Promoter CpG island methylation markers in colorectal cancer: The road ahead

Epigenomics

Volumn 4, Issue 2, 2012, Pages 179-194

  Draht, Muriel X G ^a   Riedl, Robert R ^a   Niessen, Hanneke ^a   Carvalho, Beatriz ^b   Meijer, Gerrit A ^b   Herman, James G ^c   Van Engeland, Manon ^a   Melotte, Veerle ^a   Smits, Kim M ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

colorectal cancer; DNA methylation; early detection marker; prediction marker; prognostic marker

Indexed keywords

ATM PROTEIN; BETA ACTIN; CARCINOEMBRYONIC ANTIGEN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DNA; FLNC PROTEIN; FLUOROURACIL; ID4 PROTEIN; IRINOTECAN; K RAS PROTEIN; METHYL CPG BINDING PROTEIN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; NDRG4 PROTEIN; NEUROG1 PROTIEN; OSTEOGENIN; OXALIPLATIN; PROTEIN MLH1; PROTEIN P14; PROTEIN P16; PROTEIN P53; PROTEIN RET; SECRETED FRIZZLED RELATED PROTEIN 1; SECRETED FRIZZLED RELATED PROTEIN 2; SEPT9 PROTEIN; TMEFF2 PROTEIN; TRANSCRIPTION FACTOR GATA 4; TUMOR MARKER; UNCLASSIFIED DRUG; UNINDEXED DRUG; VIMENTIN; WNT5A PROTEIN;

CANCER CLASSIFICATION; CANCER DIAGNOSIS; CANCER GENETICS; CANCER PROGNOSIS; CANCER SCREENING; CANCER STAGING; CANCER SURGERY; CANCER SURVIVAL; CARCINOGENESIS; COLONOSCOPY; COLORECTAL CANCER; CPG ISLAND; DNA METHYLATION; EARLY DIAGNOSIS; GENE STRUCTURE; GENETIC ASSOCIATION; HUMAN; OCCULT BLOOD TEST; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REVIEW; SENSITIVITY AND SPECIFICITY; TUMOR LOCALIZATION;

COLORECTAL NEOPLASMS; CPG ISLANDS; DNA METHYLATION; EARLY DETECTION OF CANCER; HUMANS; PREDICTIVE VALUE OF TESTS; PROGNOSIS; PROMOTER REGIONS, GENETIC; TUMOR MARKERS, BIOLOGICAL;

EID: 84859188168     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.12.9     Document Type: Review

References (160)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J. Clin. 59(4), 225-249 (2009).
2. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer 127(12), 2893-2917 (2010).
3. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J. Clin. 61(2), 69-90 (2011).
4. Morris EJ, Maughan NJ, Forman D, Quirke P. Who to treat with adjuvant therapy in Dukes B/stage II colorectal cancer? The need for high quality pathology. Gut 56(10), 1419-1425 (2007).
5. Jass JR. Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology 50(1), 113-130 (2007).
6. Hughes LA, Khalid-De Bakker CA, Smits KM et al. The CpG island methylator phenotype in colorectal cancer: progress and problems. Biochim. Biophys. Acta 1825(1), 77-85 (2012). Systematic review on the CpG island methylator phenotype.
7. George B, Kopetz S. Predictive and prognostic markers in colorectal cancer. Curr. Oncol. Rep. 13(3), 206-215 (2011).
8. Mutch MG. Molecular profiling and risk stratification of adenocarcinoma of the colon. J. Surg. Oncol. 96(8), 693-703 (2007).
9. Walther A, Johnstone E, Swanton C, Midgley R, Tomlinson I, Kerr D. Genetic prognostic and predictive markers in colorectal cancer. Nat. Rev. Cancer 9(7), 489-499 (2009).
10. Kondo Y, Issa JP. Epigenetic changes in colorectal cancer. Cancer Metastasis Rev. 23(1-2), 29-39 (2004).
11. Chan TA, Glockner S, Yi JM et al. Convergence of mutation and epigenetic alterations identifies common genes in cancer that predict for poor prognosis. PLoS Med. 5(5), e114 (2008).
12. Smits KM, Cleven a H, Weijenberg MP et al. Pharmacoepigenomics in colorectal cancer: a step forward in predicting prognosis and treatment response. Pharmacogenomics 9(12), 1903-1916 (2008).
