Promoter methylation of RASSF1A and DAPK and mutations of K-ras, p53, and EGFR in lung tumors from smokers and never-smokers

BMC Cancer

Volumn 7, Issue , 2007, Pages

  Liu, Yang ^a   Gao, Weimin ^b   Siegfried, Jill M ^c,f   Weissfeld, Joel L ^d,f   Luketich, James D ^e,f   Keohavong, Phouthone ^a,f  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b TEXAS TECH UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^e UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^f UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEATH ASSOCIATED PROTEIN KINASE; EPIDERMAL GROWTH FACTOR RECEPTOR; K RAS PROTEIN; PROTEIN P53; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; APOPTOSIS REGULATORY PROTEIN; PROTEIN KINASE (CALCIUM,CALMODULIN); RASSF1 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ADENOSQUAMOUS CARCINOMA; ADULT; AGED; ARTICLE; CANCER STAGING; CARCINOID; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; GENE MUTATION; HISTOPATHOLOGY; HUMAN; LARGE CELL CARCINOMA; LUNG ADENOCARCINOMA; LUNG ALVEOLUS CELL CARCINOMA; LUNG NON SMALL CELL CANCER; MAJOR CLINICAL STUDY; MALE; MULTIVARIATE ANALYSIS; NEUROENDOCRINE TUMOR; POLYMERASE CHAIN REACTION; PREVALENCE; PROMOTER REGION; PROTEIN METHYLATION; SMOKING; SQUAMOUS CELL CARCINOMA; UNITED STATES; COMPARATIVE STUDY; DNA METHYLATION; GENETICS; LUNG TUMOR; METABOLISM; MIDDLE AGED; MUTATION; ONCOGENE RAS; PHYSIOLOGY; PROTO ONCOGENE; TUMOR SUPPRESSOR GENE;

AGED; APOPTOSIS REGULATORY PROTEINS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; DNA METHYLATION; FEMALE; GENES, ERBB-1; GENES, P53; GENES, RAS; HUMANS; LUNG NEOPLASMS; MALE; MIDDLE AGED; MUTATION; PROMOTER REGIONS (GENETICS); SMOKING; TUMOR SUPPRESSOR PROTEINS;

EID: 34250795615     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-7-74     Document Type: Article

References (50)

