Methylation of RASSF1A, RASSF2A, and HIN-1 is associated with poor outcome after radiotherapy, but not surgery, in oral squamous cell carcinoma

Clinical Cancer Research

Volumn 15, Issue 12, 2009, Pages 4174-4180

  Huang, Kuo Hao ^a   Huang, Shiang Fu ^a,b   Chen, I How ^b   Liao, Chun Ta ^b   Wang, Hung Ming ^b   Hsieh, Ling Ling ^a  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; RAS PROTEIN;

ADULT; AGED; ARTICLE; CANCER RADIOTHERAPY; CANCER SURGERY; DENATURING HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; DNA METHYLATION; EPIGENETICS; GENE; GENE DOSAGE; GENE MUTATION; GENE SILENCING; HIN 1 GENE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOUTH CARCINOMA; ONCOGENE H RAS; ONCOGENE K RAS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PTEN GENE; RASSF1A GENE; RASSF2A GENE; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SQUAMOUS CELL CARCINOMA; TREATMENT OUTCOME; TUMOR SUPPRESSOR GENE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, SQUAMOUS CELL; CYTOKINES; DISEASE-FREE SURVIVAL; DNA METHYLATION; EPIGENESIS, GENETIC; FOLLOW-UP STUDIES; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE FREQUENCY; GENES, RAS; HUMANS; KAPLAN-MEIERS ESTIMATE; MIDDLE AGED; MOUTH NEOPLASMS; MUTATION; PROMOTER REGIONS, GENETIC; PROPORTIONAL HAZARDS MODELS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RADIATION TOLERANCE; REGRESSION ANALYSIS; TREATMENT OUTCOME; TUMOR SUPPRESSOR PROTEINS;

EID: 67449113765     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-08-2929     Document Type: Article

References (50)

