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Current Genomics

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ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

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Review Article

DNA Methylation Markers in Lung Cancer

Author(s): Yoonki Hong and Woo Jin Kim*

Volume 22, Issue 2, 2021

Published on: 13 October, 2020

Page: [79 - 87] Pages: 9

DOI: 10.2174/1389202921999201013164110

Price: $65

Abstract

Lung cancer is the most common cancer and the leading cause of cancer-related morbidity and mortality worldwide. As early symptoms of lung cancer are minimal and non-specific, many patients are diagnosed at an advanced stage. Despite a concerted effort to diagnose lung cancer early, no biomarkers that can be used for lung cancer screening and prognosis prediction have been established so far. As global DNA demethylation and gene-specific promoter DNA methylation are present in lung cancer, DNA methylation biomarkers have become a major area of research as potential alternative diagnostic methods to detect lung cancer at an early stage. This review summarizes the emerging DNA methylation changes in lung cancer tumorigenesis, focusing on biomarkers for early detection and their potential clinical applications in lung cancer.

Keywords: Non-small-cell lung cancer, DNA methylation, biomarker, epigenetic, tumorigenesis, hypomethylation.

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[1]
Ferlay, J.; Colombet, M.; Soerjomataram, I.; Mathers, C.; Parkin, D.M.; Piñeros, M.; Znaor, A.; Bray, F. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int. J. Cancer, 2019, 144(8), 1941-1953.
[http://dx.doi.org/10.1002/ijc.31937] [PMID: 30350310]
[2]
Khuder, S.A. Effect of cigarette smoking on major histological types of lung cancer: a meta-analysis. Lung Cancer, 2001, 31(2-3), 139-148.
[http://dx.doi.org/10.1016/S0169-5002(00)00181-1] [PMID: 11165392]
[3]
Mathers, C.; Stevens, G.; Mascarenhas, M. Global Health Risks: Mortality and Burden of Disease Attributable to Selected Major Risks; World Health Organization, 2009.
[4]
Park, E.J.; Koh, H.K.; Kwon, J.W.; Suh, M.K.; Kim, H.; Cho, S.I. Secular trends in adult male smoking from 1992 to 2006 in South Korea: age-specific changes with evolving tobacco-control policies. Public Health, 2009, 123(10), 657-664.
[http://dx.doi.org/10.1016/j.puhe.2009.09.007] [PMID: 19892378]
[5]
Park, J.Y.; Jang, S.H. Epidemiology of lung cancer in Korea: recent trends. Tuberc. Respir. Dis. (Seoul), 2016, 79(2), 58-69.
[http://dx.doi.org/10.4046/trd.2016.79.2.58] [PMID: 27064578]
[6]
Kim, H.C.; Jung, C.Y.; Cho, D.G.; Jeon, J.H.; Lee, J.E.; Ahn, J.S.; Kim, S.J.; Kim, Y.; Kim, Y.C.; Kim, J.E.; Lee, B.; Won, Y.J.; Choi, C.M. Clinical characteristics and prognostic factors of lung cancer in Korea: A pilot study of data from the Korean nationwide lung cancer registry. Tuberc. Respir. Dis. (Seoul), 2019, 82(2), 118-125.
[http://dx.doi.org/10.4046/trd.2017.0128] [PMID: 29926550]
[7]
Gettinger, S.; Horn, L.; Jackman, D.; Spigel, D.; Antonia, S.; Hellmann, M.; Powderly, J.; Heist, R.; Sequist, L.V.; Smith, D.C.; Leming, P.; Geese, W.J.; Yoon, D.; Li, A.; Brahmer, J. Five-year follow-up of nivolumab in previously treated advanced non-small-cell lung cancer: results from the CA209-003 study. J. Clin. Oncol., 2018, 36(17), 1675-1684.
[http://dx.doi.org/10.1200/JCO.2017.77.0412] [PMID: 29570421]
[8]
Oken, M.M.; Hocking, W.G.; Kvale, P.A.; Andriole, G.L.; Buys, S.S.; Church, T.R.; Crawford, E.D.; Fouad, M.N.; Isaacs, C.; Reding, D.J.; Weissfeld, J.L.; Yokochi, L.A.; O’Brien, B.; Ragard, L.R.; Rathmell, J.M.; Riley, T.L.; Wright, P.; Caparaso, N.; Hu, P.; Izmirlian, G.; Pinsky, P.F.; Prorok, P.C.; Kramer, B.S.; Miller, A.B.; Gohagan, J.K.; Berg, C.D. PLCO Project Team. Screening by chest radiograph and lung cancer mortality: the Prostate, Lung, Colorectal, and Ovarian (PLCO) randomized trial. JAMA, 2011, 306(17), 1865-1873.
[http://dx.doi.org/10.1001/jama.2011.1591] [PMID: 22031728]
[9]
Aberle, D.R.; Adams, A.M.; Berg, C.D.; Black, W.C.; Clapp, J.D.; Fagerstrom, R.M.; Gareen, I.F.; Gatsonis, C.; Marcus, P.M.; Sicks, J.D. Reduced lung-cancer mortality with low-dose computed tomographic screening. N. Engl. J. Med., 2011, 365(5), 395-409.
[PMID: 21714641]
[10]
Huo, J.; Shen, C.; Volk, R.J.; Shih, Y.T. Use of CT and chest radiography for lung cancer screening before and after publication of screening guidelines: intended and unintended uptake. JAMA Intern. Med., 2017, 177(3), 439-441.
