DNA hypermethylation biomarkers to predict response to cisplatin treatment, radiotherapy or chemoradiation: The present state of art

Cellular Oncology

Volumn 35, Issue 4, 2012, Pages 231-241

  Roossink, Frank ^a   De Jong, Steven ^a   Wisman, G Bea A ^a   Van Der Zee, Ate G J ^a   Schuuring, Ed ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Biomarker; Cervical cancer; Chemoradiation; DNA hypermethylation; Predict; Response

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; CISPLATIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; TEMOZOLOMIDE; WNT PROTEIN;

ADVANCED CANCER; BREAST CANCER; CANCER RADIOTHERAPY; CANCER STAGING; CHEMORADIOTHERAPY; COLON CANCER; DNA DAMAGE; DNA METHYLATION; GENE CONTROL; HEAD AND NECK CANCER; HUMAN; LIVER CELL CARCINOMA; LUNG CANCER; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; REVIEW; STOMACH CANCER; TESTIS CANCER; TREATMENT OUTCOME; TREATMENT RESPONSE; UTERINE CERVIX CANCER;

ANTINEOPLASTIC AGENTS; CHEMORADIOTHERAPY; CISPLATIN; DNA METHYLATION; HUMANS; NEOPLASMS; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL;

EID: 84869998952     PISSN: 22113428     EISSN: 22113436     Source Type: Journal    
DOI: 10.1007/s13402-012-0091-7     Document Type: Review

References (94)

1. J. Ferlay, H.R. Shin, F. Bray, D. Forman, C. Mathers, D.M. Parkin, Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12), 2893-2917 (2010)
2. C. McNeil, New standard of care for cervical cancer sets stage for next questions. J Natl Cancer Inst 91(6), 500-501 (1999)
3. H.M. Keys, B.N. Bundy, F.B. Stehman, L.I. Muderspach, W.E. Chafe, C.L. Suggs 3rd, J.L. Walker, D. Gersell, Cisplatin, radiation, and adjuvant hysterectomy compared with radiation and adjuvant hysterectomy for bulky stage IB cervical carcinoma. N Engl J Med 340(15), 1154-1161 (1999) (Pubitemid 29177874)
4. M. Morris, P.J. Eifel, J. Lu, P.W. Grigsby, C. Levenback, R.E. Stevens, M. Rotman, D.M. Gershenson, D.G. Mutch, Pelvic radiation with concurrent chemotherapy compared with pelvic and para-aortic radiation for high-risk cervical cancer. N Engl J Med 340(15), 1137-1143 (1999) (Pubitemid 29177872)
5. C.W. Whitney, W. Sause, B.N. Bundy, J.H. Malfetano, E.V. Hannigan, W.C. Fowler Jr., D.L. Clarke-Pearson, S.Y. Liao, Randomized comparison of fluorouracil plus cisplatin versus hydroxyurea as an adjunct to radiation therapy in stage IIB-IVA carcinoma of the cervix with negative para-aortic lymph nodes: a Gynecologic Oncology Group and Southwest Oncology Group study. J Clin Oncol 17(5), 1339-1348 (1999) (Pubitemid 29220838)
6. W.A. Peters 3rd, P.Y. Liu, R.J. Barrett 2nd, R.J. Stock, B.J. Monk, J.S. Berek, L. Souhami, P. Grigsby, W. Gordon Jr., D.S. Alberts, Concurrent chemotherapy and pelvic radiation therapy compared with pelvic radiation therapy alone as adjuvant therapy after radical surgery in high-risk early-stage cancer of the cervix. J Clin Oncol 18(8), 1606-1613 (2000) (Pubitemid 30220538)