13. Bock C. Epigenetic biomarker development. Epigenomics 1(1), 99-110 (2009). Review outlining a systematic approach to epigenetic biomarker development.
14. Esteller M, Fraga MF, Guo M et al. DNA methylation patterns in hereditary human cancers mimic sporadic tumorigenesis. Hum. Mol. Genet. 10(26), 3001-3007 (2001).
15. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N. Engl. J. Med. 349(21), 2042-2054 (2003).
16. Van Engeland M, Derks S, Smits KM, Meijer GA, Herman JG. Colorectal cancer epigenetics: complex simplicity. J. Clin. Oncol. 29(10), 1382-1391 (2011). Review providing a comprehensive overview on colorectal cancer (CRC) epigenetics.
17. Takai D, Jones PA. Comprehensive ana lysis of CpG islands in human chromosomes 21 and 22. Proc. Natl Acad. Sci. USA 99(6), 3740-3745 (2002).
18. Vucic EA, Brown CJ, Lam WL. Epigenetics of cancer progression. Pharmacogenomics 9(2), 215-234 (2008).
19. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99(3), 247-257 (1999).
20. Esteller M. Epigenetic gene silencing in cancer: the DNA hypermethylome. Hum. Mol. Genet. 16(Spec No 1), R50-R59 (2007).
21. Jost JP, Bruhat A. The formation of DNA methylation patterns and the silencing of genes. Prog. Nucleic Acid Res. Mol. Biol. 57, 217-248 (1997).
22. Kim H, Park J, Jung Y et al. DNA methyltransferase 3-like affects promoter methylation of thymine DNA glycosylase independently of DNMT1 and DNMT3B in cancer cells. Int. J. Oncol. 36(6), 1563-1572 (2010).
23. Turker MS, Bestor TH. Formation of methylation patterns in the mammalian genome. Mutat. Res. 386(2), 119-130 (1997).
24. Merlo A, Herman JG, Mao L et al. 5′ CpG island methylation is associated with transcriptional silencing of the tumour suppressor p16/CDKN2/MTS1 in human cancers. Nat. Med. 1(7), 686-692 (1995).
25. Baylin SB, Herman JG, Graff JR, Vertino PM, Issa JP. Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv. Cancer Res. 72, 141-196 (1998).
26. Bird A. The essentials of DNA methylation. Cell 70(1), 5-8 (1992).
27. Costello JF, Fruhwald MC, Smiraglia DJ et al. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat. Genet. 24(2), 132-138 (2000).
28. Esteller M. CpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future. Oncogene 21(35), 5427-5440 (2002).
29. Irizarry RA, Ladd-Acosta C, Wen B et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat. Genet. 41(2), 178-186 (2009).
30. Doi A, Park IH, Wen B et al. Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat. Genet. 41(12), 1350-1353 (2009).
31. Lopez-Serra L, Esteller M. Proteins that bind methylated DNA and human cancer: reading the wrong words. Br. J. Cancer 98(12), 1881-1885 (2008).
32. Kuroda A, Rauch TA, Todorov I et al. Insulin gene expression is regulated by DNA methylation. PLoS ONE 4(9), e6953 (2009).
33. Hoque MO, Kim MS, Ostrow KL et al. Genome-wide promoter ana lysis uncovers portions of the cancer methylome. Cancer Res. 68(8), 2661-2670 (2008).
34. Momparler RL. Cancer epigenetics. Oncogene 22(42), 6479-6483 (2003).
35. Sharma S, Kelly TK, Jones PA. Epigenetics in cancer. Carcinogenesis 31(1), 27-36 (2010).
36. Issa JP. CpG island methylator phenotype in cancer. Nat. Rev. Cancer 4(12), 988-993 (2004).
37. Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP. CpG island methylator phenotype in colorectal cancer. Proc. Natl Acad. Sci. USA 96(15), 8681-8686 (1999).
38. Tanaka N, Huttenhower C, Nosho K et al. Novel application of structural equation modeling to correlation structure ana lysis of CpG island methylation in colorectal cancer. Am. J. Pathol. 177(6), 2731-2740 (2010).
39. Weisenberger DJ, Siegmund KD, Campan M et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat. Genet. 38(7), 787-793 (2006).