[http://dx.doi.org/10.1001/jamainternmed.2016.9016] [PMID: 28135349]
[11]
Mazzone, P.J.; Silvestri, G.A.; Patel, S.; Kanne, J.P.; Kinsinger, L.S.; Wiener, R.S.; Soo Hoo, G.; Detterbeck, F.C. Screening for lung cancer. CHEST Guideline and Expert Panel Report. Chest, 2018, 153(4), 954-985.
[http://dx.doi.org/10.1016/j.chest.2018.01.016] [PMID: 29374513]
[12]
van der Aalst, C.M.; Ten Haaf, K.; de Koning, H.J. Lung cancer screening: latest developments and unanswered questions. Lancet Respir. Med., 2016, 4(9), 749-761.
[http://dx.doi.org/10.1016/S2213-2600(16)30200-4] [PMID: 27599248]
[13]
Tsou, J.A.; Hagen, J.A.; Carpenter, C.L.; Laird-Offringa, I.A. DNA methylation analysis: a powerful new tool for lung cancer diagnosis. Oncogene, 2002, 21(35), 5450-5461.
[http://dx.doi.org/10.1038/sj.onc.1205605] [PMID: 12154407]
[14]
Balgkouranidou, I.; Liloglou, T.; Lianidou, E.S. Lung cancer epigenetics: emerging biomarkers. Biomarkers Med., 2013, 7(1), 49-58.
[http://dx.doi.org/10.2217/bmm.12.111] [PMID: 23387484]
[15]
Mehta, A.; Dobersch, S.; Romero-Olmedo, A.J.; Barreto, G. Epigenetics in lung cancer diagnosis and therapy. Cancer Metastasis Rev., 2015, 34(2), 229-241.
[http://dx.doi.org/10.1007/s10555-015-9563-3] [PMID: 25939322]
[16]
Nikolaidis, G.; Raji, O.Y.; Markopoulou, S.; Gosney, J.R.; Bryan, J.; Warburton, C.; Walshaw, M.; Sheard, J.; Field, J.K.; Liloglou, T. DNA methylation biomarkers offer improved diagnostic efficiency in lung cancer. Cancer Res., 2012, 72(22), 5692-5701.
[http://dx.doi.org/10.1158/0008-5472.CAN-12-2309] [PMID: 22962272]
[17]
Robertson, K.D. DNA methylation and human disease. Nat. Rev. Genet., 2005, 6(8), 597-610.
[http://dx.doi.org/10.1038/nrg1655] [PMID: 16136652]
[18]
Feinberg, A.P.; Tycko, B. The history of cancer epigenetics. Nat. Rev. Cancer, 2004, 4(2), 143-153.
[http://dx.doi.org/10.1038/nrc1279] [PMID: 14732866]
[19]
Esteller, M.; Silva, J.M.; Dominguez, G.; Bonilla, F.; Matias-Guiu, X.; Lerma, E.; Bussaglia, E.; Prat, J.; Harkes, I.C.; Repasky, E.A.; Gabrielson, E.; Schutte, M.; Baylin, S.B.; Herman, J.G. Promoter hypermethylation and BRCA1 inactivation in sporadic breast and ovarian tumors. J. Natl. Cancer Inst., 2000, 92(7), 564-569.
[http://dx.doi.org/10.1093/jnci/92.7.564] [PMID: 10749912]
[20]
Ansari, J.; Shackelford, R.E.; El-Osta, H. Epigenetics in non-small cell lung cancer: from basics to therapeutics. Transl. Lung Cancer Res., 2016, 5(2), 155-171.
[http://dx.doi.org/10.21037/tlcr.2016.02.02] [PMID: 27186511]
[21]
Heinäniemi, M.; Nykter, M.; Kramer, R.; Wienecke-Baldacchino, A.; Sinkkonen, L.; Zhou, J.X.; Kreisberg, R.; Kauffman, S.A.; Huang, S.; Shmulevich, I. Gene-pair expression signatures reveal lineage control. Nat. Methods, 2013, 10(6), 577-583.
[http://dx.doi.org/10.1038/nmeth.2445] [PMID: 23603899]
[22]
Feinberg, A.P.; Ohlsson, R.; Henikoff, S. The epigenetic progenitor origin of human cancer. Nat. Rev. Genet., 2006, 7(1), 21-33.
[http://dx.doi.org/10.1038/nrg1748] [PMID: 16369569]
[23]
Baylin, S.B.; Ohm, J.E. Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nat. Rev. Cancer, 2006, 6(2), 107-116.
[http://dx.doi.org/10.1038/nrc1799] [PMID: 16491070]
[24]
Teschendorff, A.E.; Zheng, S.C.; Feber, A.; Yang, Z.; Beck, S.; Widschwendter, M. The multi-omic landscape of transcription factor inactivation in cancer. Genome Med., 2016, 8(1), 89.
[http://dx.doi.org/10.1186/s13073-016-0342-8] [PMID: 27562343]
[25]
Vogelstein, B.; Papadopoulos, N.; Velculescu, V.E.; Zhou, S.; Diaz, L.A., Jr; Kinzler, K.W. Cancer genome landscapes. Science, 2013, 339(6127), 1546-1558.