1. Cancer Registry Annual Report 2005: Bureau of Health Promotion. Taiwan ROC: Department of Health; 2007.
2. Silverman S, Jr. Demographics and occurrence of oral and pharyngeal cancers. The outcomes, the trends, the challenge. J Am Dent Assoc 2001;132 Suppl:7-11S.
3. Dinshaw KA, Shrivastava SK, Sarin R, Agarwal J. Critical challenges in radiation therapy for head and neck cancer. New Delhi: Oxford University Press; 2000.
4. Lin YC, Hsiao JR, Tsai ST. Salvage surgery as the primary treatment for recurrent oral squamous cell carcinoma. Oral Oncol 2004;40:183-189 (Pubitemid 38030363)
5. Bernhard EJ, Stanbridge EJ, Gupta S, et al. Direct evidence for the contribution of activated N-ras and K-ras oncogenes to increased intrinsic radiation resistance in human tumor cell lines. Cancer Res 2000;60:6597-6600
6. Ling CC, Endlich B. Radioresistance induced by oncogenic transformation. Radiat Res 1989;120:267-279 (Pubitemid 19275183)
7. Miller AC, Kariko K, Myers CE, Clark EP, Samid D. Increased radioresistance of EJras-transformed human osteosarcoma cells and its modulation by lovastatin, an inhibitor of p21ras isoprenylation. Int J Cancer 1993;53:302-307 (Pubitemid 23042883)
8. McKennaWG, Muschel RJ, Gup ta AK, Hahn SM, Bernhard EJ. The RAS signal transduction pathway and its role in radiation sensitivity. Oncogene 2003;22:5866-5875
9. Gupta AK, Bakanauskas VJ, Cerniglia GJ, et al. The Ras radiation resistance pathway. Cancer Res 2001;61:4278-4282 (Pubitemid 32721000)
10. Gupta AK, McKenna WG, Weber CN, et al. Local recurrence in head and neck cancer: relationship to radiation resistance and signal transduction. Clin Cancer Res 2002;8:885-892 (Pubitemid 34742122)
11. Gupta AK, Cerniglia GJ,Mick R, et al. Radiation sensitization of human cancer cells in vivo by inhibiting the activity of PI3K using LY294002. Int J Radiat Oncol Biol Phys 2003;56:846-853 (Pubitemid 36677381)
12. Liang K, Jin W, Knuefermann C, et al. Targeting the phosphatidylinositol 3-kinase/Akt pathway for enhancing breast cancer cells to radiotherapy. Mol Cancer Ther 2003;2:353-360
13. Grana TM, Rusyn EV, Zhou H, Sartor CI, Cox AD. Ras mediates radioresistance through both phosphatidylinositol 3-kinase-dependent and Raf-dependent but mitogen-activated protein kinase/extracellular signal-regulated kinase kinase-independent signaling pathways. Cancer Res 2002;62:4142-4150 (Pubitemid 34791086)
14. Karnoub AE, Weinberg RA. Ras oncogenes: split personalities. Nat Rev 2008;9:517-531 (Pubitemid 351881844)
15. van der Weyden L, Adams DJ. The Ras-association domain family (RASSF) members and their role in human tumourigenesis. Biochim Biophys Acta 2007;1776:58-85. (Pubitemid 47332074)
16. Osaki M, Oshimura M, Ito H. PI3K-Akt pathway: its functions and alterations in human cancer. Apoptosis 2004;9:667-676 (Pubitemid 40941196)
17. Planchon SM, Waite KA, Eng C. The nuclear affairs of PTEN. J Cell Sci 2008;121:249-253 (Pubitemid 351356695)
18. Keniry M, Parsons R. The role of PTEN signaling perturbations in cancer and in targeted therapy. Oncogene 2008;27:5477-5485
19. Krop I, Parker MT, Bloushtain-Qimron N, et al. HIN-1, an inhibitor of cell growth, invasion, and AKT activation. Cancer Res 2005;65:9659-9669 (Pubitemid 41541441)
20. Shigematsu H, Suzuki M, Takahashi T, et al. Aberrant methylation of HIN-1 (high in normal-1) is a frequent event in many human malignancies. Int J Cancer 2005;113:600-604 (Pubitemid 40038736)
21. Hsieh LL, Huang TH, Chen IH, et al. p53 polymorphisms associated with mutations in and loss of heterozygosity of the p53 gene in male oral squamous cell carcinomas in Taiwan. Br J Cancer 2005;92:30-35 (Pubitemid 40188432)
22. 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 U S A 1996;93:9821-9826
23. Scott MK, Wei J, Weinstein IB. Rapid nonradioactive detectoion of ras oncogenes in human tumors. Amplifications 1990;4:22-26
24. Betz B, Florl AR, Seifert HH, Dall P, Schulz WA, Niederacher D. Denaturing high-performance liquid chromatography (DHPLC) as a reliable high-throughput prescreening method for aberrant promoter methylation in cancer. Hum Mutat 2004;23:612-620 (Pubitemid 38720613)
25. Deng D, Deng G, Smith MF, et al. Simultaneous detection of CpG methylation and single nucleotide polymorphism by denaturing high performance liquid chromatography. Nucleic Acids Res 2002;30:E13.
26. Kim IA, Fernandes AT, Gupta AK, McKenna WG, Bernhard EJ. The influence of Ras pathway signaling on tumor radiosensitivity. Cancer Metastasis Rev 2004;23:227-236 (Pubitemid 38881808)
