature reviews. Genetics 11, 204-220, doi: 10.1038/nrg2719 (2010
14. Jones, A., et al. Role of DNA methylation and epigenetic silencing of HAND2 in endometrial cancer development. PLoS medicine 10, e1001551, doi: 10.1371/journal.pmed.1001551 (2013
15. Teschendorff, A. E., et al. Epigenetic variability in cells of normal cytology is associated with the risk of future morphological transformation. Genome medicine 4, 24, doi: 10.1186/gm323 (2012
16. Sundar, I. K., Mullapudi, N., Yao, H., Spivack, S. D., & Rahman, I. Lung cancer and its association with chronic obstructive pulmonary disease: update on nexus of epigenetics. Curr Opin Pulm Med 17, 279-285, doi: 10.1097/MCP.0b013e3283477533 (2011
17. Pastrello, C., et al. Integration, visualization and analysis of human interactome. Biochemical and biophysical research communications 445, 757-773, doi: 10.1016/j.bbrc.2014.01.151 (2014
18. Maccani, J. Z., & Maccani, M. A. Altered placental DNA methylation patterns associated with maternal smoking: current perspectives. Advances in genomics and genetics 2015, 205-214, doi: 10.2147/AGG.S61518 (2015
19. Gao, X., Jia, M., Zhang, Y., Breitling, L. P., & Brenner, H. DNA methylation changes of whole blood cells in response to active smoking exposure in adults: a systematic review of DNA methylation studies. Clinical epigenetics 7, 113, doi: 10.1186/s13148-015-0148-3 (2015
20. Flom, J. D., et al. Prenatal smoke exposure and genomic DNA methylation in a multiethnic birth cohort. Cancer epidemiology, biomarkers, & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 20, 2518-2523, doi: 10.1158/1055-9965.EPI-11-0553 (2011
21. Furniss, C. S., Marsit, C. J., Houseman, E. A., Eddy, K., & Kelsey, K. T. Line region hypomethylation is associated with lifestyle and differs by human papillomavirus status in head and neck squamous cell carcinomas. Cancer epidemiology, biomarkers, & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 17, 966-971, doi: 10.1158/1055-9965.EPI-07-2775 (2008
22. Yao, H. P., Zhou, Y. Q., Zhang, R., & Wang, M. H. MSP-RON signalling in cancer: pathogenesis and therapeutic potential. Nature reviews. Cancer 13, 466-481, doi: 10.1038/nrc3545 (2013
23. Altucci, L., Leibowitz, M. D., Ogilvie, K. M., de Lera, A. R., & Gronemeyer, H. RAR and RXR modulation in cancer and metabolic disease. Nature reviews. Drug discovery 6, 793-810, doi: 10.1038/nrd2397 (2007
24. Guida, F., et al. Dynamics of smoking-induced genome-wide methylation changes with time since smoking cessation. Human molecular genetics 24, 2349-2359, doi: 10.1093/hmg/ddu751 (2015
25. Dogan, M. V., et al. The effect of smoking on DNA methylation of peripheral blood mononuclear cells from African American women. BMC genomics 15, 151, doi: 10.1186/1471-2164-15-151 (2014
26. Zeilinger, S., et al. Tobacco smoking leads to extensive genome-wide changes in DNA methylation. PloS one 8, e63812, doi: 10.1371/journal.pone.0063812 (2013
27. Zudaire, E., et al. The aryl hydrocarbon receptor repressor is a putative tumor suppressor gene in multiple human cancers. The Journal of clinical investigation 118, 640-650, doi: 10.1172/JCI30024 (2008
28. Shenker, N. S., et al. Epigenome-wide association study in the European Prospective Investigation into Cancer and Nutrition (EPICTurin) identifies novel genetic loci associated with smoking. Human molecular genetics 22, 843-851, doi: 10.1093/hmg/dds488 (2013