1. Hecht SS Tobacco smoke carcinogens and lung cancer J Natl Cancer Inst 1999 91 1194-1210 10.1093/jnci/91.14.1194 10413421
2. Keohavong P DeMichele MA Melacrinos AC Landreneau RJ Weyant RJ Siegfried JM Detection of K-ras mutations in lung carcinomas: Relationship to prognosis Clin Cancer Res 1996 2 411-418 9816185
3. Gealy R Zhang L Siegfried JM Luketich JD Keohavong P Comparison of mutations in the p53 and K-ras genes in lung carcinomas from smoking and nonsmoking women Cancer Epidemiol Biomarkers Prev 1999 8 297-302 10207632
4. Ahrendt SA Decker PA Alawi EA Zhu YrYR Sanchez-Cespedes M Yang SC Haasler GB Kajdacsy-Balla A Demeure MJ Sidransky D Cigarette smoking is strongly associated with mutation of the K-ras gene inpatients with primary adenocarcinoma of the lung Cancer 2001 92 1525-1530 10.1002/ 1097-0142(20010915)92:6<1525::AID-CNCR1478>3.0.CO;2-H 11745231
5. Pao W Miller V Zakowski M Doherty J Politi K Sarkaria I Singh B Heelan R Rusch V Fulton L Mardis E Kupfer D Wilson R Kris M Varmus H EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib Proc Natl Acad Sci USA 2004 101 13306-13311 516528 15329413 10.1073/ pnas.0405220101
6. Kosaka T Yatabe Y Endoh H Kuwano H Takahashi T Mitsudomi T Mutations of the epidermal growth factor receptor gene in lung cancer: Biological and clinical implications Cancer Res 2004 64 8919-8923 10.1158/ 0008-5472.CAN-04-2818 15604253
7. Shigematsu H Lin L Takahashi T Nomura M Suzuki M Wistuba II Fong KM Lee H Toyooka S Shimizu N Fujisawa T Feng Z Roth JA Herz T Minna JD Gazdar AF Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancers J Natl Cancer Inst 2005 97 339-346 15741570
8. Husgafvel-Pursiainen K Boffetta P Kannio A Nyberg F Pershagen G Mukeria A Constantinescu V Fortes C Benhamou S p53 mutations and exposure to environmental tobacco smoke in a multicenter study on lung cancer Cancer Res 2000 60 2906-2911 10850436
9. Kim DH Nelson HH Wiebcke JK Zheng S Christiani DC Wain JC Mark EJ Kelsey KT p16(INK4a) and histology-specific methylation of CpG islands exposure to tobacco smoke in non-small cell lung cancer Cancer Res 2001 61 3419-3424 11309302
10. Toyooka S Maruyama R Toyooka KO Mclerran D Feng Z Fukuyama Y Virmani AK Zochbauer-Muller S Tsukuda K Sugio K Shimizu N Shimizu K Lee H Chen CY Fong KM Gilcrease M Roth JA Minna JD Gazdar AF Smoke exposure, histologic type and geography-related differences in the methylation profiles of non-small cell lung cancer Int J Cancer 2003 103 153-160 10.1002/ijc.10787 12455028
11. Divine KK Pulling LC Marron-Terada PG Liechty KC Kang T Schwartz AG Bocklage TJ Coons TA Gilliland FD Belinsky SA Multiplicity of abnormal promoter methylation in lung adenocarcinomas from smokers and never smokers Int J Cancer 2005 114 400-405 10.1002/ijc.20761 15578700
12. Liu Y Lan Q Siegfried JM Luketich JD Keohavong P Aberrant promoter methylation of p16 and MGMT genes in lung tumors from smoking and never-smoking lung cancer patients Neoplasia 2006 8 46-51 1584289 16533425 10.1593/neo.05586
13. Toyooka S Tokumo M Shigekatsu H Matsuo K Asano H Tomii K Ichihara S Suzuki M Aoe M Date H Gazda AF Shimizu N Mutational and epigenetic evidence for independent pathways for lung adenocarcinomas arising in smokers and never smokers Cancer Res 2006 66 1371-1375 10.1158/ 0008-5472.CAN-05-2625 16452191
14. Agathanggelou A Cooper WN Latif F Role of the Ras-association domain family tumor suppressor gene in human cancers Cancer Res 2005 65 3497-3508 10.1158/0008-5472.CAN-04-4088 15867337
15. Dammann R Li C Yoon JH Chin PL Bates S Pfeifer GP Epigenetic inactivation of a RAS association domain familyprotein from the lung tumour suppressor locus 3p21.3 Nat Genet 2000 25 315 319-10.1038/77083 10888881