40. Park SJ, Rashid A, Lee JH, Kim SG, Hamilton SR, Wu TT. Frequent CpG island methylation in serrated adenomas of the colorectum. Am. J. Pathol. 162(3), 815-822 (2003).
41. Ogino S, Cantor M, Kawasaki T et al. CpG island methylator phenotype (CIMP) of colorectal cancer is best characterised by quantitative DNA methylation ana lysis and prospective cohort studies. Gut 55(7), 1000-1006 (2006).
42. Shen L, Toyota M, Kondo Y et al. Integrated genetic and epigenetic ana lysis identifies three different subclasses of colon cancer. Proc. Natl Acad. Sci. USA 104(47), 18654-18659 (2007).
43. Samowitz WS, Albertsen H, Herrick J et al. Evaluation of a large, population-based sample supports a CpG island methylator phenotype in colon cancer. Gastroenterology 129(3), 837-845 (2005).
44. Toyota M, Ohe-Toyota M, Ahuja N, Issa JP. Distinct genetic profiles in colorectal tumors with or without the CpG island methylator phenotype. Proc. Natl Acad. Sci. USA 97(2), 710-715 (2000).
45. Tainsky MA. Cancer biomarker discovery: speed-bumps and tire shredders. Cancer Biomark. 6(5-6), 225-227 (2010).
46. Issaq HJ, Waybright TJ, Veenstra TD. Cancer biomarker discovery: Opportunities and pitfalls in analytical methods. Electrophoresis 32(9), 967-975 (2011).
47. Crea F, Nobili S, Paolicchi E et al. Epigenetics and chemoresistance in colorectal cancer: an opportunity for treatment tailoring and novel therapeutic strategies. Drug Resist. Updat. 14(6), 280-296 (2011).
48. Naylor S. Biomarkers: current perspectives and future prospects. Expert Rev. Mol. Diagn. 3(5), 525-529 (2003).
49. Perera FP, Weinstein IB. Molecular epidemiology: recent advances and future directions. Carcinogenesis 21(3), 517-524 (2000).
50. Vineis P, Perera F. Molecular epidemiology and biomarkers in etiologic cancer research: the new in light of the old. Cancer Epidemiol. Biomarkers Prev. 16(10), 1954-1965 (2007).
51. Levin B, Lieberman DA, Mcfarland B et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology 134(5), 1570-1595 (2008).
52. Gatto NM, Frucht H, Sundararajan V, Jacobson JS, Grann VR, Neugut AI. Risk of perforation after colonoscopy and sigmoidoscopy: a population-based study. J. Natl Cancer Inst. 95(3), 230-236 (2003).
53. Frazier a L, Colditz GA, Fuchs CS, Kuntz KM. Cost-effectiveness of screening for colorectal cancer in the general population. JAMA 284(15), 1954-1961 (2000).
54. Imperiale TF, Ransohoff DF, Itzkowitz SH, Turnbull BA, Ross ME. Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average-risk population. N. Engl. J. Med. 351(26), 2704-2714 (2004).
55. Bosch LJ, Carvalho B, Fijneman RJ et al. Molecular tests for colorectal cancer screening. Clin. Colorectal Cancer 10(1), 8-23 (2011).
56. Chen WD, Han ZJ, Skoletsky J et al. Detection in fecal DNA of colon cancer-specific methylation of the nonexpressed vimentin gene. J. Natl Cancer Inst. 97(15), 1124-1132 (2005).
57. Itzkowitz S, Brand R, Jandorf L et al. A simplified, noninvasive stool DNA test for colorectal cancer detection. Am. J. Gastroenterol. 103(11), 2862-2870 (2008).
58. Itzkowitz SH, Jandorf L, Brand R et al. Improved fecal DNA test for colorectal cancer screening. Clin. Gastroenterol. Hepatol. 5(1), 111-117 (2007).
59. Li M, Chen WD, Papadopoulos N et al. Sensitive digital quantification of DNA methylation in clinical samples. Nat. Biotechnol. 27(9), 858-863 (2009).
60. Ahlquist DA, Skoletsky JE, Boynton KA et al. Colorectal cancer screening by detection of altered human DNA in stool: feasibility of a multitarget assay panel. Gastroenterology 119(5), 1219-1227 (2000).
