CHFR promoter methylation indicates poor prognosis in stage II microsatellite stable colorectal cancer

Clinical Cancer Research

Volumn 20, Issue 12, 2014, Pages 3261-3271

  Cleven, Arjen H G ^a   Derks, Sarah ^a   Draht, Muriel X G ^a   Smits, Kim M ^a   Melotte, Veerle ^a   Van Neste, Leander ^a   Tournier, Benjamin ^b   Jooste, Valerie ^c   Chapusot, Caroline ^b   Weijenberg, Matty P ^a   Herman, James G ^d   De Bruïne, Adriaan P ^a   Van Engeland, Manon ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b Service de Pathologie   (France)

^c UNIVERSITÉ DE BOURGOGNE   (France)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; K RAS PROTEIN; MICROSATELLITE DNA; CELL CYCLE PROTEIN; CHFR PROTEIN, HUMAN; TUMOR PROTEIN;

AGED; ARTICLE; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CODON; COLORECTAL CANCER; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA REPAIR; EXON; FEMALE; GENE CLUSTER; GENE MUTATION; HUMAN; MAJOR CLINICAL STUDY; MALE; METHYLATION; MICROSATELLITE INSTABILITY; ONCOGENE K RAS; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; TUMOR SUPPRESSOR GENE; WILD TYPE; COLORECTAL TUMOR; FOLLOW UP; GENE EXPRESSION REGULATION; GENETICS; MIDDLE AGED; MORTALITY; MUTATION; PATHOLOGY; PROGNOSIS; PROSPECTIVE STUDY; SURVIVAL RATE;

AGED; CELL CYCLE PROTEINS; COLORECTAL NEOPLASMS; CPG ISLANDS; DNA METHYLATION; FEMALE; FOLLOW-UP STUDIES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; MUTATION; NEOPLASM PROTEINS; NEOPLASM STAGING; PHENOTYPE; PROGNOSIS; PROMOTER REGIONS, GENETIC; PROSPECTIVE STUDIES; SURVIVAL RATE;

EID: 84902665588     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-3734     Document Type: Article

References (62)