[http://dx.doi.org/10.1126/science.1235122] [PMID: 23539594]
[26]
Jones, A.; Teschendorff, A.E.; Li, Q.; Hayward, J.D.; Kannan, A.; Mould, T.; West, J.; Zikan, M.; Cibula, D.; Fiegl, H.; Lee, S.H.; Wik, E.; Hadwin, R.; Arora, R.; Lemech, C.; Turunen, H.; Pakarinen, P.; Jacobs, I.J.; Salvesen, H.B.; Bagchi, M.K.; Bagchi, I.C.; Widschwendter, M. Role of DNA methylation and epigenetic silencing of HAND2 in endometrial cancer development. PLoS Med., 2013, 10(11)e1001551
[http://dx.doi.org/10.1371/journal.pmed.1001551] [PMID: 24265601]
[27]
Belinsky, S.A.; Nikula, K.J.; Palmisano, W.A.; Michels, R.; Saccomanno, G.; Gabrielson, E.; Baylin, S.B.; Herman, J.G. 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(20), 11891-11896.
[http://dx.doi.org/10.1073/pnas.95.20.11891] [PMID: 9751761]
[28]
Ahrendt, S.A.; Chow, J.T.; Xu, L.H.; Yang, S.C.; Eisenberger, C.F.; Esteller, M.; Herman, J.G.; Wu, L.; Decker, P.A.; Jen, J.; Sidransky, D. Molecular detection of tumor cells in bronchoalveolar lavage fluid from patients with early stage lung cancer. J. Natl. Cancer Inst., 1999, 91(4), 332-339.
[http://dx.doi.org/10.1093/jnci/91.4.332] [PMID: 10050866]
[29]
Tsou, J.A.; Galler, J.S.; Siegmund, K.D.; Laird, P.W.; Turla, S.; Cozen, W.; Hagen, J.A.; Koss, M.N.; Laird-Offringa, I.A. Identification of a panel of sensitive and specific DNA methylation markers for lung adenocarcinoma. Mol. Cancer, 2007, 6, 70.
[http://dx.doi.org/10.1186/1476-4598-6-70] [PMID: 17967182]
[30]
Geng, J.; Sun, J.; Lin, Q.; Gu, J.; Zhao, Y.; Zhang, H.; Feng, X.; He, Y.; Wang, W.; Zhou, X.; Yu, J. Methylation status of NEUROG2 and NID2 improves the diagnosis of stage I NSCLC. Oncol. Lett., 2012, 3(4), 901-906.
[PMID: 22741015]
[31]
Topaloglu, O.; Hoque, M.O.; Tokumaru, Y.; Lee, J.; Ratovitski, E.; Sidransky, D.; Moon, C.S. Detection of promoter hypermethylation of multiple genes in the tumor and bronchoalveolar lavage of patients with lung cancer. Clin. Cancer Res., 2004, 10(7), 2284-2288.
[http://dx.doi.org/10.1158/1078-0432.CCR-1111-3] [PMID: 15073103]
[32]
Schmiemann, V.; Böcking, A.; Kazimirek, M.; Onofre, A.S.; Gabbert, H.E.; Kappes, R.; Gerharz, C.D.; Grote, H.J. Methylation assay for the diagnosis of lung cancer on bronchial aspirates: a cohort study. Clin. Cancer Res., 2005, 11(21), 7728-7734.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-0999] [PMID: 16278393]
[33]
Grote, H.J.; Schmiemann, V.; Geddert, H.; Bocking, A.; Kappes, R.; Gabbert, H.E.; Sarbia, M. Methylation of RAS association domain family protein 1A as a biomarker of lung cancer. Cancer, 2006, 108(2), 129-134.
[http://dx.doi.org/10.1002/cncr.21717] [PMID: 16444703]
[34]
van der Drift, M.A.; Prinsen, C.F.M.; Knuiman, G.J.; Janssen, J.P.; Dekhuijzen, P.N.R.; Thunnissen, F.B.J.M. Diagnosing peripheral lung cancer: the additional value of the Ras-association domain family 1A gene methylation and Kirsten rat sarcoma 2 viral oncogene homolog mutation analyses in washings in nondiagnostic bronchoscopy. Chest, 2012, 141(1), 169-175.
[http://dx.doi.org/10.1378/chest.10-2579] [PMID: 21700687]
[35]
Schmidt, B.; Liebenberg, V.; Dietrich, D.; Schlegel, T.; Kneip, C.; Seegebarth, A.; Flemming, N.; Seemann, S.; Distler, J.; Lewin, J.; Tetzner, R.; Weickmann, S.; Wille, U.; Liloglou, T.; Raji, O.; Walshaw, M.; Fleischhacker, M.; Witt, C.; Field, J.K. SHOX2 DNA methylation is a biomarker for the diagnosis of lung cancer based on bronchial aspirates. BMC Cancer, 2010, 10, 600.
[http://dx.doi.org/10.1186/1471-2407-10-600] [PMID: 21047392]
[36]
Hubers, A.J.; Brinkman, P.; Boksem, R.J.; Rhodius, R.J.; Witte, B.I.; Zwinderman, A.H.; Heideman, D.A.; Duin, S.; Koning, R.; Steenbergen, R.D.; Snijders, P.J.; Smit, E.F.; Sterk, P.J.; Thunnissen, E. Combined sputum hypermethylation and eNose analysis for lung cancer diagnosis. J. Clin. Pathol., 2014, 67(8), 707-711.
