Promoter methylation of Wnt5a is associated with microsatellite instability and BRAF V600E mutation in two large populations of colorectal cancer patients

British Journal of Cancer

Volumn 104, Issue 12, 2011, Pages 1906-1912

  Rawson, J B ^a,b   Mrkonjic, M ^a,b   Daftary, D ^c   Dicks, E ^d   Buchanan, D D ^e   Younghusband, H B ^d   Parfrey, P S ^d   Young, J P ^e   Pollett, A ^b   Green, R C ^d   Gallinger, S ^a,b,c   McLaughlin, J R ^b,f   Knight, J A ^b,f   Bapat, B ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c CANCER CARE ONTARIO   (Canada)

^d MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^e QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^f UNIVERSITY OF TORONTO   (Canada)

Author keywords

colorectal cancer; methylation; microsatellite instability; Wnt

Indexed keywords

ADULT; AGE; ARTICLE; BRAF V600E GENE; CANADA; CANCER SURVIVAL; COLORECTAL CANCER; CPG ISLAND; DNA METHYLATION; EPIGENETICS; FEMALE; GENDER; GENE MUTATION; HUMAN; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; PRIORITY JOURNAL; PROMOTER REGION; WNT5A GENE;

ADULT; AGED; COLORECTAL NEOPLASMS; DNA METHYLATION; FEMALE; HUMANS; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; MUTATION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS B-RAF; WNT PROTEINS;

EID: 79958179303     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2011.165     Document Type: Article

References (40)

