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Annals of Oncology Advance Access originally published online on January 22, 2009
Annals of Oncology 2009 20(7):1216-1222; doi:10.1093/annonc/mdn782
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© The Author 2009. Published by Oxford University Press on behalf of the European Society for Medical Oncology. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org

gastrointestinal tumors

MGMT and MLH1 promoter methylation versus APC, KRAS and BRAF gene mutations in colorectal cancer: indications for distinct pathways and sequence of events

S. de Vogel1,2, M. P. Weijenberg1, J. G. Herman3, K. A. D. Wouters2, A. F. P. M. de Goeij2, P. A. van den Brandt1, A. P. de Bruïne2 and M. van Engeland2,*

1 Department of Epidemiology, GROW—School for Oncology and Developmental Biology, Maastricht University, Maastricht, The Netherlands
2 Department of Pathology, GROW—School for Oncology and Developmental Biology, Maastricht University, Maastricht, The Netherlands
3 The Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins School of Medicine, Baltimore, USA

* Correspondence to: Dr M. van Engeland, Department of Pathology, GROW—School for Oncology and Developmental Biology, Maastricht University, PO Box 616, 6200 MD Maastricht, The Netherlands. Tel: +31-43-3874622; Fax: +31-43-3876613; E-mail: m.vanengeland{at}path.unimaas.nl

Background: To study how caretaker gene silencing relates to gatekeeper mutations in colorectal cancer (CRC), we investigated whether O6-methylguanine DNA methyltransferase (MGMT) and Human Mut-L Homologue 1 (MLH1) promoter hypermethylation are associated with APC, KRAS and BRAF mutations among 734 CRC patients.

Methods: We compared MGMT hypermethylation with G:C > A:T mutations in APC and KRAS and with the occurrence of such mutations in CpG or non-CpG dinucleotides in APC. We also compared MLH1 hypermethylation with truncating APC mutations and activating KRAS and BRAF mutations.

Results: Only 10% of the tumors showed both MGMT and MLH1 hypermethylation. MGMT hypermethylation occurred more frequently in tumors with G:C > A:T KRAS mutations (55%) compared with those without these mutations (38%, P < 0.001). No such difference was observed for G:C > A:T mutations in APC, regardless of whether mutations occurred in CpG or non-CpG dinucleotides. MLH1 hypermethylation was less common in tumors with APC mutations (P = 0.006) or KRAS mutations (P = 0.001), but was positively associated with BRAF mutations (P < 0.001).

Conclusions: MGMT hypermethylation is associated with G:C > A:T mutations in KRAS, but not in APC, suggesting that MGMT hypermethylation may succeed APC mutations but precedes KRAS mutations in colorectal carcinogenesis. MLH1-hypermethylated tumors harbor fewer APC and KRAS mutations and more BRAF mutations, suggesting that they develop distinctly from an MGMT methylator pathway.

Key words: APC, BRAF, KRAS mutations, CRC, MGMT methylation, MLH1 methylation

Received for publication September 13, 2008. Revision received December 11, 2008. Accepted for publication December 12, 2008.


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