[http://dx.doi.org/10.1136/jclinpath-2014-202414] [PMID: 24915850]
[37]
Leng, S.; Do, K.; Yingling, C.M.; Picchi, M.A.; Wolf, H.J.; Kennedy, T.C.; Feser, W.J.; Baron, A.E.; Franklin, W.A.; Brock, M.V.; Herman, J.G.; Baylin, S.B.; Byers, T.; Stidley, C.A.; Belinsky, S.A. Defining a gene promoter methylation signature in sputum for lung cancer risk assessment. Clin. Cancer Res., 2012, 18(12), 3387-3395.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-3049] [PMID: 22510351]
[38]
Wang, Y.C.; Lu, Y.P.; Tseng, R.C.; Lin, R.K.; Chang, J.W.; Chen, J.T.; Shih, C.M.; Chen, C.Y. Inactivation of hMLH1 and hMSH2 by promoter methylation in primary non-small cell lung tumors and matched sputum samples. J. Clin. Invest., 2003, 111(6), 887-895.
[http://dx.doi.org/10.1172/JCI15475] [PMID: 12639995]
[39]
Destro, A.; Bianchi, P.; Alloisio, M.; Laghi, L.; Di Gioia, S.; Malesci, A.; Cariboni, U.; Gribaudi, G.; Bulfamante, G.; Marchetti, A.; Bosari, S.; Infante, M.; Ravasi, G.; Roncalli, M. K-ras and p16(INK4A)alterations in sputum of NSCLC patients and in heavy asymptomatic chronic smokers. Lung Cancer, 2004, 44(1), 23-32.
[http://dx.doi.org/10.1016/j.lungcan.2003.10.002] [PMID: 15013580]
[40]
Belinsky, S.A.; Grimes, M.J.; Casas, E.; Stidley, C.A.; Franklin, W.A.; Bocklage, T.J.; Johnson, D.H.; Schiller, J.H. Predicting gene promoter methylation in non-small-cell lung cancer by evaluating sputum and serum. Br. J. Cancer, 2007, 96(8), 1278-1283.
[http://dx.doi.org/10.1038/sj.bjc.6603721] [PMID: 17406356]
[41]
Cirincione, R.; Lintas, C.; Conte, D.; Mariani, L.; Roz, L.; Vignola, A.M.; Pastorino, U.; Sozzi, G. Methylation profile in tumor and sputum samples of lung cancer patients detected by spiral computed tomography: a nested case-control study. Int. J. Cancer, 2006, 118(5), 1248-1253.
[http://dx.doi.org/10.1002/ijc.21473] [PMID: 16152615]
[42]
Fujii, M.; Fujimoto, N.; Hiraki, A.; Gemba, K.; Aoe, K.; Umemura, S.; Katayama, H.; Takigawa, N.; Kiura, K.; Tanimoto, M.; Kishimoto, T. Aberrant DNA methylation profile in pleural fluid for differential diagnosis of malignant pleural mesothelioma. Cancer Sci., 2012, 103(3), 510-514.
[http://dx.doi.org/10.1111/j.1349-7006.2011.02180.x] [PMID: 22146010]
[43]
Brock, M.V.; Hooker, C.M.; Ota-Machida, E.; Han, Y.; Guo, M.; Ames, S.; Glöckner, S.; Piantadosi, S.; Gabrielson, E.; Pridham, G.; Pelosky, K.; Belinsky, S.A.; Yang, S.C.; Baylin, S.B.; Herman, J.G. DNA methylation markers and early recurrence in stage I lung cancer. N. Engl. J. Med., 2008, 358(11), 1118-1128.
[http://dx.doi.org/10.1056/NEJMoa0706550] [PMID: 18337602]
[44]
Yamamoto, H.; Toyooka, S.; Mitsudomi, T. Impact of EGFR mutation analysis in non-small cell lung cancer. Lung Cancer, 2009, 63(3), 315-321.
[http://dx.doi.org/10.1016/j.lungcan.2008.06.021] [PMID: 18760859]
[45]
Zhang, Y.; Wang, R.; Song, H.; Huang, G.; Yi, J.; Zheng, Y.; Wang, J.; Chen, L. Methylation of multiple genes as a candidate biomarker in non-small cell lung cancer. Cancer Lett., 2011, 303(1), 21-28.
[http://dx.doi.org/10.1016/j.canlet.2010.12.011] [PMID: 21255913]
[46]
Yang, J.; Shen, Y.; Liu, B.; Tong, Y. Promoter methylation of BRMS1 correlates with smoking history and poor survival in non-small cell lung cancer patients. Lung Cancer, 2011, 74(2), 305-309.
[http://dx.doi.org/10.1016/j.lungcan.2011.03.002] [PMID: 21726917]
[47]
Dietrich, D.; Hasinger, O.; Liebenberg, V.; Field, J.K.; Kristiansen, G.; Soltermann, A. DNA methylation of the homeobox genes PITX2 and SHOX2 predicts outcome in non-small-cell lung cancer patients. Diagn. Mol. Pathol., 2012, 21(2), 93-104.