61. Ned RM, Melillo S, Marrone M. Fecal DNA testing for colorectal cancer screening: the ColoSure™ test. PLoS Curr. 3, RRN1220 (2011).
62. Huang Z, Li L, Wang J. Hypermethylation of SFRP2 as a potential marker for stool-based detection of colorectal cancer and precancerous lesions. Dig. Dis. Sci. 52(9), 2287-2291 (2007).
63. Wang DR, Tang D. Hypermethylated SFRP2 gene in fecal DNA is a high potential biomarker for colorectal cancer noninvasive screening. World J. Gastroenterol. 14(4), 524-531 (2008).
64. Oberwalder M, Zitt M, Wontner C et al. SFRP2 methylation in fecal DNA - a marker for colorectal polyps. Int. J. Colorectal Dis. 23(1), 15-19 (2008).
65. Nagasaka T, Tanaka N, Cullings HM et al. Analysis of fecal DNA methylation to detect gastrointestinal neoplasia. J. Natl Cancer Inst. 101(18), 1244-1258 (2009).
66. Zhang W, Bauer M, Croner RS et al. DNA stool test for colorectal cancer: hypermethylation of the secreted frizzled-related protein-1 gene. Dis. Colon Rectum 50(10), 1618-1626; discussion 1626-1617 (2007).
67. Lenhard K, Bommer GT, Asutay S et al. Analysis of promoter methylation in stool: a novel method for the detection of colorectal cancer. Clin. Gastroenterol. Hepatol. 3(2), 142-149 (2005).
68. Petko Z, Ghiassi M, Shuber A et al. Aberrantly methylated CDKN2A, MGMT, and MLH1 in colon polyps and in fecal DNA from patients with colorectal polyps. Clin. Cancer Res. 11(3), 1203-1209 (2005).
69. Leung WK, To KF, Man EP et al. Detection of hypermethylated DNA or cyclooxygenase-2 messenger RNA in fecal samples of patients with colorectal cancer or polyps. Am. J. Gastroenterol. 102(5), 1070-1076 (2007).
70. Melotte V, Lentjes MH, Van Den Bosch SM et al. N-Myc downstream-regulated gene 4 (NDRG4): a candidate tumor suppressor gene and potential biomarker for colorectal cancer. J. Natl Cancer Inst. 101(13), 916-927 (2009).
71. Hellebrekers DM, Lentjes MH, Van Den Bosch SM et al. GATA4 and GATA5 are potential tumor suppressors and biomarkers in colorectal cancer. Clin. Cancer Res. 15(12), 3990-3997 (2009).
72. Glöckner SC, Dhir M, Yi JM et al. Methylation of TFPI2 in stool DNA: a potential novel biomarker for the detection of colorectal cancer. Cancer Res. 69(11), 4691-4699 (2009).
73. Kim MS, Louwagie J, Carvalho B et al. Promoter DNA methylation of oncostatin m receptor-beta as a novel diagnostic and therapeutic marker in colon cancer. PLoS ONE 4(8), e6555 (2009).
74. Bosch LJ, Oort FA, Neerincx M et al. DNA methylation of phosphatase and actin regulator 3 detects colorectal cancer in stool and complements FIT. Cancer Prev. Res. (Phila.) 5(3), 464-472 (2012). First study reporting a high sensitivity and specificity for the fecal immunochemical test in combination with a methylation marker in fecal DNA for early detection of CRC.
75. Ahlquist DA, Zou H, Domanico M et al. Next-generation stool DNA test accurately detects colorectal cancer or large adenomas. Gastroenterology 142(2), 248-256 (2011). Reports high sensitivity and specificity of a methylation marker panel in fecal DNA for the early detection of CRC.
76. Leung WK, To KF, Man EP et al. Quantitative detection of promoter hypermethylation in multiple genes in the serum of patients with colorectal cancer. Am. J. Gastroenterol. 100(10), 2274-2279 (2005).
77. Ebert MP, Model F, Mooney S et al. Aristaless-like homeobox-4 gene methylation is a potential marker for colorectal adenocarcinomas. Gastroenterology 131(5), 1418-1430 (2006).
78. Lofton-Day C, Model F, Devos T et al. DNA methylation biomarkers for blood-based colorectal cancer screening. Clin. Chem. 54(2), 414-423 (2008).