1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70. (Pubitemid 30046295)
2. Schuebel KE, Chen W, Cope L, Glockner SC, Suzuki H, Yi JM, et al. Comparing the DNA hypermethylome with gene mutations in human colorectal cancer. PLoS Genet 2007;3:1709-23. (Pubitemid 47510263)
3. Sjoblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, et al. The consensus coding sequences of human breast and colorectal cancers. Science 2006;314:268-74. (Pubitemid 44571966)
4. Wood LD, Parsons DW, Jones S, Lin J, Sjoblom T, Leary RJ, et al. The genomic landscapes of human breast and colorectal cancers. Science 2007;318:1108-13. (Pubitemid 350134889)
5. van Engeland M, Derks S, Smits KM, Meijer GA, Herman JG. Colorectal cancer epigenetics: complex simplicity. J Clin Oncol 2011;29:1382-91.
6. Ogino S, Cantor M, Kawasaki T, Brahmandam M, Kirkner GJ, Weisenberger DJ, et al. CpG island methylator phenotype (CIMP) of colorectal cancer is best characterised by quantitative DNA methylation analysis and prospective cohort studies. Gut 2006;55:1000-6. (Pubitemid 43962613)
7. Ogino S, Kawasaki T, Kirkner GJ, Kraft P, Loda M, Fuchs CS. Evaluation of markers for CpG island methylator phenotype (CIMP) in colorectal cancer by a large population-based sample. J Mol Diagnostics 2007;9:305-14. (Pubitemid 47305066)
8. Samowitz WS, Albertsen H, Herrick J, Levin TR, Sweeney C, Murtaugh MA, et al. Evaluation of a large, population-based sample supports a CpG island methylator phenotype in colon cancer. Gastroenterology 2005;129:837-45. (Pubitemid 41242676)
9. Shen L, Toyota M, Kondo Y, Lin E, Zhang L, Guo Y, et al.Integrated genetic and epigenetic analysis identifies three different subclasses of colon cancer. Proc Natl Acad Sci U S A 2007;104:18654-9. (Pubitemid 350210752)
10. Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci U S A 1999;96:8681-6. (Pubitemid 29354851)
11. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nature Genet 2006;38:787-93. (Pubitemid 43980599)
12. Hughes LA, Khalid-de Bakker CA, Smits KM, van den Brandt PA, Jonkers D, Ahuja N, et al. The CpG island methylator phenotype in colorectal cancer: progress and problems. Biochim Biophys Acta 2012;1825:77-85.
13. Ogino S, Meyerhardt JA, Kawasaki T, Clark JW, Ryan DP, Kulke MH, et al.CpGisland methylation, response to combination chemotherapy, and patient survival in advanced microsatellite stable colorectal carcinoma. Virchows Arch 2007;450:529-37. (Pubitemid 46676250)
14. Samowitz WS, Sweeney C, Herrick J, Albertsen H, Levin TR, Murtaugh MA, et al. Poor survival associated with the BRAF V600E mutation in microsatellite-stable colon cancers. Cancer Res 2005;65:6063-9.
15. Shen L, Catalano PJ, Benson ABIII, 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 2007;13:6093-8. (Pubitemid 350075067)
16. Ogino S, Nosho K, Kirkner GJ, Kawasaki T, Meyerhardt JA, Loda M, et al. CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut 2009;58:90-6.
17. Hughes LA, Melotte V, de Schrijver J, de Maat M, Smit VT, Bovee JV, et al. The CpG island methylator phenotype: what's in a name? Cancer Res 2013;73:5858-68.
18. Wiggers T, Jeekel J, Arends JW, Brinkhorst AP, Kluck HM, Luyk CI, et al. No-touch isolation technique in colon cancer: a controlled prospective trial. Br J Surg 1988;75:409-15.
19. Wiggers T, Arends JW, Volovics A. Regression analysis of prognostic factors in colorectal cancer after curative resections. Dis Colon Rectum 1988;31:33-41. (Pubitemid 18045232)
20. Van den Brandt PA, Schouten LJ, Goldbohm RA, Dorant E, HunenPM. Development of a record linkage protocol for use in the Dutch Cancer Registry for Epidemiological Research. Int J Epidemiol 1990;19:553-8. (Pubitemid 20331799)
21. de Vogel S, Wouters KA, Gottschalk RW, van Schooten FJ, de Goeij AF, de Bruine AP, et al. Genetic variants of methyl metabolizing enzymes and epigenetic regulators: associations with promoter CpG island hypermethylation in colorectal cancer. Cancer Epidemiol Biomark Prev 2009;18:3086-96.
22. Choi JS, Kim KH, Jeon YK, Kim SH, Jang SG, Ku JL, et al. Promoter hypermethylation of the ADAM23 gene in colorectal cancer cell lines and cancer tissues. Int J Cancer J Int du Cancer 2009;124:1258-62.