[http://dx.doi.org/10.1097/PDM.0b013e318240503b] [PMID: 22555092]
[48]
Lokk, K.; Vooder, T.; Kolde, R.; Välk, K.; Võsa, U.; Roosipuu, R.; Milani, L.; Fischer, K.; Koltsina, M.; Urgard, E.; Annilo, T.; Metspalu, A.; Tõnisson, N. Methylation markers of early-stage non-small cell lung cancer. PLoS One, 2012, 7(6)e39813
[http://dx.doi.org/10.1371/journal.pone.0039813] [PMID: 22768131]
[49]
Levenson, V.V. DNA methylation as a universal biomarker. Expert Rev. Mol. Diagn., 2010, 10(4), 481-488.
[http://dx.doi.org/10.1586/erm.10.17]
[50]
Hsu, H.S.; Chen, T.P.; Hung, C.H.; Wen, C.K.; Lin, R.K.; Lee, H.C.; Wang, Y.C. Characterization of a multiple epigenetic marker panel for lung cancer detection and risk assessment in plasma. Cancer, 2007, 110(9), 2019-2026.
[http://dx.doi.org/10.1002/cncr.23001] [PMID: 17876837]
[51]
Russo, A.L.; Thiagalingam, A.; Pan, H.; Califano, J.; Cheng, K.H.; Ponte, J.F.; Chinnappan, D.; Nemani, P.; Sidransky, D.; Thiagalingam, S. Differential DNA hypermethylation of critical genes mediates the stage-specific tobacco smoke-induced neoplastic progression of lung cancer. Clin. Cancer Res., 2005, 11(7), 2466-2470.
[http://dx.doi.org/10.1158/1078-0432.CCR-04-1962] [PMID: 15814621]
[52]
Kneip, C.; Schmidt, B.; Seegebarth, A.; Weickmann, S.; Fleischhacker, M.; Liebenberg, V.; Field, J.K.; Dietrich, D. SHOX2 DNA methylation is a biomarker for the diagnosis of lung cancer in plasma. J. Thorac. Oncol., 2011, 6(10), 1632-1638.
[http://dx.doi.org/10.1097/JTO.0b013e318220ef9a] [PMID: 21694641]
[53]
Tuo, L.; Sha, S.; Huayu, Z.; Du, K. P16INK4a gene promoter methylation as a biomarker for the diagnosis of non-small cell lung cancer: An updated meta-analysis. Thorac. Cancer, 2018, 9(8), 1032-1040.
[http://dx.doi.org/10.1111/1759-7714.12783] [PMID: 29927090]
[54]
Liu, Y.; An, Q.; Li, L.; Zhang, D.; Huang, J.; Feng, X.; Cheng, S.; Gao, Y. Hypermethylation of p16INK4a in Chinese lung cancer patients: biological and clinical implications. Carcinogenesis, 2003, 24(12), 1897-1901.
[http://dx.doi.org/10.1093/carcin/bgg169] [PMID: 12970072]
[55]
Bearzatto, A.; Conte, D.; Frattini, M.; Zaffaroni, N.; Andriani, F.; Balestra, D.; Tavecchio, L.; Daidone, M.G.; Sozzi, G. p16(INK4A) Hypermethylation detected by fluorescent methylation-specific PCR in plasmas from non-small cell lung cancer. Clin. Cancer Res., 2002, 8(12), 3782-3787.
[PMID: 12473590]
[56]
Suga, Y.; Miyajima, K.; Oikawa, T.; Maeda, J.; Usuda, J.; Kajiwara, N.; Ohira, T.; Uchida, O.; Tsuboi, M.; Hirano, T.; Kato, H.; Ikeda, N. Quantitative p16 and ESR1 methylation in the peripheral blood of patients with non-small cell lung cancer. Oncol. Rep., 2008, 20(5), 1137-1142.
[PMID: 18949413]
[57]
Schwarzenbach, H.; Hoon, D.S.B.; Pantel, K. Cell-free nucleic acids as biomarkers in cancer patients. Nat. Rev. Cancer, 2011, 11(6), 426-437.
[http://dx.doi.org/10.1038/nrc3066] [PMID: 21562580]
[58]
Bremnes, R.M.; Sirera, R.; Camps, C. Circulating tumour-derived DNA and RNA markers in blood: a tool for early detection, diagnostics, and follow-up? Lung Cancer, 2005, 49(1), 1-12.
[http://dx.doi.org/10.1016/j.lungcan.2004.12.008] [PMID: 15949585]
[59]
Salvi, S.; Gurioli, G.; De Giorgi, U.; Conteduca, V.; Tedaldi, G.; Calistri, D.; Casadio, V. Cell-free DNA as a diagnostic marker for cancer: current insights. OncoTargets Ther., 2016, 9, 6549-6559.
[http://dx.doi.org/10.2147/OTT.S100901] [PMID: 27822059]
[60]
Wielscher, M.; Vierlinger, K.; Kegler, U.; Ziesche, R.; Gsur, A.; Weinhäusel, A. Diagnostic performance of plasma DNA methylation profiles in lung cancer, pulmonary fibrosis and COPD. EBioMedicine, 2015, 2(8), 929-936.
[http://dx.doi.org/10.1016/j.ebiom.2015.06.025] [PMID: 26425700]
[61]
Cancer Genome Atlas Research Network. Comprehensive genomic characterization of squamous cell lung cancers. Nature, 2012, 489(7417), 519-525.