7. P.G. Rose, B.N. Bundy, E.B. Watkins, J.T. Thigpen, G. Deppe, M.A. Maiman, D.L. Clarke-Pearson, S. Insalaco, Concurrent cisplatin-based radiotherapy and chemotherapy for locally advanced cervical cancer. N Engl J Med 340(15), 1144-1153 (1999) (Pubitemid 29177873)
8. Chemoradiotherapy for Cervical Cancer Meta-Analysis Collaboration, Reducing Uncertainties About the Effects of Chemoradiotherapy for Cervical Cancer: A Systematic Review and Meta-Analysis of Individual Patient Data From 18 Randomized Trials. J Clin Oncol 26(35), 5802-5812 (2008)
9. A.W. Fyles, M. Pintilie, P. Kirkbride, W. Levin, L.A. Manchul, G.A. Rawlings, Prognostic factors in patients with cervix cancer treated by radiation therapy: results of a multiple regression analysis. Radiother Oncol 35(2), 107-117 (1995)
10. A. Jakobsen, P. Bichel, M. Vaeth, New prognostic factors in squamous cell carcinoma of cervix uteri. Am J Clin Oncol 8(1), 39-43 (1985) (Pubitemid 15059338)
11. D.S. Kapp, D. Fischer, E. Gutierrez, E.I. Kohorn, P.E. Schwartz, Pretreatment prognostic factors in carcinoma of the uterine cervix: a multivariable analysis of the effect of age, stage, histology and blood counts on survival. Int J Radiat Oncol Biol Phys 9(4), 445-455 (1983) (Pubitemid 13097080)
12. C.A. Perez, P.W. Grigsby, S.M. Nene, H.M. Camel, A. Galakatos, M.S. Kao, M.A. Lockett, Effect of tumor size on the prognosis ofcarcinoma of the uterine cervix treated with irradiation alone. Cancer 69(11), 2796-2806 (1992)
13. F.B. Stehman, B.N. Bundy, P.J. DiSaia, H.M. Keys, J.E. Larson, W.C. Fowler, Carcinoma of the cervix treated with radiation therapy. I. A multi-variate analysis of prognostic variables in the Gynecologic Oncology Group. Cancer 67(11), 2776-2785 (1991)
14. R.A. Cooper, C.M. West, D.P. Wilks, J.P. Logue, S.E. Davidson, S.A. Roberts, R.D. Hunter, Tumour vascularity is a significant prognostic factor for cervix carcinoma treated with radiotherapy: independence from tumour radiosensitivity. Br J Cancer 81(2), 354-358 (1999) (Pubitemid 29423718)
15. C.M. West, S.E. Davidson, S.A. Roberts, R.D. Hunter, The independence of intrinsic radiosensitivity as a prognostic factor for patient response to radiotherapy of carcinoma of the cervix. Br J Cancer 76(9), 1184-1190 (1997) (Pubitemid 27448015)
16. T. Toita, Y. Kakinohana, S. Shinzato, K. Ogawa, M. Yoshinaga, S. Iraha, M. Higashi, K. Sakumoto, K. Kanazawa, S. Sawada, Tumor diameter/volume and pelvic node status assessed by magnetic resonance imaging (MRI) for uterine cervical cancer treated with irradiation. Int J Radiat Oncol Biol Phys 43(4), 777-782 (1999) (Pubitemid 29152649)
17. C.A. Meanwell, K.A. Kelly, S. Wilson, C. Roginski, C. Woodman, R. Griffiths, G. Blackledge, Young age as a prognostic factor in cervical cancer: analysis of population based data from 10,022 cases. Br Med J (Clin Res Ed) 296(6619), 386-391 (1988) (Pubitemid 18039330)