27. Dallol A, Agathanggelou A, Tommasi S, Pfeifer GP, Maher ER, Latif F. Involvement of the RASSF1A tumor suppressor gene in controlling cell migration. Cancer Res 2005;65:7653-7659 (Pubitemid 41297238)
28. Thaler S, Hahnel PS, Schad A, Dammann R, Schuler M. RASSF1A mediates p21Cip1/Waf1-dependent cell cycle arrest and senescence through modulation of the Raf-MEK-ERK pathway and inhibition of Akt. Cancer Res 2009;69:1748-1757
29. Imai T, Toyota M, Suzuki H, et al. Epigenetic inactivation of RASSF2 in oral squamous cell carcinoma. Cancer Sci 2008;99:958-966 (Pubitemid 351997598)
30. Kuo MY, Jeng JH, Chiang CP, Hahn LJ. Mutations of Ki-ras oncogene codon 12 in betel quid chewing-related human oral squamous cell carcinoma in Taiwan. J Oral Pathol Med 1994;23:70-74 (Pubitemid 2054226)
31. Chang SE, Bhatia P, Johnson NW, et al. Ras mutations in United Kingdom examples of oral malignancies are infrequent. Int J Cancer1991;48:409-412
32. Warnakulasuriya KA, Chang SE, Johnson NW. Point mutations in the Ha-ras oncogene are detectable in formalin-fixed tissues of oral squamous cell carcinomas, but are infrequent in British cases. J Oral Pathol Med 1992;21:225-229
33. Xu J, Gimenez-Conti IB, Cunningham JE, et al. Alterations of p53, cyclin D1, Rb, and H-ras in human oral carcinomas related to tobacco use. Cancer 1998;83:204-212 (Pubitemid 28317798)
34. Sakai E, Rikimaru K, Ueda M, et al.The p53 tumor-suppressor gene and ras oncogene mutations in oral squamous-cell carcinoma. Int J Cancer 1992;52:867-872 (Pubitemid 23009500)
35. Lee LW, Yang KS, Yeh KT, Wang NM, Lin TH, Chang JG. Mutation analysis of ras oncogenes in oral squamous cell carcinoma. Mid Taiwan J Med 2001;6:69-73.
36. Dong SM, Sun DI, Benoit NE, Kuzmin I, Lerman MI, Sidransky D. Epigenetic inactivation of RASSF1A in head and neck cancer. Clin Cancer Res 2003;9:3635-3640 (Pubitemid 37169228)
37. Maruya S, Issa JP, Weber RS, et al. Differential methylation status of tumor-associated genes in head and neck squamous carcinoma: incidence and potential implications. Clin Cancer Res 2004;10:3825-3830 (Pubitemid 38697618)
38. Hasegawa M, Nelson HH, Peters E, Ringstrom E, Posner M, Kelsey KT. Patterns of gene promotermethylation in squamous cell cancer of the head and neck. Oncogene 2002;21:4231-4236 (Pubitemid 34753829)
39. Hogg RP, Honorio S, Martinez A, et al. Frequent 3p allele loss and epigenetic inactivation of the RASSF1A tumour suppressor gene from region 3p21.3 in head and neck squamous cell carcinoma. Eur J Cancer 2002;38:1585-1592 (Pubitemid 34879144)
40. Tran TN, Liu Y, Takagi M, Yamaguchi A, Fujii H. Frequent promoter hypermethylation of RASSF1A and p16INK4a and infrequent allelic loss other than 9p21 in betel-associated oral carcinoma in a Vietnamese non-smoking/non-drinking female population. J Oral Pathol Med 2005;34:150-156 (Pubitemid 40293223)
41. Dammann R, Schagdarsurengin U, Liu L, et al. Frequent RASSF1A promoter hypermethylation and K-ras mutations in pancreatic carcinoma. Oncogene 2003;22:3806-3812 (Pubitemid 36760743)
42. 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 (Pubitemid 30841096)
43. Kiel C, Wohlgemuth S, Rousseau F, et al. Recognizing and defining true Ras binding domains II: in silico prediction based on homology modelling and energy calculations. J Mol Biol 2005;348:759-775 (Pubitemid 40515681)
44. Mavros A, Hahn M,Wieland I, et al. Infrequent genetic alterations of the tumor suppressor gene PTEN/MMAC1 in squamous cell carcinoma of the oral cavity. J Oral Pathol Med 2002;31:270-276 (Pubitemid 34667678)
45. Shin KH, Kim JM, Rho KS, Park KH, Oh JE, Min BM. Inactivation of the PTEN gene by mutation, exonic deletion, and loss of transcript in human oral squamous cell carcinomas. Int J Oncol 2002;21:997-1001.
46. Ishida E, Nakamura M, Ikuta M, et al. Promotor hypermethylation of p14ARF is a key alteration for progression of oral squamous cell carcinoma. Oral Oncol 2005;41:614-622 (Pubitemid 40828879)
47. Yang Q, Kiernan CM, Tian Y, et al. Methylation of CASP8, DCR2, and HIN-1 in neuroblastoma is associated with poor outcome. Clin Cancer Res 2007;13:3191-3197
48. Bussink J, van der Kogel AJ, Kaanders JH. Activation of the PI3-K/AKT pathway and implications for radioresistance mechanisms in head and neck cancer. Lancet Oncol 2008;9:288-296 (Pubitemid 351722948)
49. Kim IA, Bae SS, Fernandes A, et al. Selective inhibition of Ras, phosphoinositide 3 kinase, and Akt isoforms increases the radiosensitivity of human carcinoma cell lines. Cancer Res 2005;65:7902-7910 (Pubitemid 41297268)
50. Esteller M. Epigenetic gene silencing in cancer: the DNA hypermethylome. Hum Mol Genet 2007;16Spec No. 1:R50-9.