1. Ahn JB, Chung WB, Maeda O, Shin SJ, Kim HS, Chung HC, Kim NK, Issa JP (2011) DNA methylation predicts recurrence from resected stage III proximal colon cancer. Cancer 117(9): 1847-1854
2. Albuquerque C, Baltazar C, Filipe B, Penha F, Pereira T, Smits R, Cravo M, Lage P, Fidalgo P, Claro I, Rodrigues P, Veiga I, Ramos JS, Fonseca I, Leitao CN, Fodde R (2010) Colorectal cancers show distinct mutation spectra in members of the canonical WNT signaling pathway according to their anatomical location and type of genetic instability. Genes Chromosomes Cancer 49(8): 746-759
3. Carethers JM, Smith EJ, Behling CA, Nguyen L, Tajima A, Doctolero RT, Cabrera BL, Goel A, Arnold CA, Miyai K, Boland CR (2004) Use of 5-fluorouracil and survival in patients with microsatellite-unstable colorectal cancer. Gastroenterology 126(2): 394-401 (Pubitemid 38182296)
4. Dahlin AM, Palmqvist R, Henriksson ML, Jacobsson M, Eklof V, Rutegard J, Oberg A, Van Guelpen BR (2010) The role of the CpG island methylator phenotype in colorectal cancer prognosis depends on microsatellite instability screening status. Clin Cancer Res 16(6): 1845-1855
5. Dejmek J, Dejmek A, Safholm A, Sjolander A, Andersson T (2005) Wnt-5a protein expression in primary dukes B colon cancers identifies a subgroup of patients with good prognosis. Cancer Res 65(20): 9142-9146 (Pubitemid 41507974)
6. Eads CA, Danenberg KD, Kawakami K, Saltz LB, Blake C, Shibata D, Danenberg PV, Laird PW (2000) MethyLight: a high-throughput assay to measure DNA methylation. Nucleic Acids Res 28(8): E32
7. Green RC, Green JS, Buehler SK, Robb JD, Daftary D, Gallinger S, McLaughlin JR, Parfrey PS, Younghusband HB (2007) Very high incidence of familial colorectal cancer in Newfoundland: a comparison with Ontario and 13 other population-based studies. Fam Cancer 6(1): 53-62 (Pubitemid 46295298)
8. Green RC, Parfrey PS, Woods MO, Younghusband HB (2009) Prediction of Lynch syndrome in consecutive patients with colorectal cancer. J Natl Cancer Inst 101(5): 331-340
9. Jonsson M, Dejmek J, Bendahl PO, Andersson T (2002) Loss of Wnt-5a protein is associated with early relapse in invasive ductal breast carcinomas. Cancer Res 62(2): 409-416 (Pubitemid 34106413)
10. Ki DH, Jeung HC, Park CH, Kang SH, Lee GY, Lee WS, Kim NK, Chung HC, Rha SY (2007) Whole genome analysis for liver metastasis gene signatures in colorectal cancer. Int J Cancer 121(9): 2005-2012
11. Kim JH, Shin SH, Kwon HJ, Cho NY, Kang GH (2009) Prognostic implications of CpG island hypermethylator phenotype in colorectal cancers. Virchows Arch 455(6): 485-494
12. Kremenevskaja N, von Wasielewski R, Rao AS, Schofl C, Andersson T, Brabant G (2005) Wnt-5a has tumor suppressor activity in thyroid carcinoma. Oncogene 24(13): 2144-2154 (Pubitemid 40516581)
13. Leris AC, Roberts TR, Jiang WG, Newbold RF, Mokbel K (2005) WNT5A expression in human breast cancer. Anticancer Res 25(2A): 731-734 (Pubitemid 40546838)
14. Liang H, Chen Q, Coles AH, Anderson SJ, Pihan G, Bradley A, Gerstein R, Jurecic R, Jones SN (2003) Wnt5a inhibits B cell proliferation and functions as a tumor suppressor in hematopoietic tissue. Cancer Cell 4(5): 349-360 (Pubitemid 37491096)
15. Lindor NM, Burgart LJ, Leontovich O, Goldberg RM, Cunningham JM, Sargent DJ, Walsh-Vockley C, Petersen GM, Walsh MD, Leggett BA, Young JP, Barker MA, Jass JR, Hopper J, Gallinger S, Bapat B, Redston M, Thibodeau SN (2002) Immunohistochemistry vs micro-satellite instability testing in phenotyping colorectal tumors. J Clin Oncol 20(4): 1043-1048 (Pubitemid 34141849)
16. Loughrey MB, Waring PM, Tan A, Trivett M, Kovalenko S, Beshay V, Young MA, McArthur G, Boussioutas A, Dobrovic A (2007) Incorporation of somatic BRAF mutation testing into an algorithm for the investigation of hereditary non-polyposis colorectal cancer. Fam Cancer 6(3): 301-310 (Pubitemid 47175009)
17. Martin V, Valencia A, Agirre X, Cervera J, San Jose-Eneriz E, Vilas-Zornoza A, Rodriguez-Otero P, Sanz MA, Herrera C, Torres A, Prosper F, Roman-Gomez J (2010) Epigenetic regulation of the non-canonical Wnt pathway in acute myeloid leukemia. Cancer Sci 101(2): 425-432
18. Mazieres J, He B, You L, Xu Z, Lee AY, Mikami I, Reguart N, Rosell R, McCormick F, Jablons DM (2004) Wnt inhibitory factor-1 is silenced by promoter hypermethylation in human lung cancer. Cancer Res 64(14): 4717-4720 (Pubitemid 38924512)
19. Mrkonjic M, Roslin NM, Greenwood CM, Raptis S, Pollett A, Laird PW, Pethe VV, Chiang T, Daftary D, Dicks E, Thibodeau SN, Gallinger S, Parfrey PS, Younghusband HB, Potter JD, Hudson TJ, McLaughlin JR, Green RC, Zanke BW, Newcomb PA, Paterson AD, Bapat B (2010) Specific variants in the MLH1 gene region may drive DNA methylation, loss of protein expression, and MSI-H colorectal cancer. PLoS One 5(10): e13314
20. Newcomb PA, Baron J, Cotterchio M, Gallinger S, Grove J, Haile R, Hall D, Hopper JL, Jass J, Le Marchand L, Limburg P, Lindor N, Potter JD, Templeton AS, Thibodeau S, Seminara D (2007) Colon cancer family registry: an international resource for studies of the genetic epidemiology of colon cancer. Cancer Epidemiol Biomarkers Prev 16(11): 2331-2343 (Pubitemid 351196365)