18. F.N. Rutledge, M.F. Mitchell, M. Munsell, S. Bass, V. McGuffee, E.N. Atkinson, Youth as a prognostic factor in carcinoma of the cervix: a matched analysis. Gynecol Oncol 44(2), 123-130 (1992)
19. K.M. Prise, J.M. O'Sullivan, Radiation-induced bystander signalling in cancer therapy. Nat Rev Cancer 9(5), 351-360 (2009)
20. D. Verellen, M. De Ridder, N. Linthout, K. Tournel, G. Soete, G. Storme, Innovations in image-guided radiotherapy. Nat Rev Cancer 7 (12), 949-960 (2007) (Pubitemid 350165868)
21. M.W. Dewhirst, Y. Cao, B. Moeller, Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response. Nat Rev Cancer 8(6), 425-437 (2008) (Pubitemid 351744964)
22. A. Bird, Perceptions of epigenetics. Nature 447(7143), 396-398 (2007) (Pubitemid 46816744)
23. S.B. Baylin,M. Esteller, M.R. Rountree, K.E. Bachman, K. Schuebel, J.G. Herman, Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum Mol Genet 10(7), 687-692 (2001) (Pubitemid 32331576)
24. S.B. Baylin, J.E. Ohm, Epigenetic gene silencing in cancer -a mechanism for early oncogenic pathway addiction? Nat Rev Cancer 6(2), 107-116 (2006) (Pubitemid 43361543)
25. J.G. Herman, S.B. Baylin, Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 349(21), 2042-2054 (2003) (Pubitemid 37448928)
26. N. Yang, E.R. Nijhuis, H.H. Volders, J.J. Eijsink, A. Lendvai, B. Zhang, H. Hollema, E. Schuuring, G.B. Wisman, A.G. van der Zee, Gene promoter methylation patterns throughout the process of cervical carcinogenesis. Cell Oncol 32(1-2), 131-143 (2010)
27. G.H. Kang, S. Lee, W.H. Kim, H.W. Lee, J.C. Kim, M.G. Rhyu, J.Y. Ro, Epstein-barr virus-positive gastric carcinoma demonstrates frequent aberrant methylation of multiple genes and constitutes CpG island methylator phenotype-positive gastric carcinoma. AmJ Pathol 160(3), 787-794 (2002) (Pubitemid 34224568)
28. G.H. Kang, S. Lee, N.-Y. Cho, T. Gandamihardja, T.I. Long, D.J. Weisenberger, M. Campan, P.W. Laird, DNA methylation profiles of gastric carcinoma characterized by quantitative DNA methylation analysis. Lab Invest 88(2), 161-170 (2008) (Pubitemid 351161274)
29. K.L. Richards, B. Zhang, K.A. Baggerly, S. Colella, J.C. Lang, D.E. Schuller, R. Krahe, Genome-wide hypomethylation in head and neck cancer is more pronounced in HPV-negative tumors and is associated with genomic instability. PLoS One 4(3), e4941 (2009)
30. W.A. Burgers, L. Blanchon, S. Pradhan, Y. de Launoit, T. Kouzarides, F. Fuks, Viral oncoproteins target the DNA methyltransferases. Oncogene 26(11), 1650-1655 (2007) (Pubitemid 46398736)
31. C.B. Yoo, P.A. Jones, Epigenetic therapy of cancer: past, present and future. Nat Rev Drug Discov 5(1), 37-50 (2006)
32. J.A. Plumb, G. Strathdee, J. Sludden, S.B. Kaye, R. Brown, Reversal of drug resistance in human tumor xenografts by 2'-deoxy-5-azacytidine-induced demethylation of the hMLH1 gene promoter. Cancer Res 60(21), 6039-6044 (2000)
33. G. Strathdee, M.J. MacKean, M. Illand, R. Brown, A role for methylation of the hMLH1 promoter in loss of hMLH1 expression and drug resistance in ovarian cancer. Oncogene 18(14), 2335-2341 (1999) (Pubitemid 29192710)