[http://dx.doi.org/10.1038/nature11404] [PMID: 22960745]
[62]
Ooki, A.; Maleki, Z.; Tsay, J.J.; Goparaju, C.; Brait, M.; Turaga, N.; Nam, H.S.; Rom, W.N.; Pass, H.I.; Sidransky, D.; Guerrero-Preston, R.; Hoque, M.O. A panel of novel detection and prognostic methylated DNA markers in primary non-small cell lung cancer and serum DNA. Clin. Cancer Res., 2017, 23(22), 7141-7152.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-1222] [PMID: 28855354]
[63]
Hulbert, A.; Jusue-Torres, I.; Stark, A.; Chen, C.; Rodgers, K.; Lee, B.; Griffin, C.; Yang, A.; Huang, P.; Wrangle, J.; Belinsky, S.A.; Wang, T.H.; Yang, S.C.; Baylin, S.B.; Brock, M.V.; Herman, J.G. Early detection of lung cancer using DNA promoter hypermethylation in plasma and sputum. Clin. Cancer Res., 2017, 23(8), 1998-2005.
[http://dx.doi.org/10.1158/1078-0432.CCR-16-1371] [PMID: 27729459]
[64]
Xu, W.; Lu, J.; Zhao, Q.; Wu, J.; Sun, J.; Han, B.; Zhao, X.; Kang, Y. Genome-wide plasma cell-free DNA methylation profiling identifies potential biomarkers for lung cancer. Dis. Markers, 2019, 20194108474
[http://dx.doi.org/10.1155/2019/4108474] [PMID: 30867848]
[65]
Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: the next generation. Cell, 2011, 144(5), 646-674.
[http://dx.doi.org/10.1016/j.cell.2011.02.013] [PMID: 21376230]
[66]
Teschendorff, A.E.; Yang, Z.; Wong, A.; Pipinikas, C.P.; Jiao, Y.; Jones, A.; Anjum, S.; Hardy, R.; Salvesen, H.B.; Thirlwell, C.; Janes, S.M.; Kuh, D.; Widschwendter, M. Correlation of smoking-associated DNA methylation changes in buccal cells with DNA methylation changes in epithelial cancer. JAMA Oncol., 2015, 1(4), 476-485.
[http://dx.doi.org/10.1001/jamaoncol.2015.1053] [PMID: 26181258]
[67]
Stirzaker, C.; Taberlay, P.C.; Statham, A.L.; Clark, S.J. Mining cancer methylomes: prospects and challenges. Trends Genet., 2014, 30(2), 75-84.
[http://dx.doi.org/10.1016/j.tig.2013.11.004] [PMID: 24368016]
[68]
Bibikova, M.; Le, J.; Barnes, B.; Saedinia-Melnyk, S.; Zhou, L.; Shen, R.; Gunderson, K.L. Genome-wide DNA methylation profiling using Infinium® assay. Epigenomics, 2009, 1(1), 177-200.
[http://dx.doi.org/10.2217/epi.09.14] [PMID: 22122642]
[69]
Hinoue, T.; Weisenberger, D.J.; Lange, C.P.; Shen, H.; Byun, H.M.; Van Den Berg, D.; Malik, S.; Pan, F.; Noushmehr, H.; van Dijk, C.M.; Tollenaar, R.A.; Laird, P.W. Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res., 2012, 22(2), 271-282.
[http://dx.doi.org/10.1101/gr.117523.110] [PMID: 21659424]
[70]
Breitling, L.P.; Yang, R.; Korn, B.; Burwinkel, B.; Brenner, H. Tobacco-smoking-related differential DNA methylation: 27K discovery and replication. Am. J. Hum. Genet., 2011, 88(4), 450-457.
[http://dx.doi.org/10.1016/j.ajhg.2011.03.003] [PMID: 21457905]
[71]
Rakyan, V.K.; Down, T.A.; Maslau, S.; Andrew, T.; Yang, T.P.; Beyan, H.; Whittaker, P.; McCann, O.T.; Finer, S.; Valdes, A.M.; Leslie, R.D.; Deloukas, P.; Spector, T.D. Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res., 2010, 20(4), 434-439.
[http://dx.doi.org/10.1101/gr.103101.109] [PMID: 20219945]
[72]
Maegawa, S.; Hinkal, G.; Kim, H.S.; Shen, L.; Zhang, L.; Zhang, J.; Zhang, N.; Liang, S.; Donehower, L.A.; Issa, J.P. Widespread and tissue specific age-related DNA methylation changes in mice. Genome Res., 2010, 20(3), 332-340.
[http://dx.doi.org/10.1101/gr.096826.109] [PMID: 20107151]
[73]
Teschendorff, A.E.; Menon, U.; Gentry-Maharaj, A.; Ramus, S.J.; Weisenberger, D.J.; Shen, H.; Campan, M.; Noushmehr, H.; Bell, C.G.; Maxwell, A.P.; Savage, D.A.; Mueller-Holzner, E.; Marth, C.; Kocjan, G.; Gayther, S.A.; Jones, A.; Beck, S.; Wagner, W.; Laird, P.W.; Jacobs, I.J.; Widschwendter, M. Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res., 2010, 20(4), 440-446.
[http://dx.doi.org/10.1101/gr.103606.109] [PMID: 20219944]
[74]
Christensen, B.C.; Houseman, E.A.; Marsit, C.J.; Zheng, S.; Wrensch, M.R.; Wiemels, J.L.; Nelson, H.H.; Karagas, M.R.; Padbury, J.F.; Bueno, R.; Sugarbaker, D.J.; Yeh, R.F.; Wiencke, J.K.; Kelsey, K.T. Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet., 2009, 5(8)e1000602
[http://dx.doi.org/10.1371/journal.pgen.1000602] [PMID: 19680444]
[75]
Shiah, Y.J.; Fraser, M.; Bristow, R.G.; Boutros, P.C. Comparison of pre-processing methods for Infinium HumanMethylation450 BeadChip array. Bioinformatics, 2017, 33(20), 3151-3157.