79. Herbst A, Rahmig K, Stieber P et al. Methylation of NEUROG1 in serum is a sensitive marker for the detection of early colorectal cancer. Am. J. Gastroenterol. 106(6), 1110-1118 (2011).
80. Devos T, Tetzner R, Model F et al. Circulating methylated SEPT9 DNA in plasma is a biomarker for colorectal cancer. Clin. Chem. 55(7), 1337-1346 (2009).
81. Payne SR. From discovery to the clinic: the novel DNA methylation biomarker (m)SEPT9 for the detection of colorectal cancer in blood. Epigenomics 2(4), 575-585 (2010).
82. Tanzer M, Balluff B, Distler J et al. Performance of epigenetic markers SEPT9 and ALX4 in plasma for detection of colorectal precancerous lesions. PLoS ONE 5(2), e9061 (2010).
83. Warren JD, Xiong W, Bunker a M et al. Septin 9 methylated DNA is a sensitive and specific blood test for colorectal cancer. BMC Med. 9(1), 133 (2011).
84. Tang D, Liu J, Wang DR, Yu HF, Li YK, Zhang JQ. Diagnostic and prognostic value of the methylation status of secreted frizzled-related protein 2 in colorectal cancer. Clin. Invest. Med. 34(2), E88-E95 (2011).
85. Ahlquist DA, Taylor WR, Mahoney DW et al. The stool DNA test is more accurate than the plasma septin 9 test in detecting colorectal neoplasia. Clin. Gastroenterol. Hepatol. 10(3), 272-277 (2012).
86. Deschoolmeester V, Baay M, Specenier P, Lardon F, Vermorken JB. A review of the most promising biomarkers in colorectal cancer: one step closer to targeted therapy. Oncologist 15(7), 699-731 (2010).
87. Graziano F, Cascinu S. Prognostic molecular markers for planning adjuvant chemotherapy trials in Dukes' B colorectal cancer patients: how much evidence is enough? Ann. Oncol. 14(7), 1026-1038 (2003).
88. Klump B, Nehls O, Okech T et al. Molecular lesions in colorectal cancer: impact on prognosis? Original data and review of the literature. Int. J. Colorectal Dis. 19(1), 23-42 (2004).
89. Belt EJ, Van Stijn MF, Bril H et al. Lymph node negative colorectal cancers with isolated tumor deposits should be classified and treated as stage III. Ann. Surg. Oncol. 17(12), 3203-3211 (2010).
90. George S, Primrose J, Talbot R et al. Will Rogers revisited: prospective observational study of survival of 3592 patients with colorectal cancer according to number of nodes examined by pathologists. Br. J. Cancer 95(7), 841-847 (2006).
91. Nosho K, Baba Y, Tanaka N et al. Tumour-infiltrating T-cell subsets, molecular changes in colorectal cancer, and prognosis: cohort study and literature review. J. Pathol. 222(4), 350-366 (2010).
92. Prall F, Nizze H, Barten M. Tumour budding as prognostic factor in stage I/II colorectal carcinoma. Histopathology 47(1), 17-24 (2005).
93. Pritchard CC, Grady WM. Colorectal cancer molecular biology moves into clinical practice. Gut 60(1), 116-129 (2011).
94. Fretwell VL, Ang CW, Tweedle EM, Rooney PS. The impact of lymph node yield on Duke's B and C colorectal cancer survival. Colorectal Dis. 12(10), 995-1000 (2010).
95. Chau I, Allen MJ, Cunningham D et al. The value of routine serum carcinoembryonic antigen measurement and computed tomography in the surveillance of patients after adjuvant chemotherapy for colorectal cancer. J. Clin. Oncol. 22(8), 1420-1429 (2004).
96. Oussoultzoglou E, Rosso E, Fuchshuber P et al. Perioperative carcinoembryonic antigen measurements to predict curability after liver resection for colorectal metastases: a prospective study. Arch. Surg. 143(12), 1150-1158; discussion 1158-1159 (2008).
97. Tan E, Gouvas N, Nicholls RJ, Ziprin P, Xynos E, Tekkis PP. Diagnostic precision of carcinoembryonic antigen in the detection of recurrence of colorectal cancer. Surg. Oncol. 18(1), 15-24 (2009).
98. Kelley RK, Venook a P. Prognostic and predictive markers in stage II colon cancer: is there a role for gene expression profiling? Clin. Colorectal Cancer 10(2), 73-80 (2011).