34. F. Fang, C. Balch, J. Schilder, T. Breen, S. Zhang, C. Shen, L. Li, C. Kulesavage, A.J. Snyder, K.P. Nephew, D.E. Matei, A phase 1 and pharmacodynamic study of decitabine in combination with carboplatin in patients with recurrent, platinum-resistant, epithelial ovarian cancer. Cancer 116(17), 4043-4053 (2010)
35. J.M. Scandura, G.J. Roboz, M. Moh, E.W. Morawa, F. Brenet, J.R. Bose, L. Villegas, U.S. Gergis, S.A. Mayer, C.M. Ippoliti, T.J. Curcio, E.K. Ritchie, E.J. Feldman, Phase I study of epigenetic priming with decitabine prior to standard induction chemotherapy for patients with AML. Blood 118(6), 1472-1480 (2011)
36. M. Li, C. Balch, J.S. Montgomery, M. Jeong, J.H. Chung, P. Yan, T.H. Huang, S. Kim, K.P. Nephew, Integrated analysis of DNA methylation and gene expression reveals specific signaling pathways associated with platinum resistance in ovarian cancer. BMC Med Genomics 2, 34 (2009)
37. J.P. Issa, V. Gharibyan, J. Cortes, J. Jelinek, G. Morris, S. Verstovsek, M. Talpaz, G. Garcia-Manero, H.M. Kantarjian, Phase II study of low-dose decitabine in patients with chronic myelogenous leukemia resistant to imatinib mesylate. J Clin Oncol 23(17), 3948-3956 (2005) (Pubitemid 46218698)
38. R.M. Glasspool, M. Gore, G. Rustin, I. McNeish, R. Wilson, S. Pledge, J. Paul, M. Mackean, S. Halford, S. Kaye, Scottish Gynaecological Cancer Trials Group, Randomized phase II study of decitabine in combination with carboplatin compared with carboplatin alone in patients with recurrent advanced ovarian cancer. ASCO Meeting Abstracts 27(15), 5562 (2009)
39. S.S. Liu, R.C. Leung, K.Y. Chan, P.M. Chiu, A.N. Cheung, K.F. Tam, T.Y. Ng, L.C.Wong, H.Y. Ngan, p73 expression is associated with the cellular radiosensitivity in cervical cancer after radiotherapy. Clin Cancer Res 10(10), 3309-3316 (2004) (Pubitemid 38685435)
40. G. Narayan, H. Arias-Pulido, S. Koul, H. Vargas, F.F. Zhang, J. Villella, A. Schneider, M.B. Terry, M. Mansukhani, V.V. Murty, Frequent promoter methylation of CDH1, DAPK, RARB, and HIC1 genes in carcinoma of cervix uteri: its relationship to clinical outcome. Mol Cancer 2, 24 (2003)
41. G. Narayan, H. Arias-Pulido, S.V. Nandula, K. Basso, D.D. Sugirtharaj, H. Vargas, M. Mansukhani, J. Villella, L. Meyer, A. Schneider, L. Gissmann,M. Durst, B. Pothuri, V.V. Murty, Promoter hypermethylation of FANCF: disruption of Fanconi Anemia-BRCA pathway in cervical cancer. Cancer Res 64(9), 2994-2997 (2004) (Pubitemid 38581394)
42. T. Taniguchi, M. Tischkowitz, N. Ameziane, S.V. Hodgson, C.G. Mathew, H. Joenje, S.C. Mok, A.D. D'Andrea, Disruption of the Fanconi anemia-BRCA pathway in cisplatin-sensitive ovarian tumors. Nature Med 9(5), 568-574 (2003) (Pubitemid 36597103)