[http://dx.doi.org/10.1093/bioinformatics/btx372] [PMID: 28605401]
[76]
Pidsley, R.; Zotenko, E.; Peters, T.J.; Lawrence, M.G.; Risbridger, G.P.; Molloy, P.; Van Djik, S.; Muhlhausler, B.; Stirzaker, C.; Clark, S.J. Critical evaluation of the Illumina MethylationEPIC BeadChip microarray for whole-genome DNA methylation profiling. Genome Biol., 2016, 17(1), 208.
[http://dx.doi.org/10.1186/s13059-016-1066-1] [PMID: 27717381]
[77]
Moon, D.H.; Kwon, S.O.; Kim, W.J.; Hong, Y. Identification of serial DNA methylation changes in the blood samples of patients with lung cancer. Tuberc. Respir. Dis. (Seoul), 2019, 82(2), 126-132.
[http://dx.doi.org/10.4046/trd.2018.0042] [PMID: 30302959]
[78]
Palmisano, W.A.; Divine, K.K.; Saccomanno, G.; Gilliland, F.D.; Baylin, S.B.; Herman, J.G.; Belinsky, S.A. Predicting lung cancer by detecting aberrant promoter methylation in sputum. Cancer Res., 2000, 60(21), 5954-5958.
[PMID: 11085511]
[79]
Dogan, M.V.; Shields, B.; Cutrona, C.; Gao, L.; Gibbons, F.X.; Simons, R.; Monick, M.; Brody, G.H.; Tan, K.; Beach, S.R.; Philibert, R.A. The effect of smoking on DNA methylation of peripheral blood mononuclear cells from African American women. BMC Genomics, 2014, 15, 151.
[http://dx.doi.org/10.1186/1471-2164-15-151] [PMID: 24559495]
[80]
Tsaprouni, L.G.; Yang, T.P.; Bell, J.; Dick, K.J.; Kanoni, S.; Nisbet, J.; Viñuela, A.; Grundberg, E.; Nelson, C.P.; Meduri, E.; Buil, A.; Cambien, F.; Hengstenberg, C.; Erdmann, J.; Schunkert, H.; Goodall, A.H.; Ouwehand, W.H.; Dermitzakis, E.; Spector, T.D.; Samani, N.J.; Deloukas, P. Cigarette smoking reduces DNA methylation levels at multiple genomic loci but the effect is partially reversible upon cessation. Epigenetics, 2014, 9(10), 1382-1396.
[http://dx.doi.org/10.4161/15592294.2014.969637] [PMID: 25424692]
[81]
Zaghlool, S.B.; Al-Shafai, M.; Al Muftah, W.A.; Kumar, P.; Falchi, M.; Suhre, K. Association of DNA methylation with age, gender, and smoking in an Arab population. Clin. Epigenetics, 2015, 7, 6.
[http://dx.doi.org/10.1186/s13148-014-0040-6] [PMID: 25663950]
[82]
Guida, F.; Sandanger, T.M.; Castagné, R.; Campanella, G.; Polidoro, S.; Palli, D.; Krogh, V.; Tumino, R.; Sacerdote, C.; Panico, S.; Severi, G.; Kyrtopoulos, S.A.; Georgiadis, P.; Vermeulen, R.C.; Lund, E.; Vineis, P.; Chadeau-Hyam, M. Dynamics of smoking-induced genome-wide methylation changes with time since smoking cessation. Hum. Mol. Genet., 2015, 24(8), 2349-2359.
[http://dx.doi.org/10.1093/hmg/ddu751] [PMID: 25556184]
[83]
Riboli, E.; Kaaks, R. The EPIC Project: rationale and study design. European Prospective Investigation into Cancer and Nutrition. Int. J. Epidemiol., 1997, 26(Suppl. 1), S6-S14.
[http://dx.doi.org/10.1093/ije/26.suppl_1.S6] [PMID: 9126529]
[84]
Giles, G.G.; English, D.R. The Melbourne Collaborative. The Melbourne Collaborative Cohort Study. In: IARC Sci. Publ; , 2002; 156, pp. 69-70.
[PMID: 12484128]
[85]
Fasanelli, F.; Baglietto, L.; Ponzi, E.; Guida, F.; Campanella, G.; Johansson, M.; Grankvist, K.; Johansson, M.; Assumma, M.B.; Naccarati, A.; Chadeau-Hyam, M.; Ala, U.; Faltus, C.; Kaaks, R.; Risch, A.; De Stavola, B.; Hodge, A.; Giles, G.G.; Southey, M.C.; Relton, C.L.; Haycock, P.C.; Lund, E.; Polidoro, S.; Sandanger, T.M.; Severi, G.; Vineis, P. Hypomethylation of smoking-related genes is associated with future lung cancer in four prospective cohorts. Nat. Commun., 2015, 6, 10192.