29. Zhang, Y., et al. F2RL3 methylation in blood DNA is a strong predictor of mortality. International journal of epidemiology 43, 1215-1225, doi: 10.1093/ije/dyu006 (2014
30. Fasanelli, F., et al. Hypomethylation of smoking-related genes is associated with future lung cancer in four prospective cohorts. Nature communications 6, 10192, doi: 10.1038/ncomms10192 (2015
31. Joehanes, R., et al. Epigenetic Signatures of Cigarette SmokingCLINICAL PERSPECTIVE. Circulation: Cardiovascular Genetics 9, 436-447, doi: 10.1161/CIRCGENETICS.116.001506 (2016
32. Guilhamon, P., et al. Meta-analysis of IDH-mutant cancers identifies EBF1 as an interaction partner for TET2. Nature communications 4, 2166, doi: 10.1038/ncomms3166 (2013
33. Novakovic, B., et al. Postnatal stability, tissue, and time specific effects of AHRR methylation change in response to maternal smoking in pregnancy. Epigenetics 9, 377-386, doi: 10.4161/epi.27248 (2014
34. Tsay, J. J., Tchou-Wong, K. M., Greenberg, A. K., Pass, H., & Rom, W. N. Aryl hydrocarbon receptor and lung cancer. Anticancer Res 33, 1247-1256 (2013
35. Szklarczyk, D., et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic acids research 43, D447-452, doi: 10.1093/nar/gku1003 (2015
36. Fiuza, U. M., & Arias, A. M. Cell and molecular biology of Notch. The Journal of endocrinology 194, 459-474, doi: 10.1677/JOE-07-0242 (2007
37. Radtke, F., & Raj, K. The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nature reviews. Cancer 3, 756-767, doi: 10.1038/nrc1186 (2003
38. Medina, P. P., & Sanchez-Cespedes, M. Involvement of the chromatin-remodeling factor BRG1/SMARCA4 in human cancer. Epigenetics: official journal of the DNA Methylation Society 3, 64-68, doi: 10.4161/epi.3.2.6153 (2008
39. Kretzmer, H., et al. DNA methylome analysis in Burkitt and follicular lymphomas identifies differentially methylated regions linked to somatic mutation and transcriptional control. Nature genetics 47, 1316-1325, doi: 10.1038/ng.3413 (2015
40. Jelinic, P., et al. Recurrent SMARCA4 mutations in small cell carcinoma of the ovary. Nature genetics 46, 424-426, doi: 10.1038/ng.2922 (2014
41. Medina, P. P., et al. Genetic and epigenetic screening for gene alterations of the chromatin-remodeling factor, SMARCA4/BRG1, in lung tumors. Genes, chromosomes, & cancer 41, 170-177, doi: 10.1002/gcc.20068 (2004
42. Britson, J., Barton, F., Balko, J. M., & Black, E. P. Deregulation of DUSP activity in EGFR-mutant lung cancer cell lines contributes to sustained ERK1/2 signaling. Biochem bioph res co 390, 849-854, doi: 10.1016/j.bbrc.2009.10.061 (2009
43. Chitale, D., et al. An integrated genomic analysis of lung cancer reveals loss of DUSP4 in EGFR-mutant tumors. Oncogene 28, 2773-2783, doi: 10.1038/onc.2009.135 (2009
44. Armes, J. E., et al. Candidate tumor-suppressor genes on chromosome arm 8p in early-onset and high-grade breast cancers. Oncogene 23, 5697-5702, doi: 10.1038/sj.onc.1207740 (2004
45. Waha, A., et al. Epigenetic downregulation of mitogen-activated protein kinase phosphatase MKP-2 relieves its growth suppressive activity in glioma cells. Cancer research 70, 1689-1699, doi: 10.1158/0008-5472.CAN-09-3218 (2010
46. Lawan, A., et al. Deletion of the dual specific phosphatase-4 (DUSP-4) gene reveals an essential non-redundant role for MAP kinase phosphatase-2 (MKP-2) in proliferation and cell survival. Journal of Biological Chemistry 286, 12933-12943, doi: 10.1074/jbc. M110.181370 (2011