99. Umetani N, Takeuchi H, Fujimoto A, Shinozaki M, Bilchik a J, Hoon DS. Epigenetic inactivation of ID4 in colorectal carcinomas correlates with poor differentiation and unfavorable prognosis. Clin. Cancer Res. 10(22), 7475-7483 (2004).
100. Tanaka M, Chang P, Li Y et al. Association of CHFR promoter methylation with disease recurrence in locally advanced colon cancer. Clin. Cancer Res. 17(13), 4531-4540 (2011).
101. Krtolica K, Krajnovic M, Usaj-Knezevic S, Babic D, Jovanovic D, Dimitrijevic B. Comethylation of p16 and MGMT genes in colorectal carcinoma: correlation with clinicopathological features and prognostic value. World J. Gastroenterol. 13(8), 1187-1194 (2007).
102. Whitehall VL, Walsh MD, Young J, Leggett BA, Jass JR. Methylation of O-6- methylguanine DNA methyltransferase characterizes a subset of colorectal cancer with low-level DNA microsatellite instability. Cancer Res. 61(3), 827-830 (2001).
103. Xu XL, Yu J, Zhang HY et al. Methylation profile of the promoter CpG islands of 31 genes that may contribute to colorectal carcinogenesis. World J. Gastroenterol. 10(23), 3441-3454 (2004).
104. Ogino S, Nosho K, Kirkner GJ et al. CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut 58(1), 90-96 (2009).
105. Shima K, Morikawa T, Baba Y et al. MGMT promoter methylation, loss of expression and prognosis in 855 colorectal cancers. Cancer Causes Control 22(2), 301-309 (2011).
106. Kohonen-Corish MR, Daniel JJ, Chan C et al. Low microsatellite instability is associated with poor prognosis in stage C colon cancer. J. Clin. Oncol. 23(10), 2318-2324 (2005).
107. Mokarram P, Kumar K, Brim H et al. Distinct high-profile methylated genes in colorectal cancer. PLoS ONE 4(9), e7012 (2009).
108. Yi JM, Dhir M, Van Neste L et al. Genomic and epigenomic integration identifies a prognostic signature in colon cancer. Clin. Cancer Res. 17(6), 1535-1545 (2011).
109. Ahn JB, Chung WB, Maeda O et al. DNA methylation predicts recurrence from resected stage III proximal colon cancer. Cancer 117(9), 1847-1854 (2011).
110. Ward RL, Cheong K, Ku SL, Meagher A, O'connor T, Hawkins NJ. Adverse prognostic effect of methylation in colorectal cancer is reversed by microsatellite instability. J. Clin. Oncol. 21(20), 3729-3736 (2003). First study reporting a prognostic significance for CpG island methylation phenotype in microsatellite-stable CRC patients.
111. Barault L, Charon-Barra C, Jooste V et al. Hypermethylator phenotype in sporadic colon cancer: study on a population-based series of 582 cases. Cancer Res. 68(20), 8541-8546 (2008). First population-based study investigating the prognostic relevance of CpG island methylator phenotype in three subgroups.
112. Saltz LB, Niedzwiecki D, Hollis D et al. Irinotecan fluorouracil plus leucovorin is not superior to fluorouracil plus leucovorin alone as adjuvant treatment for stage III colon cancer: results of CALGB 89803. J. Clin. Oncol. 25(23), 3456-3461 (2007).
113. Edwards MS, Chadda SD, Zhao Z, Barber BL, Sykes DP. A systematic review of treatment guidelines for metastatic colorectal cancer. Colorectal Dis. 14(2), e31-e47 (2012).
114. Goldberg RM. Therapy for metastatic colorectal cancer. Oncologist 11(9), 981-987 (2006).
115. Tejpar S, Bertagnolli M, Bosman F et al. Prognostic and predictive biomarkers in resected colon cancer: current status and future perspectives for integrating genomics into biomarker discovery. Oncologist 15(4), 390-404 (2010).
116. Simon R. Development and validation of biomarker classifiers for treatment selection. J. Stat. Plan. Inference 138(2), 308-320 (2008).
117. Amado RG, Wolf M, Peeters M et al. Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer. J. Clin. Oncol. 26(10), 1626-1634 (2008).