43. J.L. Ramirez, R. Rosell, M. Taron, M. Sanchez-Ronco, V. Alberola, PenasR. de Las, J.M. Sanchez, T. Moran,C.Camps,B. Massuti, J.J. Sanchez, F. Salazar, S. Catot, 14-3-3sigma methylation in pretreatment serum circulating DNA of cisplatin-plus-gemcitabinetreated advanced non-small-cell lung cancer patients predicts survival: The Spanish Lung Cancer Group. J Clin Oncol 23 (36), 9105-9112 (2005)
44. M. Zurita, P.C. Lara, R. del Moral, B. Torres, J.L. Linares-Fernandez, S.R. Arrabal, J. Martinez-Galan, F.J. Oliver, J.M. Ruizde Almodovar, Hypermethylated 14-3-3-sigma and ESR1 gene promoters in serum as candidate biomarkers for the diagnosis and treatment efficacy of breast cancer metastasis. BMC Cancer 10, 217 (2010)
45. P. Chaudhry, R. Srinivasan, F.D. Patel, Utility of gene promoter methylation in prediction of response to platinum-based chemotherapy in epithelial ovarian cancer (EOC). Cancer Invest 27(8), 877-884 (2009)
46. J.M. Teodoridis, J. Hall, S. Marsh, H.D. Kannall, C. Smyth, J. Curto, N. Siddiqui, H. Gabra, H.L. McLeod, G. Strathdee, R. Brown, CpG island methylation of DNA damage response genes in advanced ovarian cancer. Cancer Res 65(19), 8961-8967 (2005) (Pubitemid 41377387)
47. Y. Zhang, X. Qu, W. Jing, X. Hu, X. Yang, K. Hou, Y. Teng, J. Zhang, Y. Liu, GSTP1 determines cis-platinum cytotoxicity in gastric adenocarcinoma MGC803 cells: regulation by promoter methylation and extracellular regulated kinase signaling. Anticancer Drugs 20(3), 208-214 (2009)
48. R.C. Cumming, J. Lightfoot, K. Beard, H. Youssoufian, P.J. O'Brien, M. Buchwald, Fanconi anemia group C protein prevents apoptosis in hematopoietic cells through redox regulation of GSTP1. Nature Med 7(7), 814-820 (2001) (Pubitemid 32691636)
49. H.Y. Chen, C.J. Shao, F.R. Chen, A.L. Kwan, Z.P. Chen, Role of ERCC1 promoter hypermethylation in drug resistance to cisplatin in human gliomas. Int J Cancer 126(8), 1944-1954 (2010)
50. W. Wang, Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat Rev Genet 8 (10), 735-748 (2007) (Pubitemid 47429206)
51. K.S. Park, H.K. Kim, J.H. Lee, Y.B. Choi, S.Y. Park, S.H. Yang, S.Y. Kim, K.M. Hong, Transglutaminase 2 as a cisplatin resistance marker in non-small cell lung cancer. J Cancer Res Clin Oncol 136 (4), 493-502 (2010)
52. M. D'Eletto, M.G. Farrace, L. Falasca, V. Reali, S. Oliverio, G. Melino, M. Griffin, G.M. Fimia, M. Piacentini, Transglutaminase 2 is involved in autophagosome maturation. Autophagy 5(8), 1145-1154 (2009)
53. L.J. Nicholson, P.R. Smith, L. Hiller, P.W. Szlosarek, C. Kimberley, J. Sehouli, D. Koensgen, A.Mustea, P. Schmid, T. Crook, Epigenetic silencing of argininosuccinate synthetase confers resistance to platinum-induced cell death but collateral sensitivity to arginine auxotrophy in ovarian cancer. Int J Cancer 125(6), 1454-1463 (2009)
54. S. Battisti, D. Valente, L. Albonici, R. Bei, A. Modesti, C. Palumbo, Nutritional stress and arginine auxotrophy confer high sensitivity to chloroquine toxicity in mesothelioma cells. Am J Resp Cell Mol Biol 46(4), 498-506 (2012)