[http://dx.doi.org/10.1038/ncomms10192] [PMID: 26667048]
[86]
Hallmans, G.; Agren, A.; Johansson, G.; Johansson, A.; Stegmayr, B.; Jansson, J.H.; Lindahl, B.; Rolandsson, O.; Söderberg, S.; Nilsson, M.; Johansson, I.; Weinehall, L. Cardiovascular disease and diabetes in the Northern Sweden Health and Disease Study Cohort - evaluation of risk factors and their interactions. Scand. J. Public Health Suppl., 2003, 61, 18-24.
[http://dx.doi.org/10.1080/14034950310001432] [PMID: 14660243]
[87]
Zhang, Y.; Yang, R.; Burwinkel, B.; Breitling, L.P.; Holleczek, B.; Schöttker, B.; Brenner, H. F2RL3 methylation in blood DNA is a strong predictor of mortality. Int. J. Epidemiol., 2014, 43(4), 1215-1225.
[http://dx.doi.org/10.1093/ije/dyu006] [PMID: 24510982]
[88]
Zhang, Y.; Schöttker, B.; Ordóñez-Mena, J.; Holleczek, B.; Yang, R.; Burwinkel, B.; Butterbach, K.; Brenner, H. F2RL3 methylation, lung cancer incidence and mortality. Int. J. Cancer, 2015, 137(7), 1739-1748.
[http://dx.doi.org/10.1002/ijc.29537] [PMID: 25821117]
[89]
Zhang, Y.; Breitling, L.P.; Balavarca, Y.; Holleczek, B.; Schöttker, B.; Brenner, H. Comparison and combination of blood DNA methylation at smoking-associated genes and at lung cancer-related genes in prediction of lung cancer mortality. Int. J. Cancer, 2016, 139(11), 2482-2492.
[http://dx.doi.org/10.1002/ijc.30374] [PMID: 27503000]
[90]
Shenker, N.S.; Polidoro, S.; van Veldhoven, K.; Sacerdote, C.; Ricceri, F.; Birrell, M.A.; Belvisi, M.G.; Brown, R.; Vineis, P.; Flanagan, J.M. Epigenome-wide association study in the European Prospective Investigation into Cancer and Nutrition (EPIC-Turin) identifies novel genetic loci associated with smoking. Hum. Mol. Genet., 2013, 22(5), 843-851.
[http://dx.doi.org/10.1093/hmg/dds488] [PMID: 23175441]
[91]
Wang, L.; Aakre, J.A.; Jiang, R.; Marks, R.S.; Wu, Y.; Chen, J.; Thibodeau, S.N.; Pankratz, V.S.; Yang, P. Methylation markers for small cell lung cancer in peripheral blood leukocyte DNA. J. Thorac. Oncol., 2010, 5(6), 778-785.
[http://dx.doi.org/10.1097/JTO.0b013e3181d6e0b3] [PMID: 20421821]
[92]
Richmond, R.C.; Hemani, G.; Tilling, K. Davey Smith G; Relton CL. Challenges and novel approaches for investigating molecular mediation. Hum. Mol. Genet., 2016, 25, 149-156.
[http://dx.doi.org/10.1093/hmg/ddw197]
[93]
Battram, T.; Richmond, R.C.; Baglietto, L.; Haycock, P.C.; Perduca, V.; Bojesen, S.E.; Gaunt, T.R.; Hemani, G.; Guida, F.; Carreras-Torres, R.; Hung, R.; Amos, C.I.; Freeman, J.R.; Sandanger, T.M.; Nøst, T.H.; Nordestgaard, B.G.; Teschendorff, A.E.; Polidoro, S.; Vineis, P.; Severi, G.; Hodge, A.M.; Giles, G.G.; Grankvist, K.; Johansson, M.B.; Johansson, M.; Davey Smith, G.; Relton, C.L. Appraising the causal relevance of DNA methylation for risk of lung cancer. Int. J. Epidemiol., 2019, 48(5), 1493-1504.
[http://dx.doi.org/10.1093/ije/dyz190] [PMID: 31549173]
[94]
Chen, Y.; Widschwendter, M.; Teschendorff, A.E. Systems-epigenomics inference of transcription factor activity implicates aryl-hydrocarbon-receptor inactivation as a key event in lung cancer development. Genome Biol., 2017, 18(1), 236.
[http://dx.doi.org/10.1186/s13059-017-1366-0] [PMID: 29262847]
[95]
Boule, L.A.; Winans, B.; Lambert, K.; Vorderstrasse, B.A.; Topham, D.J.; Pavelka, M.S., Jr; Lawrence, B.P. Activation of the aryl hydrocarbon receptor during development enhances the pulmonary CD4+ T-cell response to viral infection. Am. J. Physiol. Lung Cell. Mol. Physiol., 2015, 309(3), L305-L313.
[http://dx.doi.org/10.1152/ajplung.00135.2015] [PMID: 26071552]
[96]
Beamer, C.A.; Shepherd, D.M. Role of the aryl hydrocarbon receptor (AhR) in lung inflammation. Semin. Immunopathol., 2013, 35(6), 693-704.
[http://dx.doi.org/10.1007/s00281-013-0391-7] [PMID: 23963493]
[97]
Horvath, S.; Zhang, Y.; Langfelder, P.; Kahn, R.S.; Boks, M.P.; van Eijk, K.; van den Berg, L.H.; Ophoff, R.A. Aging effects on DNA methylation modules in human brain and blood tissue. Genome Biol., 2012, 13(10), R97.
[http://dx.doi.org/10.1186/gb-2012-13-10-r97] [PMID: 23034122]

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