118. Di Fiore F, Blanchard F, Charbonnier F et al. Clinical relevance of KRAS mutation detection in metastatic colorectal cancer treated by Cetuximab plus chemotherapy. Br. J. Cancer 96(8), 1166-1169 (2007).
119. Lievre A, Bachet JB, Le Corre D et al. KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Res. 66(8), 3992-3995 (2006).
120. Boland CR, Goel A. Microsatellite instability in colorectal cancer. Gastroenterology 138(6), 2073-2087.e3 (2010).
121. Des Guetz G, Schischmanoff O, Nicolas P, Perret GY, Morere JF, Uzzan B. Does microsatellite instability predict the efficacy of adjuvant chemotherapy in colorectal cancer? A systematic review with meta-analysis. Eur. J. Cancer 45(10), 1890-1896 (2009).
122. Bertagnolli MM, Niedzwiecki D, Compton CC et al. Microsatellite instability predicts improved response to adjuvant therapy with irinotecan, fluorouracil, and leucovorin in stage III colon cancer: Cancer and Leukemia Group B Protocol 89803. J. Clin. Oncol. 27(11), 1814-1821 (2009).
123. Fallik D, Borrini F, Boige V et al. Microsatellite instability is a predictive factor of the tumor response to irinotecan in patients with advanced colorectal cancer. Cancer Res. 63(18), 5738-5744 (2003).
124. Popat S, Hubner R, Houlston RS. Systematic review of microsatellite instability and colorectal cancer prognosis. J. Clin. Oncol. 23(3), 609-618 (2005).
125. Ogino S, Meyerhardt JA, Kawasaki T et al. CpG island methylation, response to combination chemotherapy, and patient survival in advanced microsatellite stable colorectal carcinoma. Virchows Arch. 450(5), 529-537 (2007).
126. Shen L, Catalano PJ, Benson AB 3rd, O'Dwyer P, Hamilton SR, Issa JP. Association between DNA methylation and shortened survival in patients with advanced colorectal cancer treated with 5-fluorouracil based chemotherapy. Clin. Cancer Res. 13(20), 6093-6098 (2007).
127. Jover R, Nguyen TP, Perez-Carbonell L et al. 5-fluorouracil adjuvant chemotherapy does not increase survival in patients with CpG island methylator phenotype colorectal cancer. Gastroenterology 140(4), 1174-1181 (2011).
128. Esteller M, Herman JG. Generating mutations but providing chemosensitivity: the role of O6-methylguanine DNA methyltransferase in human cancer. Oncogene 23(1), 1-8 (2004).
129. Jacinto FV, Esteller M. MGMT hypermethylation: a prognostic foe, a predictive friend. DNA Repair (Amst.) 6(8), 1155-1160 (2007).
130. Agrelo R, Cheng WH, Setien F et al. Epigenetic inactivation of the premature aging Werner syndrome gene in human cancer. Proc. Natl Acad. Sci. USA 103(23), 8822-8827 (2006).
131. Kawasaki T, Ohnishi M, Suemoto Y et al. WRN promoter methylation possibly connects mucinous differentiation, microsatellite instability and CpG island methylator phenotype in colorectal cancer. Mod. Pathol. 21(2), 150-158 (2008).
132. Laird PW. The power and the promise of DNA methylation markers. Nat. Rev. Cancer 3(4), 253-266 (2003).
133. Shivapurkar N, Gazdar a F. DNA methylation based biomarkers in non-invasive cancer screening. Curr. Mol. Med. 10(2), 123-132 (2010).
134. Esteller M, Sanchez-Cespedes M, Rosell R, Sidransky D, Baylin SB, Herman JG. Detection of aberrant promoter hypermethylation of tumor suppressor genes in serum DNA from non-small cell lung cancer patients. Cancer Res. 59(1), 67-70 (1999).
135. Bailey VJ, Easwaran H, Zhang Y et al. MS-qFRET: a quantum dot-based method for ana lysis of DNA methylation. Genome Res. 19(8), 1455-1461 (2009).
136. Rifai N, Gillette MA, Carr SA. Protein biomarker discovery and validation: the long and uncertain path to clinical utility. Nat. Biotechnol. 24(8), 971-983 (2006).