16. Burbee DG Forgacs E Zochbauer-Muller S Shivakumar L Fong K Gao B Randle D Kondo M Virmani A Bader S Sekido Y Latif F Milchgrub S Toyooka S Gazda AF Lerman MI Zabarovsky E White M Minna JD Epigenetic inactivation of RASSF1A in lung and breast cancers and malignant phenotype suppression J Natl Cancer Inst 2001 93 691-699 10.1093/jnci/93.9.691 11333291
17. Marsit CJ Kim DH Liu M Hinds PW Wiencke JK Nelson HH Kelsey KT Hypermethylation of RASSF1A and BLU tumor suppressor genes in non-small cell lung cancer: Implications for tobacco smoking during adolescence Int J Cancer 2005 114 219-223 10.1002/ijc.20714 15540210
18. Shohat G Shani G Eisenstein M Kimchi A The DAP-kinase family of proteins: Study of a novel group of calcium-regulated death-promoting kinases Biochim Biophys Acta 2002 1600 1-2 45-50 12445458
19. Inbal B Cohen O Polak-Charcon S Kopolovic J Vadai E Eisenbach L Kimchi A DAP kinase links the control of apoptosis to metastasis Nature 1997 390 180-184 10.1038/36599 9367156
20. Tang X Khuri FR Lee JJ Kemp BL Liu D Hong WK Mao L Hypermethylation of the death-associated protein (DAP) kinase promoter and aggressiveness in stage I non-small-cell lung cancer J Natl Cancer Inst 2000 92 1511-1516 10.1093/jnci/92.18.1511 10995806
21. Kim DH Nelson HH Wiencke JK Christiani DC Wain JC Mark EJ Kelsey KT Promoter methylation of DAP-kinase: Association with advanced stage in non-small cell lung cancer Oncogene 2001 20 1765-1770 10.1038/ sj.onc.1204302 11313923
22. Baylin SB Ohm JE Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nat Rev Cancer 2006 6 107-116 10.1038/ nrc1799 16491070
23. Rouleau J Macleod AR Szyf M Regulation of the DNA methyltransferase by the Ras-AP-1 signaling pathway J Biol Chem 1995 270 1595-1601 10.1074/ jbc.270.4.1595 7829490
24. Macleod AR Rouleau J Szyf M Regulation of DNA methylation by the Ras signaling pathway J Biol Chem 1995 270 11327-11337 10.1074/ jbc.270.19.11327 7744770
25. Vos MD Ellis CA Bell A Birrer MJ Clark GJ Ras uses the novel tumor suppressor RASSF1 as an effector to mediate apoptosis J Biol Chem 2000 275 35669-35672 10.1074/jbc.C000463200 10998413
26. Khokhlatchev A Rabizadeh S Xavier R Nedwidek M Chen T Zhang XF Seed B Avruch J Identification of a novel Ras-regulated proapoptotic pathway Curr Biol 2002 12 253-265 10.1016/S0960-9822(02)00683-8 11864565
27. Feig LA Buchsbaum RJ Cell signaling: Life or death decisions of ras proteins Curr Biol 2002 12 R259-261 10.1016/S0960-9822(02)00787-X 11937045
28. Ortiz-Vega S Khokhlatchev A Nedwidek M Zhang XF Dammann R Pfeifer GP Avruch J The putative tumor suppressor RASSF1A homodimerizes and heterodimerizes with the Ras-GTP binding protein Nore1 Oncogene 2002 21 1381-1390 10.1038/sj.onc.1205192 11857081
29. Raveh T Droguett G Horwitz MS DePinho RA Kimchi A DAP kinase activates a p19ARF/p53-mediated apoptotic checkpoint to suppress oncogenic transformation Nat Cell Biol 2001 3 1-7 10.1038/35050500 11146619
30. Gottlieb TM Oren M p53 in growth control and neoplasia Biochim Biophys Acta 1996 1287 77-102 8672531
31. Ko LJ Prives C p53: Puzzle and paradigm Genes Dev 1996 10 1054-1072 8654922
32. Arteaga CL Overview of epidermal growth factor receptor biology and its role as a therapeutic target in human neoplasia Semin Oncol 2002 29 3-9 12422308
33. Paez JG Janne PA Lee JC Tracy S Greulich H Gabriel S Herman P Kaye FJ Lindeman N Boggon TJ Naoki K Sasaki H Fujii Y Eck MJ Sellers WR Johnson BE Meyerson M EGFR mutations in lung cancer: Correlation with linical response to gefitinib therapy Science 2004 304 1497-1500 10.1126/ science.1099314 15118125
34. Lynch TJ Bell DW Sordella R Gurubhagavatula S Okimoto RA Brannigan BW Harris PL Hasserlat SM Supko JG Haluska FG Louis DN Christiani DC Settleman J Haber DA Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib N Engl J Med 2004 350 2129-2139 10.1056/NEJMoa040938 15118073