21. Ogino S, Goel A (2008) Molecular classification and correlates in colorectal cancer. J Mol Diagn 10(1): 13-27 (Pubitemid 351184831)
22. Ogino S, Kawasaki T, Brahmandam M, Cantor M, Kirkner GJ, Spiegelman D, Makrigiorgos GM, Weisenberger DJ, Laird PW, Loda M, Fuchs CS (2006) Precision and performance characteristics of bisulfite conversion and real-time PCR (MethyLight) for quantitative DNA methylation analysis. J Mol Diagn 8(2): 209-217 (Pubitemid 43811244)
23. Ogino S, Nosho K, Kirkner GJ, Kawasaki T, Meyerhardt JA, Loda M, Giovannucci EL, Fuchs CS (2009) CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut 58(1): 90-96
24. Ortega P, Moran A, de Juan C, Frias C, Hernandez S, Lopez-Asenjo JA, Sanchez-Pernaute A, Torres A, Iniesta P, Benito M (2008) Differential Wnt pathway gene expression and E-cadherin truncation in sporadic colorectal cancers with and without microsatellite instability. Clin Cancer Res 14(4): 995-1001 (Pubitemid 351302544)
25. Raptis S, Mrkonjic M, Green RC, Pethe VV, Monga N, Chan YM, Daftary D, Dicks E, Younghusband BH, Parfrey PS, Gallinger SS, McLaughlin JR, Knight JA, Bapat B (2007) MLH1 -93G> A promoter polymorphism and the risk of microsatellite-unstable colorectal cancer. J Natl Cancer Inst 99(6): 463-474 (Pubitemid 47078735)
26. Rawson J, Mrkonjic M, Darshana D, Dicks E, Buchanan D, Younghusband H, Parfrey P, Young J, Green R, Pollett A, Gallinger S, McLaughlin J, Knight J, Bapat B (2011) Promoter methylation of Wnt antagonists DKK1 and SFRP1 are associated with opposing tumor subtypes in a large cohort of colorectal cancer. Carcinogenesis, e-pub ahead of print 8 February 2011
27. Ribic CM, Sargent DJ, Moore MJ, Thibodeau SN, French AJ, Goldberg RM, Hamilton SR, Laurent-Puig P, Gryfe R, Shepherd LE, Tu D, Redston M, Gallinger S (2003) Tumor microsatellite-instability status as a predictor of benefit from fluorouracil-based adjuvant chemotherapy for colon cancer. N Engl J Med 349(3): 247-257 (Pubitemid 36859476)
28. Samowitz WS, Slattery ML, Sweeney C, Herrick J, Wolff RK, Albertsen H (2007) APC mutations and other genetic and epigenetic changes in colon cancer. Mol Cancer Res 5(2): 165-170 (Pubitemid 46423997)
29. Tanaka N, Huttenhower C, Nosho K, Baba Y, Shima K, Quackenbush J, Haigis KM, Giovannucci E, Fuchs CS, Ogino S (2010) Novel application of structural equation modeling to correlation structure analysis of CpG island methylation in colorectal cancer. Am J Pathol 177(6): 2731-2740
30. Thorstensen L, Lind GE, Lovig T, Diep CB, Meling GI, Rognum TO, Lothe RA (2005) Genetic and epigenetic changes of components affecting the WNT pathway in colorectal carcinomas stratified by microsatellite instability. Neoplasia 7(2): 99-108 (Pubitemid 40315987)
31. Wang Q, Symes AJ, Kane CA, Freeman A, Nariculam J, Munson P, Thrasivoulou C, Masters JR, Ahmed A (2010) A novel role for Wnt/Ca2+ signaling in actin cytoskeleton remodeling and cell motility in prostate cancer. PLoS One 5(5): e10456
32. Wang Q, Williamson M, Bott S, Brookman-Amissah N, Freeman A, Nariculam J, Hubank MJ, Ahmed A, Masters JR (2007) Hypomethylation of WNT5A, CRIP1 and S100P in prostate cancer. Oncogene 26(45): 6560-6565 (Pubitemid 47530597)
33. Wang Y (2009) Wnt/Planar cell polarity signaling: a new paradigm for cancer therapy. Mol Cancer Ther 8(8): 2103-2109
34. Weeraratna AT, Jiang Y, Hostetter G, Rosenblatt K, Duray P, Bittner M, Trent JM (2002) Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 1(3): 279-288 (Pubitemid 41039152)
35. Weisenberger DJ, Campan M, Long TI, Kim M, Woods C, Fiala E, Ehrlich M, Laird PW (2005) Analysis of repetitive element DNA methylation by MethyLight. Nucleic Acids Res 33(21): 6823-6836 (Pubitemid 41830488)
36. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, Kang GH, Widschwendter M, Weener D, Buchanan D, Koh H, Simms L, Barker M, Leggett B, Levine J, Kim M, French AJ, Thibodeau SN, Jass J, Haile R, Laird PW (2006) CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 38(7): 787-793 (Pubitemid 43980599)
37. Woods MO, Hyde AJ, Curtis FK, Stuckless S, Green JS, Pollett AF, Robb JD, Green RC, Croitoru ME, Careen A, Chaulk JA, Jegathesan J, McLaughlin JR, Gallinger SS, Younghusband HB, Bapat BV, Parfrey PS (2005) High frequency of hereditary colorectal cancer in Newfoundland likely involves novel susceptibility genes. Clin Cancer Res 11(19 Part 1): 6853-6861 (Pubitemid 41428740)
38. Yamamoto H, Oue N, Sato A, Hasegawa Y, Yamamoto H, Matsubara A, Yasui W, Kikuchi A (2010) Wnt5a signaling is involved in the aggressiveness of prostate cancer and expression of metalloproteinase. Oncogene 29(14): 2036-2046
39. Ying J, Li H, Yu J, Ng KM, Poon FF, Wong SC, Chan AT, Sung JJ, Tao Q (2008) WNT5A exhibits tumor-suppressive activity through antagoniz ing the Wnt/beta-catenin signaling, and is frequently methylated in colorectal cancer. Clin Cancer Res 14(1): 55-61 (Pubitemid 351377978)
40. Yuzugullu H, Benhaj K, Ozturk N, Senturk S, Celik E, Toylu A, Tasdemir N, Yilmaz M, Erdal E, Akcali KC, Atabey N, Ozturk M (2009) Canonical Wnt signaling is antagonized by noncanonical Wnt5a in hepatocellular carcinoma cells. Mol Cancer 8: 90