137. Jeddeloh JA, Greally JM, Rando OJ. Reduced-representation methylation mapping. Genome Biol. 9(8), 231 (2008).
138. Oda M, Glass JL, Thompson RF et al. High-resolution genome-wide cytosine methylation profiling with simultaneous copy number ana lysis and optimization for limited cell numbers. Nucleic Acids Res. 37(12), 3829-3839 (2009).
139. Kibriya MG, Raza M, Jasmine F et al. A genome-wide DNA methylation study in colorectal carcinoma. BMC Med. Genomics 4, 50 (2011).
140. 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 93(18), 9821-9826 (1996).
141. Eads CA, Danenberg KD, Kawakami K et al. MethyLight: a high-throughput assay to measure DNA methylation. Nucleic Acids Res. 28(8), E32 (2000).
142. Tost J, Gut IG. DNA methylation ana lysis by pyrosequencing. Nat. Protoc. 2(9), 2265-2275 (2007).
143. Gonzalgo ML, Liang G. Methylation-sensitive single-nucleotide primer extension (Ms-SNuPE) for quantitative measurement of DNA methylation. Nat. Protoc. 2(8), 1931-1936 (2007).
144. Brena RM, Auer H, Kornacker K, Plass C. Quantification of DNA methylation in electrofluidics chips (Bio-COBRA). Nat. Protoc. 1(1), 52-58 (2006).
145. Ehrich M, Nelson MR, Stanssens P et al. Quantitative high-throughput ana lysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc. Natl Acad. Sci. USA 102(44), 15785-15790 (2005).
146. Van Vlodrop IJ, Niessen HE, Derks S et al. Analysis of promoter CpG island hypermethylation in cancer: location, location, location! Clin. Cancer Res. 17(13), 4225-4231 (2011).
147. Mischak H, Allmaier G, Apweiler R et al. Recommendations for biomarker identification and qualification in clinical proteomics. Sci. Transl. Med. 2(46), 46ps42 (2010).
148. Dancey JE, Dobbin KK, Groshen S et al. Guidelines for the development and incorporation of biomarker studies in early clinical trials of novel agents. Clin. Cancer Res. 16(6), 1745-1755 (2010).
149. Williams SA, Slavin DE, Wagner JA, Webster CJ. A cost-effectiveness approach to the qualification and acceptance of biomarkers. Nat. Rev. Drug Discov. 5(11), 897-902 (2006).
150. Sawyers CL. The cancer biomarker problem. Nature 452(7187), 548-552 (2008).
151. Diamandis EP. Cancer biomarkers: can we turn recent failures into success? J. Natl Cancer Inst. 102(19), 1462-1467 (2010).
152. Luo YX, Chen DK, Song SX, Wang L, Wang JP. Aberrant methylation of genes in stool samples as diagnostic biomarkers for colorectal cancer or adenomas: a meta-analysis. Int. J. Clin. Pract. 65(12), 1313-1320 (2011).
153. Hopewell S, Loudon K, Clarke MJ, Oxman a D, Dickersin K. Publication bias in clinical trials due to statistical significance or direction of trial results. Cochrane Database Syst. Rev. 1, MR000006 (2009).
154. Ioannidis JP, Trikalinos TA. An exploratory test for an excess of significant findings. Clin. Trials 4(3), 245-253 (2007).
155. Kyzas PA, Loizou KT, Ioannidis JP. Selective reporting biases in cancer prognostic factor studies. J. Natl Cancer Inst. 97(14), 1043-1055 (2005).
156. Debauve G, Capouillez A, Belayew A, Saussez S. The helicase-like transcription factor and its implication in cancer progression. Cell. Mol. Life Sci. 65(4), 591-604 (2008).
157. Mccart a E, Vickaryous NK, Silver A. Apc mice: models, modifiers and mutants. Pathol. Res. Pract. 204(7), 479-490 (2008).
158. Mohammad HP, Zhang W, Prevas HS et al. Loss of a single Hic1 allele accelerates polyp formation in Apc(Delta716) mice. Oncogene 30(23), 2659-2669 (2011).
159. Wales MM, Biel MA, El Deiry W et al. p53 activates expression of HIC-1, a new candidate tumour suppressor gene on 17p13.3. Nat. Med. 1(6), 570-577 (1995).
160. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM. REporting recommendations for tumor MARKer prognostic studies (REMARK). Nat. Clin. Pract. Oncol. 2(8), 416-422 (2005).