Frequent epigenetic silencing of the p16 gene in non-small cell lung cancers of tobacco smokers

Japanese Journal of Cancer Research

Volumn 93, Issue 10, 2002, Pages 1107-1113

  Yanagawa, Naoki ^a   Tamura, Gen ^a   Oizumi, Hiroyuki ^a   Takahashi, Nobumasa ^a   Shimazaki, Yasuhisa ^a   Motoyama, Teiichi ^a  

^a YAMAGATA UNIVERSITY   (Japan)

Author keywords

Non small cell lung cancer; p16 gene; Promoter methylation; Tobacco smoking

Indexed keywords

AGED; ARTICLE; CHROMOSOME 9; DNA METHYLATION; FEMALE; GENE SILENCING; GENETICS; HETEROZYGOSITY LOSS; HUMAN; LUNG NON SMALL CELL CANCER; LUNG TUMOR; MALE; MIDDLE AGED; PROMOTER REGION; SMOKING; TUMOR SUPPRESSOR GENE; ADULT; CANCER RISK; CIGARETTE SMOKING; CONTROLLED STUDY; GENE DELETION; GENE INACTIVATION; HISTOPATHOLOGY; HOMOZYGOSITY; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG CARCINOGENESIS; MAJOR CLINICAL STUDY; MUTATIONAL ANALYSIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METHYLATION; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; SQUAMOUS CELL CARCINOMA; STATISTICAL ANALYSIS;

AGED; CARCINOMA, NON-SMALL-CELL LUNG; CHROMOSOMES, HUMAN, PAIR 9; DNA METHYLATION; FEMALE; GENE SILENCING; GENES, P16; HUMANS; LOSS OF HETEROZYGOSITY; LUNG NEOPLASMS; MALE; MIDDLE AGED; PROMOTER REGIONS (GENETICS); SMOKING;

MICROSATELLITE DNA; PROTEIN P16;

EID: 0036808073     PISSN: 09105050     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2002.tb01212.x     Document Type: Article

References (37)