55. W. Dai, J.M. Teodoridis, C. Zeller, J. Graham, J. Hersey, J.M. Flanagan, E. Stronach, D.W. Millan, N. Siddiqui, J. Paul, R. Brown, Systematic CpG islands methylation profiling of genes in the wnt pathway in epithelial ovarian cancer identifies biomarkers of progression-free survival. Clin Cancer Res 17(12), 4052-4062 (2011)
56. J.A. Plumb, G. Strathdee, J. Sludden, S.B. Kaye, R. Brown, Reversal of drug resistance in human tumor xenografts by 2'-deoxy-5-azacytidine-induced demethylation of the hMLH1 gene promoter. Cancer Res 60(21), 6039-6044 (2000)
57. G. Gifford, J. Paul, P.A. Vasey, S.B. Kaye, R. Brown, The acquisition of hMLH1 methylation in plasma DNA after chemotherapy predicts poor survival for ovarian cancer patients. Clin Cancer Res 10(13), 4420-4426 (2004) (Pubitemid 38878884)
58. Wu Q, Vasquez KM (2008) Human MLH1 Protein Participates in Genomic Damage Checkpoint Signaling in Response to DNA Interstrand Crosslinks, while MSH2 Functions in DNA Repair. Plos Genet 4 (9)
59. H.-Y. Su, H.-C. Lai, Y.-W. Lin, C.-Y. Liu, C.-K. Chen, Y.-C. Chou, S.-P. Lin, W.-C. Lin, H.-Y. Lee, M.-H. Yu, Epigenetic silencing of SFRP5 is related to malignant phenotype and chemoresistance of ovarian cancer through Wnt signaling pathway. Int J Cancer 127 (3), 555-567 (2010)
60. J. Staub, J. Chien, Y. Pan, X. Qian, K. Narita, G. Aletti, M. Scheerer, L.R. Roberts, J. Molina, V. Shridhar, Epigenetic silencing of HSulf-1 in ovarian cancer:implications in chemoresistance. Oncogene 26(34), 4969-4978 (2007) (Pubitemid 47172647)
61. X. Chang, C.L. Monitto, S. Demokan, M.S. Kim, S.S. Chang, X. Zhong, J.A. Califano, D. Sidransky, Identification of hypermethylated genes associated with cisplatin resistance in human cancers. Cancer Res 70(7), 2870-2879 (2010)
62. W.J. Kim, Q.N. Vo, M. Shrivastav, T.A. Lataxes, K.D. Brown, Aberrant methylation of the ATM promoter correlates with increased radiosensitivity in a human colorectal tumor cell line. Oncogene 21(24), 3864-3871 (2002) (Pubitemid 34620854)
63. K. Roy, L. Wang, G.M. Makrigiorgos, B.D. Price, Methylation of the ATM promoter in glioma cells alters ionizing radiation sensitivity. Biochem Biophys Res Commun 344(3), 821-826 (2006)
64. H. De Schutter, H. Geeraerts, E. Verbeken, S. Nuyts, Promoter methylation of TIMP3 and CDH1 predicts better outcome in head and neck squamous cell carcinoma treated by radiotherapy only. Oncol Rep 21(2), 507-513 (2009)
65. S.L. Gerson, Clinical relevance of MGMT in the treatment of cancer. J Clin Oncol 20(9), 2388-2399 (2002) (Pubitemid 34441669)
66. M.E. Hegi, A.C. Diserens, T. Gorlia, M.F. Hamou, N. de Tribolet, M. Weller, J.M. Kros, J.A. Hainfellner, W. Mason, L. Mariani, J.E. Bromberg, P. Hau, R.O. Mirimanoff, J.G. Cairncross, R.C. Janzer, R. Stupp, MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352(10), 997-1003 (2005) (Pubitemid 40349502)
67. M. Esteller, J. Garcia-Foncillas, E. Andion, S.N. Goodman, O.F. Hidalgo, V. Vanaclocha, S.B. Baylin, J.G. Herman, Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 343(19), 1350-1354 (2000)
