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Research Paper

The proto CpG island methylator phenotype of sessile serrated adenomas/polyps

ORCID Icon, , , , , , , , , , , , ORCID Icon & ORCID Icon show all
Pages 1088-1105 | Received 20 Jul 2018, Accepted 22 Oct 2018, Published online: 22 Nov 2018

References

  • Jass JR Serrated adenoma of the colorectum and the DNA-methylator phenotype. Nat Clin Pract Oncol. 2005 Aug;2(8):398–405. PubMed PMID: 16130936.
  • Phipps AI, Limburg PJ, Baron JA, et al. Association between molecular subtypes of colorectal cancer and patient survival. Gastroenterology. 2015 Jan;148(1):77–87 e2. . PubMed PMID: 25280443; PubMed Central PMCID: PMCPMC4274235.
  • Hinoue T, Weisenberger DJ, Lange CP, et al. Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res. 2012 Feb;22(2):271–282. . PubMed PMID: 21659424; PubMed Central PMCID: PMCPMC3266034.
  • Okugawa Y, Grady WM, Goel A Epigenetic alterations in colorectal cancer: emerging biomarkers. Gastroenterology. 2015 Oct;149(5):1204–1225 e12. . PubMed PMID: 26216839; PubMed Central PMCID: PMCPMC4589488.
  • Ijspeert JEG, Vermeulen L, Meijer GA, et al. Serrated neoplasia-role in colorectal carcinogenesis and clinical implications. Nat Rev Gastroenterol Hepatol. 2015 Jul;12(7):401–409. . PubMed PMID: 25963511.
  • Bettington M, Walker N, Clouston A, et al. The serrated pathway to colorectal carcinoma: current concepts and challenges. Histopathology. 2013 Feb;62(3):367–386. . PubMed PMID: 23339363.
  • Toyota M, Ahuja N, Ohe-Toyota M, et al. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci U S A. 1999 Jul 20;96(15):8681–8686. PubMed PMID: 10411935; eng.
  • Deaton AM, Bird A CpG islands and the regulation of transcription. Genes Dev. 2011 May 15;25(10):1010–1022. PubMed PMID: 21576262; PubMed Central PMCID: PMCPMC3093116.
  • Feinberg AP, Ohlsson R, Henikoff S The epigenetic progenitor origin of human cancer. Nat Rev Genet. 2006 Jan;7(1):21–33. PubMed PMID: 16369569.
  • Jones PA, Baylin SB The epigenomics of cancer. Cell. 2007 Feb 23;128(4):683–692. PubMed PMID: 17320506; PubMed Central PMCID: PMCPMC3894624.
  • Issa JP Aging and epigenetic drift: a vicious cycle. J Clin Invest. 2014 Jan;124(1):24–29. PubMed PMID: 24382386; PubMed Central PMCID: PMCPMC3871228.
  • Rodriguez-Paredes M, Esteller M. Cancer epigenetics reaches mainstream oncology. Nat Med. 2011 Mar;17(3):330–339. PubMed PMID: 21386836.
  • Boland CR, Goel A Microsatellite instability in colorectal cancer. Gastroenterology. 2010 Jun;138(6):2073–2087 e3. PubMed PMID: 20420947; PubMed Central PMCID: PMCPMC3037515.
  • O’Brien MJ, Yang S, Mack C, et al. Comparison of microsatellite instability, CpG island methylation phenotype, BRAF and KRAS status in serrated polyps and traditional adenomas indicates separate pathways to distinct colorectal carcinoma end points. Am J Surg Pathol. 2006 Dec;30(12):1491–1501. PubMed PMID: 17122504.
  • 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. 2006 Jul;38(7):787–793. PubMed PMID: 16804544; eng.
  • Bettington M, Walker N, Rosty C, et al. Clinicopathological and molecular features of sessile serrated adenomas with dysplasia or carcinoma. Gut. 2017 Jan;66(1):97–106. PubMed PMID: 26475632.
  • Carethers JM, Smith EJ, Behling CA, et al. Use of 5-fluorouracil and survival in patients with microsatellite-unstable colorectal cancer. Gastroenterology. 2004 Feb;126(2):394–401. PubMed PMID: 14762775.
  • Le DT, Uram JN, Wang H, et al. PD-1 blockade in tumors with mismatch-repair deficiency. New Engl J Med. 2015 Jun 25;372(26):2509–2520. PubMed PMID: WOS:000356788200007; English.
  • Bosman FT, Carneiro F, Hruban RH, et al. WHO classification of tumors of the digestive system. Lyon: International Agency for Research on Cancer Publisher; 2010.