1. Rom, W. N., Hay, J. G., Lee, T. C., Jiang, Y. and Tchouwong, K. Molecular and genetic aspects of lung cancer. Am. J. Respir. Crit. Care Med., 161, 1355-1367 (2000).
2. INK4A is an early event in lung cancer and a potential marker for early diagnosis. Proc. Natl. Acad. Sci. USA, 95, 11891-11896 (1998).
3. INK4a and histology-specific methylation of CpG islands by exposure to tobacco smoke in non-small cell lung cancer. Cancer Res., 61, 3419-3424 (2001).
4. Greenblatt, M. S., Bennett, W. P., Hollstein, M. and Harris, C. C. Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res., 54, 4855-4878 (1994).
5. Denissenko, M. F., Pao, A., Tang, M. and Pfeifer, G. P. Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in p53. Science, 274, 430-432 (1996).
6. Esposito, V., Baldi, A., De Luca, A., Micheli, P., Mazzarella, G., Baldi, F., Caputi, M. and Giordano, A. Prognostic value of p53 in non-small cell lung cancer: relationship with proliferating cell nuclear antigen and cigarette smoking. Hum. Pathol., 28, 233-237 (1997).
7. Tammemagi, M. C., McLaughlin, J. R. and Bull, S. B. Meta-analysis of p53 tumor suppressor gene alterations and clinicopathological features in resected lung cancers. Cancer Epidemiol. Biomarkers Prev., 8, 625-634 (1999).
8. Sozzi, G., Sard, L., De Gregorio, L., Marchetti, A., Musso, K., Buttitta, F., Tornielli, S., Pellegrini, S., Veronese, M. L., Manenti, G., Incardone, M., Chella, A., Angeletti, C. A., Pastorino, U., Huebner, K., Bevilaqua, G., Pilotti, S., Croce, C. M. and Pierotti, M. A. Association between cigarette smoking and FHIT gene alterations in lung cancer. Cancer Res., 57, 2121-2123 (1997).
9. Nelson, H. H., Christiani, D. C., Mark, E. J., Wiencke, J. K., Wain, J. C. and Kelsey, K. T. Implications and prognostic value of K-ras mutation for early-stage lung cancer in women. J. Natl. Cancer Inst., 91, 2032-2038 (1999).
10. Cespedes, M. S., Decker, P. A., Doffek, K. M., Esteller, M., Westra, W. H., Alawi, E. A., Herman, J. G., Demeure, M. J., Sidransky, D. and Ahrendt, S. A. Increased loss of chromosome 9p21 but not p16 inactivation in primary non-small cell lung cancer from smokers. Cancer Res., 61, 2092-2096 (2001).
11. Sherr, C. J. G1 phase progression: cycling on cue. Cell, 79, 551-555 (1994).
12. Weinberg, R. A. The retinoblastoma protein and cell cycle control. Cell, 81, 323-330 (1995).
13. Serrano, M., Hannon, G. J. and Beach, D. A new regulatory motif in cell cycle control causing specific inhibition of cyclin D/CDK4. Nature, 366, 704-707 (1993).
14. Kamb, A., Guis, N. A., Weaver-Feldhaus, J., Liu, Q., Harshman, K., Tavtigian, S. V., Stodkert, E., Day, R. S., Johns, B. E. and Skolnick, M. H. A cell cycle regulator potentially involved in genesis of many tumor types. Science, 264, 436-440 (1994).
15. INK4A expression in resected non-small cell lung tumors. Cancer Res., 56, 3415-3420 (1996).
16. INK4A inactivation in non small-cell lung cancers. Oncogene, 16, 497-504 (1998).
17. Cespedes, M. S., Reed, A. L., Buta, M., Wu, L., Westra, W. H., Herman, J. G., Yang, S. C., Jen, J. and Sidransky, D. Inactivation of the INK4A/ARF locus frequently coexists with TP53 mutations in non-small cell lung cancer. Oncogene, 18, 5843-5849 (1999).
18. Nobori, T., Miura, K., Wu, D. J., Lois, A., Takabayashi, K. and Carson, D. A deletion of the cyclin-dependent kinase-4 inhibitor gene in multiple human cancers. Nature, 368, 753-756 (1994).
19. De Vos, S., Miller, C. W., Gombart, A. F., Cho, S. K. and Koeffler, H. P. Alterations of CDKN2 (p16) in non-small cell lung cancer. Genes Chromosom. Cancer, 14, 165-170 (1995).
20. Cairns, P., Mao, L., Merlo, A., Lee, D. J., Schwab, D., Eby, Y., Tokino, K., van der Riet, P., Blaugrund, J. E. and Sidransky, D. Rates of p16 (MTS1) mutations in primary tumors with 9p loss. Science, 265, 415-417 (1994).
21. INK4B/MTS2, and p18 genes in primary and metastatic lung cancer. Cancer Res., 55, 1448-1451 (1995).