68. K.H. Huang, S.F. Huang, I.H. Chen, C.T. Liao, H.M. Wang, L.L. Hsieh, Methylation of RASSF1A, RASSF2A, and HIN-1 is associated with poor outcome after radiotherapy, but not surgery, in oral squamous cell carcinoma. Clin Cancer Res 15(12), 4174-4180 (2009)
69. Q.Z. Zhao, K.F. Dou, Methylation of Ras association domain family protein 1, isoform A correlated with proliferation and drug resistance in hepatocellular carcinoma cell line SMMC-7721. J Gastroenterol Hepatol 22(5), 683-689 (2007)
70. S. Honda, M. Haruta, W. Sugawara, F. Sasaki, M. Ohira, T. Matsunaga, H. Yamaoka, H. Horie, N. Ohnuma, A. Nakagawara, E. Hiyama, S. Todo, Y. Kaneko, The methylation status of RASSF1A promoter predicts responsiveness to chemotherapy and eventual cure in hepatoblastoma patients. Int J Cancer 123 (5), 1117-1125 (2008)
71. J. Bernier, E.J. Hall, A. Giaccia, Radiation oncology: a century of achievements. Nat Rev Cancer 4(9), 737-747 (2004) (Pubitemid 39215072)
72. D. Wang, S.J. Lippard, Cellular processing of platinum anticancer drugs. Nat Rev Drug Discov 4(4), 307-320 (2005) (Pubitemid 41130944)
73. M.B. Kastan, J. Bartek, Cell-cycle checkpoints and cancer. Nature 432(7015), 316-323 (2004) (Pubitemid 39551659)
74. Y. Shiloh, ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3(3), 155-168 (2003) (Pubitemid 37328868)
75. F. Roossink, H.W. Wieringa, M.G. Noordhuis, K.A. Ten Hoor, M. Kok, L. Slagter-Menkema, G.H. de Bock, H. Hollema, E. Pras, E.G.E. de Vries, S. de Jong, A.G.J. van der Zee, E. Schuuring, G.B.A. Wisman, M.A.T.M. van Vugt, The Role of ATM and 53BP1 as Predictive Markers and Therapeutic Targets in Cervical Cancer. Int J Cancer (2012). doi:10.1002/ijc.27488
76. J.P.T. Morris, S.C. Wang, M. Hebrok, KRAS, Hedgehog, Wnt and the twisted developmental biology of pancreatic ductal adenocarcinoma. Nat Rev Cancer 10(10), 683-695 (2010)
77. S. Angers, R.T. Moon, Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol 10(7), 468-477 (2009)
78. Y. Kawano, R. Kypta, Secreted antagonists of the Wnt signalling pathway. J Cell Sci 116(13), 2627-2634 (2003) (Pubitemid 36857216)
79. Y.W. Lin, M.T. Chung, H.C. Lai, M. De Yan, Y.L. Shih, C.C. Chang, M.H. Yu, Methylation analysis of SFRP genes family in cervical adenocarcinoma. J Cancer Res Clin Oncol 135(12), 1665-1674 (2009)
80. J. Ko, K.S. Ryu, Y.H. Lee, D.S. Na, Y.S. Kim, Y.M. Oh, I.S. Kim, J.W. Kim, Human Secreted Frizzled-Related Protein Is Downregulated and Induces Apoptosis in Human Cervical Cancer. Exp Cell Res 280(2), 280-287 (2002) (Pubitemid 35333769)
81. E.F. Wagner, A.R. Nebreda, Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 9(8), 537-549 (2009)
82. J.S. Sebolt-Leopold, R. Herrera, Targeting the mitogen-activated protein kinase cascade to treat cancer. Nat Rev Cancer 4(12), 937-947 (2004) (Pubitemid 39626217)
83. A.E. Karnoub, R.A. Weinberg, Ras oncogenes: split personalities. Nat Rev Mol Cell Biol 9(7), 517-531 (2008) (Pubitemid 351881844)