23. Wanajo A, Sasaki A, Nagasaki H, Shimada S, Otsubo T, Owaki S, et al. Methylation of the calcium channel-related gene, CACNA2D3, is frequent and a poor prognostic factor in gastric cancer. Gastroenterology 2008;135:580-90.
24. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novelPCRassay for methylation status of CpGislands. Proc Natl Acad Sci U S A 1996;93:9821-6. (Pubitemid 26296693)
25. Derks S, Lentjes MH, Hellebrekers DM, de Bruine AP, Herman JG, van Engeland M. Methylation-specific PCR unraveled. Cell Oncol 2004;26:291-9.
26. Suraweera N, Duval A, Reperant M, Vaury C, Furlan D, Leroy K, et al. Evaluation of tumor microsatellite instability using five quasimonomorphic mononucleotide repeats and pentaplex PCR. Gastroenterology 2002;123:1804-11. (Pubitemid 35408304)
27. Luchtenborg M, Weijenberg MP, Wark PA, Saritas AM, Roemen GM, van Muijen GN, et al. Mutations in APC, CTNNB1 and K-ras genes and expression of hMLH1 in sporadic colorectal carcinomas from the Netherlands Cohort Study. BMC Cancer 2005;5:160.
28. Sieben NL, Roemen GM, Oosting J, Fleuren GJ, van Engeland M, Prat J. Clonal analysis favours a monoclonal origin for serous borderline tumours with peritoneal implants. J Pathol 2006;210:405-11. (Pubitemid 44830600)
29. Carlis J, Bruso K. How many clusters to report: a recursive heuristic. Conference proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society; 2010:1069-72.
30. Kaushal D, Naeve CW. Loading and preparing data for analysis in spotfire. Curr Protoc Bioinformatics 2004;Chapter 7:Unit 7 8.
31. Worthley DL, Whitehall VL, Spring KJ, Leggett BA. Colorectal carcinogenesis: road maps to cancer. World J Gastroenterol 2007;13:3784-91. (Pubitemid 47272303)
32. Kawasaki T, Ohnishi M, Nosho K, Suemoto Y, Kirkner GJ, Meyerhardt JA, et al. CpG island methylator phenotype-low (CIMP-low) colorectal cancer shows not only few methylated CIMP-high-specific CpG islands, but also low-level methylation at individual loci. Mod Pathol 2008;21:245-55. (Pubitemid 351304277)
33. Lee S, Cho NY, Choi M, Yoo EJ, Kim JH, Kang GH. Clinicopathological features of CpG island methylator phenotype-positive colorectal cancer and its adverse prognosis in relation to KRAS/BRAF mutation. Pathol Int 2008;58:104-13.
34. Derks S, Postma C, Carvalho B, van den Bosch SM, Moerkerk PT, Herman JG, et al. Integrated analysis of chromosomal, microsatellite and epigenetic instability in colorectal cancer identifies specific associations between promoter methylation of pivotal tumour suppressor and DNA repair genes and specific chromosomal alterations. Carcinogenesis 2008;29:434-9. (Pubitemid 351359685)
35. Ogino S, Kawasaki T, Kirkner GJ, Loda M, Fuchs CS. CpG island methylator phenotype-low (CIMP-low) in colorectal cancer: possible associations with male sex and KRAS mutations. J Mol diagnostics; 8:582- 8.
36. Hinoue T, Weisenberger DJ, Lange CP, Shen H, Byun HM, Van Den Berg D, et al. Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res 2012;22:271-82.
37. Popat S, Hubner R, Houlston RS. Systematic review of microsatellite instability and colorectal cancer prognosis. J Clin Oncol 2005;23:609-18. (Pubitemid 46224239)
38. Zlobec I, Kovac M, Erzberger P, Molinari F, Bihl MP, Rufle A, et al. Combined analysis of specific KRAS mutation, BRAF and microsatellite instability identi fies prognostic subgroups of sporadic and hereditary colorectal cancer. Int J Cancer J int du Cancer 2010;127:2569-75.
39. Tanaka M, Chang P, Li Y, Li D, Overman M, Maru DM, et al. Association of CHFR promoter methylation with disease recurrence in locally advanced colon cancer. Clin Cancer Res 2011;17:4531-40.
40. Barault L, Charon-Barra C, Jooste V, de la Vega MF, Martin L, Roignot P, et al. Hypermethylator phenotype in sporadic colon cancer: study on a population-based series of 582 cases. Cancer Res 2008;68:8541-6.
41. Draht MXG, Smits KM, Tournier B, Jooste V, Chapusot C, Carvalho B, et al. Promoter CpG island methylation of RET predicts poor prognosis in stage II colorectal cancer patients. Mol Oncol. 2014 Feb 2. pii: S1574-7891(14)00025-8.