47. Gröschl, B., et al. Expression of the MAP kinase phosphatase DUSP4 is associated with microsatellite instability in colorectal cancer (CRC) and causes increased cell proliferation. International Journal of Cancer 132, 1537-1546, doi: 10.1002/ijc.27834 (2013
48. Kramer, A., Green, J., Pollard, J. Jr., & Tugendreich, S. Causal analysis approaches in Ingenuity Pathway Analysis. Bioinformatics 30, 523-530, doi: 10.1093/bioinformatics/btt703 (2014
49. Glaab, E., Baudot, A., Krasnogor, N., Schneider, R., & Valencia, A. EnrichNet: network-based gene set enrichment analysis. Bioinformatics 28, i451-i457, doi: 10.1093/bioinformatics/bts389 (2012
50. Backes, C., et al. GeneTrail-advanced gene set enrichment analysis. Nucleic acids research 35, W186-192, doi: 10.1093/nar/gkm323 (2007
51. Agresti, A. A survey of exact inference for contingency tables. Statistical science 7, 131-153, doi: 10.1214/ss/1177011454 (1992
52. Benjamini, Y., & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the royal statistical society. Series B (Methodological) 289-300 (1995
53. Ogata, H., et al. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic acids research 27, 29-34, doi: 10.1093/nar/27.1.29 (1999
54. Kelder, T., et al. WikiPathways: building research communities on biological pathways. Nucleic acids research 40, D1301-1307, doi: 10.1093/nar/gkr1074 (2012
55. Nishimura, D. BioCarta. Biotech Software, & Internet Report: The Computer Software Journal for Scient 2, 117-120 (2001
56. Maere, S., Heymans, K., & Kuiper, M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21, 3448-3449, doi: 10.1093/bioinformatics/bti551 (2005
57. Berkopec, A. HyperQuick algorithm for discrete hypergeometric distribution. Journal of Discrete Algorithms 5, 341-347, doi: 10.1016/j.jda.2006.01.001 (2007
58. Supek, F., Bošnjak, M., Škunca, N., & Šmuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PloS one 6, e21800, doi: 10.1371/journal.pone.0021800 (2011
59. Shannon, P., et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome research 13, 2498-2504, doi: 10.1101/gr.1239303 (2003
60. The Cancer Genome Atlas Research Networks, Comprehensive genomic characterization of squamous cell lung cancers. Nature 489, 519-525, doi: 10.1038/nature11404 (2012
61. The Cancer Genome Atlas Research Networks, Comprehensive molecular profiling of lung adenocarcinoma. Nature 511, 543-550, doi: 10.1038/nature13385 (2014
62. Tomczak, K., Czerwinska, P., & Wiznerowicz, M. The Cancer Genome Atlas (TCGA): an immeasurable source of knowledge. Contemporary oncology 19, A68-77, doi: 10.5114/wo.2014.47136 (2015
63. Koch, A., De Meyer, T., Jeschke, J., & Van Criekinge, W. MEXPRESS: visualizing expression, DNA methylation and clinical TCGA data. BMC genomics 16, 636, doi: 10.1186/s12864-015-1847-z (2015
64. Gayen, A. The frequency distribution of the product-moment correlation coefficient in random samples of any size drawn from non-normal universes. Biometrika 38, 219-247, doi: 10.1093/biomet/38.1-2.219 (1951
65. Wilcoxon, F. Individual comparisons by ranking methods. Biometrics bulletin 1, 80-83, doi: 10.2307/3001968 (1945
66. Chen, H., & Boutros, P. C. VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC bioinformatics 12, 35, doi: 10.1186/1471-2105-12-35 (2011
67. Wickham, H. ggplot2: elegant graphics for data analysis (Springer, 2016