22. Merlo, A., Herman, J. G., Mao, L., Lee, D. J., Gabrielson, E., Burger, P. C., Baylin, S. B. and Sidransky, D. 5′ CpG island methylation is associated with transcriptional silencing of the tumor suppressor p16/CDKN2/MTS1 in human cancer. Nat. Med., 1, 686-692 (1995).
23. Kashiwabara, K., Oyama, T., Sano, T., Fukuda, T. and Nakajima, T. Correlation between methylation status of the p16/CDKN2 gene and the expression of p16 and Rb proteins in primary non-small cell lung cancers. Int. J. Cancer, 79, 215-220 (1998).
24. Cairns, P., Polascik, T. J., Eby, Y., Tokino, K., Califano, J., Merlo, A., Mao, L., Herath, J., Jenkins, R., Westra, W., Rutter, J. L., Buckler, A., Gabrielson, E., Tockman, M., Cho, K. R., Hedrick, L., Bova, G. S., Isaacs, W., Koch, W., Schwab, D. and Sidransky, D. Frequency of homozygous deletion at p16/CDKN2 in primary human tumors. Nat. Genet., 11, 210-212 (1995).
25. Reed, A. L., Califano, J., Cairns, P., Westra, W. H., Jones, R. M., Koch, W., Ahrendt, S., Eby, Y., Sewell, D., Nawroz, H., Bartek, J. and Sidransky, D. High frequency of p16 (CDKN2/MTS-1/INK4A) inactivation in head and neck squamous cell carcinoma. Cancer Res., 56, 3630-3633 (1996).
26. Herman, J. G., Graff, J. R., Myohane, S., Nelkin, B. D. and Baylin, S. B. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc. Natl. Acad. Sci. USA, 93, 9821-9826 (1996).
27. Sakata, K., Tamura, G., Maesawa, C., Suzuki, Y., Terashima, M., Satoh, K., Eda, Y., Suzuki, A., Sekiyama, S. and Satodate, R. Loss of heterozygosity on the short arm of chromosome 9 without p16 gene mutation in gastric carcinomas. Jpn. J. Cancer Res., 86, 333-335 (1995).
28. Gorgoulis, V. G., Zacharatos, P., Kotsinas, A., Liloglou, T., Kyroudi, A., Veslemes, M., Rassidakis, A., Halazonetis, T. D., Field, J. K. and Kittas, C. Alterations of p16-pRb pathway and the chromosome locus 9p21-22 in non-small-cell lung carcinomas: relationship with p53 and MDM2 protein expression. Am. J. Pathol., 144, 296-302 (1998).
29. INK4A and alterations of the 9p21-23 chromosome region in non-small-cell lung carcinomas: relationship with tumor growth parameters and ploidy status. Int. J. Cancer, 89, 133-141 (2000).
30. Muller, S. Z., Fong, K. M., Virtami, A. K., Geradts, J., Gazdar, A. F. and Minna, J. D. Aberrant promotor methylation of multiple genes in non-small cell lung cancers. Cancer Res., 61, 249-255 (2001).
31. Belinsky, S. A., Palmisano, W. A., Gilliland, F. D., Crooks, L. A., Divine, K. K., Winters, S. A., Grimes, M. J., Harms, H. J., Tellez, C. S., Smith, T. M., Moots, P. P., Lechner, J. F., Stidley, C. A. and Crowell, R. E. Aberrant promoter methylation in bronchial epithelium and sputum from current and former smokers. Cancer Res., 62, 2370-2377 (2002).
32. INK4A in primary rat lung tumors. Mol. Cell. Biol., 17, 1366-1374 (1997).
33. Eguchi, K., Kanai, Y., Kobayashi, K. and Hirohashi, S. DNA hypermethylation at the D17S5 locus in non-small cell lung cancers: its association with smoking history. Cancer Res., 57, 4913-4915 (1997).
34. Lee, Y. W., Klein, C. B., Kargacin, B., Salnikow, K., Kitahara, J., Dowjat, W., Zhitkovich, A., Christie, N. T. and Costa, M. Carcinogenic nickel silences gene expression by chromatin condensation and DNA methylation: a new model for epigenetic carcinogens. Mol. Cell. Biol., 15, 2547-2557 (1995).
35. Belinsky, S. A., Nikula, K. J., Baylin, S. B. and Issa, J. P. Increased cytosine DNA-methyltransferase activity is target-cell-specific and an early event in lung cancer. Proc. Natl. Acad. Sci. USA, 93, 4045-4050 (1996).
36. Okami, K., Cairns, P., Westra, W. H., Linn, J. F., Ahrendt, S. A., Wu, L., Sidransky, D. and Jen, J. Detailed deletion mapping at chromosome 9p21 in non-small cell lung cancer by microsatellite analysis and fluorescence in situ hybridization. Int. J. Cancer, 74, 588-592 (1997).
37. Nakayama, T., Kanedo, M., Kodama, M. and Nagata, C. Cigarette smoke induces DNA single-strand breaks in human cells. Nature, 314, 462-464 (1985).