84. M.G. Noordhuis, J.J.H. Eijsink, K.A. ten Hoor, F. Roossink, H. Hollema, H.J.G. Arts, E. Pras, J.H. Maduro, A.K.L. Reyners, G.H. de Bock, G.B.A. Wisman, E. Schuuring, A.G.J. van der Zee, Expression of Epidermal Growth Factor Receptor (EGFR) and Activated EGFR Predict Poor Response to (Chemo)radiation and Survival in Cervical Cancer. Clin Cancer Res 15(23), 7389-7397 (2009)
85. Y. Liu, B. Cui, Y. Qiao, Y. Zhang, Y. Tian, J. Jiang, D. Ma, B. Kong, Phosphoinositide-3-kinase inhibition enhances radiosensitization of cervical cancer in vivo. Int J Gynecol Cancer 21(1), 100-105 (2011)
86. D.D. Meira, V.H. de Almeida, J.S. Mororo, I. Nobrega, L. Bardella, R.L. Silva, R.M. Albano, C.G. Ferreira, Combination of cetuximab with chemoradiation, trastuzumab or MAPK inhibitors: mechanisms of sensitisation of cervical cancer cells. Br J Cancer 101 (5), 782-791 (2009)
87. M. Ongenaert, G.B. Wisman, H.H. Volders, A.J. Koning, A.G. Zee, W. van Criekinge, E. Schuuring, Discovery of DNA methylation markers in cervical cancer using relaxation ranking. BMC Med Genomics 1, 57 (2008). doi:10.1186/1755-8794- 1-57
88. M.O. Hoque, M.S. Kim, K.L. Ostrow, J. Liu, G.B. Wisman, H.L. Park, M.L. Poeta, C. Jeronimo, R. Henrique, A. Lendvai, E. Schuuring, S. Begum, E. Rosenbaum, M. Ongenaert, K. Yamashita, J. Califano, W. Westra, A.G. van der Zee, W. Van Criekinge, D. Sidransky, Genome-wide promoter analysis uncovers portions of the cancer methylome. Cancer Res 68(8), 2661-2670 (2008) (Pubitemid 351556263)
89. J.J. Eijsink, A. Lendvai, V. Deregowski, H.G. Klip, G. Verpooten, L. Dehaspe, G.H. de Bock, H. Hollema, W. van Criekinge, E. Schuuring, A.G. van der Zee, G.B. Wisman, A four gene methylation marker panel as triage test in hr-HPV positive patients. Int J Cancer 130(8), 1861-1869 (2012)
90. E.R. Nijhuis, N. Reesink-Peters, G.B. Wisman, H.W. Nijman, J. van Zanden, H. Volders, H. Hollema, A.J. Suurmeijer, E. Schuuring, A.G. van der Zee, An overviewof innovative techniques to improve cervical cancer screening. Cell Oncol 28(5-6), 233-246 (2006) (Pubitemid 44950095)
91. D. Serre, B.H. Lee, A.H. Ting, MBD-isolated Genome Sequencing provides a high-throughput and comprehensive survey of DNA methylation in the human genome. Nucleic Acids Res 38(2), 391-399 (2010)
92. S. Stolzenburg, A. Bilsland, W.N. Keith, M.G. Rots, Modulation of gene expression using zinc finger-based artificial transcription factors. Methods Mol Biol 649, 117-132 (2010)
93. S. Koul, J. Houldsworth, M.M. Mansukhani, A. Donadio, J.M. McKiernan, V.E. Reuter, G.J. Bosl, R.S. Chaganti, V.V. Murty, Characteristic promoter hypermethylation signatures in male germ cell tumors. Mol Cancer 1, 8 (2002)
94. S.L. Lim, P. Smith, N. Syed, C. Coens, H. Wong, M. van der Burg, P. Szlosarek, T. Crook, J.A. Green, Promoter hypermethylation of FANCF and outcome in advanced ovarian cancer. Br J Cancer 98 (8), 1452-1456 (2008) (Pubitemid 351543586)