35. Herman JG Graff JR Myohanen S Nelkin BD Baylin SB Methylation-specific PCR: A novel PCR assay for methylation status of CpG islands Proc Natl Acad Sci USA 1996 93 9821-9826 38513 8790415 10.1073/pnas.93.18.9821
36. Palmisano WA Divine KK Saccomanno G Gilliland FD Baylin SB Herman JG Belinsky SA Predicting lung cancer by detecting aberrantpromoter methylation in sputum Cancer Res 2000 60 5954-5958 11085511
37. Belinsky SA Palmisano WA Gilliland FD Crooks LA Divine KK Winters SA Grimes MJ Harms HJ Tellez CS Smith TM Moots PP Lechner JF Stidley CA Crowell RE Aberrant promoter methylation in bronchial epithelium and sputum from current and former smokers Cancer Res 2002 62 2370-2377 11956099
38. Gao WM Mady HH Yu GY Siegfried JM Luketich JD Melhem MF Keohavong P Comparison of p53 mutations between adenocarcinoma and squamous cell carcinoma of the lung: Unique spectra involving G to A transitions and G to T transversions in both histologic types Lung Cancer 2003 40 141-150 10.1016/S0169-5002(03)00035-7 12711114
39. Zhang W Stabile LP Keohavong P Romkes M Grandis JR Traynor AM Siegfried JM Mutation and polymorphism in the EGFR-TK domain associated with lung cancer J Thorac Oncol 2006 1 635-647 17409930
40. Suzuki M Shigematsu H Iizasa T Hiroshima K Nakatani Y Minna JD Fujisawa T Exclusive mutation in epidermal growth factorreceptor gene, HER-2, and KRAS, and synchronous methylation of nonsmall cell lung cancer Cancer 2006 106 2200-2207 10.1002/cncr.21853 16598760
41. Endoh H Yatabe Y Shimizu S Tajima K Kuwano H Takahashi T Mitsudomi T RASSF1A gene inactivation in non-small cell lung cancer and its clinical implication Int J Cancer 2003 106 45-51 10.1002/ijc.11184 12794755
42. Kim DH Kim JS Ji YI Shim YM Kim H Han J Park J Hypermethylation of RASSF1A promoter is associated with theage at starting smoking and a poor prognosis in primary non-smallcell lung cancer Cancer Res 2003 63 3743-3746 12839968
43. Kim DH Kim JS Park JH Lee SK Ji YI Kwon YM Shim YM Han J Park J Relationship of Ras association domain family 1 methylation and K-ras mutation in primary non-small cell lung cancer Cancer Res 2003 63 6206-6211 14559805
44. Toyooka S Toyooka KO Miyajima K Reddy JL Toyota M Sathyanarayana UG Padar A Tockman MS Lam S Shivapurkar N Gazdar AF Epigenetic down-regulation of death-associated protein kinase in lung cancers Clin Cancer Res 2003 9 3034-3041 12912953
45. Russo AL Thiagalingam A Pan H Califano J Cheng KH Ponte JF 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 2466-2470 10.1158/1078-0432.CCR-04-1962 15814621
46. Tomizawa Y Kohno T Kondo H Otsuka A Nishioka M Niki T Yamada T Maeshima A Yoshimura K Saito R Minna JD Yokota J Clinicopathological significance of epigenetic inactivation of RASSF1A at 3p21.3 in stage I lung adenocarcinoma Clin Cancer Res 2002 8 2362-2368 12114441
47. Tomizawa Y Iijima H Sunaga N Sato K Takise A Otani Y Tanaka S Suga T Saito R Ishizuka T Dobashi K Minna JD Nakajima T Mori M Clinicopathologic significance of the mutations of the epidermal growth factor receptor gene in patients with non-small cell lung cancer Clin Cancer Res 2005 11 6816-6822 10.1158/1078-0432.CCR-05-0441 16203769
48. Van Engeland M Roemen GM Brink M Pachen MM Weijenberg MP de Bruine AP Arends JW van den Brandt PA de Goeij AF Herman JG K-ras mutations and RASSF1A promoter methylation in colorectal cancer Oncogene 2002 21 3792-3795 10.1038/sj.onc.1205466 12032847
49. Dammann R Schagdarsurengin U Strunnikova M Rastetter M Seidel C Liu L Tommasi S Pfeifer GP Epigenetic inactivation of the Ras-association domain family 1 (RASSF1A) gene and its function in human carcinogenesis Histol Histopathol 2003 18 665-677 12647816
50. Oliveira C Vello S Domingo E Preto A Hofstra RM Hamelin R Yamamoto H Seruca R Schwartz S Jr Concomitant RASSF1A hypermethylation and KRAS/ BRAF mutations occur preferentially in MSI sporadic colorectal cancer Oncogene 2005 24 7630-7634 10.1038/sj.onc.1208906 16007118