42. van Vlodrop IJ, Niessen HE, Derks S, Baldewijns MM, van Criekinge W, Herman JG, et al. Analysis of promoter CpG island hypermethylation in cancer: location, location, location! Clin Cancer Res 2011;17:4225-31.
43. 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 2003;21:3729-36. (Pubitemid 46606226)
44. Quinn E, Hawkins N, Yip YL, Suter C, Ward R. CD103+ intraepithelial lymphocytes-a unique population in microsatellite unstable sporadic colorectal cancer. Eur J Cancer 2003;39:469-75. (Pubitemid 36173691)
45. Lamlum H, Ilyas M, Rowan A, Clark S, Johnson V, Bell J, et al. The type of somatic mutation at APC in familial adenomatous polyposis is determined by the site of the germline mutation: a new facet to Knudson's 'two-hit' hypothesis. Nat Med 1999;5:1071-5. (Pubitemid 29439582)
46. Tomlinson I, Bodmer W. Selection, the mutation rate and cancer: ensuring that the tail does not wag the dog. Nat Med 1999;5:11-2. (Pubitemid 29050986)
47. Brandes JC, van Engeland M, Wouters KA, Weijenberg MP, Herman JG. CHFR promoter hypermethylation in colon cancer correlates with the microsatellite instability phenotype. Carcinogenesis 2005;26:1152-6. (Pubitemid 41214309)
48. Mizuno K, Osada H, Konishi H, Tatematsu Y, Yatabe Y, Mitsudomi T, et al. Aberrant hypermethylation of the CHFR prophase checkpoint gene in human lung cancers. Oncogene 2002;21:2328-33. (Pubitemid 34407292)
49. Shibata Y, Haruki N, Kuwabara Y, Ishiguro H, Shinoda N, Sato A, et al. Chfr expression is downregulated by CpG island hypermethylation in esophageal cancer. Carcinogenesis 2002;23:1695-9.
50. Corn PG, Summers MK, Fogt F, Virmani AK, Gazdar AF, Halazonetis TD, et al. Frequent hypermethylation of the 5′ CpG island of the mitotic stress checkpoint gene Chfr in colorectal and non-small cell lung cancer. Carcinogenesis 2003;24:47-51. (Pubitemid 36193194)
51. Satoh A, Toyota M, Itoh F, Sasaki Y, Suzuki H, Ogi K, et al. Epigenetic inactivation of CHFR and sensitivity to microtubule inhibitors in gastric cancer. Cancer Res 2003;63:8606-13. (Pubitemid 38064034)
52. Kang D, Chen J, Wong J, Fang G. The checkpoint protein Chfr is a ligase that ubiquitinates Plk1 and inhibits Cdc2 at the G2 to M transition. J Cell Biol 2002;156:249-59. (Pubitemid 34839907)
53. Scolnick DM, Halazonetis TD. Chfr de fines a mitotic stress checkpoint that delays entry into metaphase. Nature 2000;406:430-5. (Pubitemid 30625565)
54. Maddika S, Sy SM, Chen J. Functional interaction between Chfr and Kif22 controls genomic stability. J Biol Chem 2009;284:12998-3003.
55. Bertholon J, Wang Q, Falette N, Verny C, Auclair J, Chassot C, et al. Chfr inactivation is not associated to chromosomal instability in colon cancers. Oncogene 2003;22:8956-60. (Pubitemid 38021513)
56. Fu Z, Regan K, Zhang L, Muders MH, Thibodeau SN, French A, et al. Deficiencies in Chfr and Mlh1 synergistically enhance tumor susceptibility in mice. J Clin Invest 2009;119:2714-24.
57. Oh YM, Kwon YE, Kim JM, Bae SJ, Lee BK, Yoo SJ, et al. Chfr is linked to tumour metastasis through the downregulation of HDAC1. Nat Cell Biol 2009;11:295-302.
58. Derks S, Cleven AH, Melotte V, Smits KM, Brandes JC, Azad N, et al. Emerging evidence for CHFR as a cancer biomarker: from tumor biology to precision medicine. Cancer Metastasis Rev 2014;33:161-71.
59. Banno K, Yanokura M, Kawaguchi M, Kuwabara Y, Akiyoshi J, Kobayashi Y, et al. Epigenetic inactivation of the CHFR gene in cervical cancer contributes to sensitivity to taxanes. Int J Oncol 2007;31:713-20.
60. Ogi K, Toyota M, Mita H, Satoh A, Kashima L, Sasaki Y, et al. Small interfering RNA-inducedCHFR silencing sensitizes oral squamous cell cancer cells to microtubule inhibitors. Cancer Biol Ther 2005;4:773-80. (Pubitemid 41351179)
61. Koga Y, Kitajima Y, Miyoshi A, Sato K, Sato S, Miyazaki K. The signifi cance of aberrant CHFR methylation for clinical response to microtubule inhibitors in gastric cancer. J Gastroenterol 2006;41:133-9.
62. Swanton C, Tomlinson I, Downward J. Chromosomal instability, colorectal cancer and taxane resistance. Cell Cycle 2006;5:818-23. (Pubitemid 44145573)