  • Kambara T, Simms LA, Whitehall VL, et al. BRAF mutation is associated with DNA methylation in serrated polyps and cancers of the colorectum. Gut. 2004 Aug;53(8):1137–1144. PubMed PMID: 15247181.
  • Rex DK, Ahnen DJ, Baron JA, et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol. 2012 Sep;107(9):1315–29; quiz 1314, 1330. PubMed PMID: 22710576; PubMed Central PMCID: PMCPMC3629844.
  • Fang M, Ou J, Hutchinson L, et al. The BRAF oncoprotein functions through the transcriptional repressor MAFG to mediate the CpG Island methylator phenotype. Mol Cell. 2014 Sep 18;55(6):904–915. PubMed PMID: 25219500; PubMed Central PMCID: PMCPMC4170521.
  • Carragher LA, Snell KR, Giblett SM, et al. V600EBraf induces gastrointestinal crypt senescence and promotes tumour progression through enhanced CpG methylation of p16INK4a. EMBO Mol Med. 2010 Nov;2(11):458–471. PubMed PMID: 20941790; PubMed Central PMCID: PMCPMC3394506.
  • Rad R, Cadinanos J, Rad L, et al. A genetic progression model of Braf(V600E)-induced intestinal tumorigenesis reveals targets for therapeutic intervention. Cancer Cell. 2013 Jul 8;24(1):15–29. PubMed PMID: 23845441; PubMed Central PMCID: PMCPMC3706745.
  • Sakamoto N, Feng Y, Stolfi C, et al. BRAF(V600E) cooperates with CDX2 inactivation to promote serrated colorectal tumorigenesis. Elife. 2017 Jan 10;6. doi: 10.7554/eLife.20331. PubMed PMID: 28072391; PubMed Central PMCID: PMCPMC5268782.
  • Lieberman DA, Rex DK, Winawer SJ, et al. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US multi-society task force on colorectal cancer. Gastroenterology. 2012 Sep;143(3):844–857. PubMed PMID: 22763141.
  • Singh H, Nugent Z, Demers AA, et al. The reduction in colorectal cancer mortality after colonoscopy varies by site of the cancer. Gastroenterology. 2010 Oct;139(4):1128–1137. PubMed PMID: 20600026.
  • East JE, Vieth M, Rex DK Serrated lesions in colorectal cancer screening: detection, resection, pathology and surveillance. Gut. 2015 Jun;64(6):991–1000. PubMed PMID: 25748647.
  • Gourevitch RA, Rose S, Crockett SD, et al. Variation in pathologist classification of colorectal adenomas and serrated polyps. Am J Gastroenterol. 2018 Jan 30. PubMed PMID: 29380819. 113 431–439
  • Pohl H, Srivastava A, Bensen SP, et al. Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study. Gastroenterology. 2013 Jan;144(1):74–80 e1. PubMed PMID: 23022496.
  • Bettington M, Walker N, Rosty C, et al. Critical appraisal of the diagnosis of the sessile serrated adenoma. Am J Surg Pathol. 2014 Feb;38(2):158–166. PubMed PMID: 24418851.
  • Sawhney MS, Farrar WD, Gudiseva S, et al. Microsatellite instability in interval colon cancers. Gastroenterology. 2006 Dec;131(6):1700–1705. PubMed PMID: 17087932.
  • Bird AP Use of restriction enzymes to study eukaryotic dna methylation .2. Symmetry of methylated sites supports semi-conservative copying of methylation pattern. J Mol Biol. 1978;118(1):49–60. PubMed PMID: WOS:A1978EM86300003; English.
  • Wu H, Zhang Y Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell. 2014 Jan 16; 156 (1–2): 45–68. PubMed PMID: 24439369; PubMed Central PMCID: PMCPMC3938284.
  • Menigatti M, Cattaneo E, Sabates-Bellver J, et al. The protein tyrosine phosphatase receptor type R gene is an early and frequent target of silencing in human colorectal tumorigenesis. Mol Cancer. 2009;8:124. doi: 1476-4598-8-124 [pii]
  • Menigatti M, Truninger K, Gebbers JO, et al. Normal colorectal mucosa exhibits sex- and segment-specific susceptibility to DNA methylation at the hMLH1 and MGMT promoters. Oncogene. 2009 Feb 12;28(6):899–909. PubMed PMID: 19060925; eng.
  • Menigatti M, Staiano T, Manser CN, et al. Epigenetic silencing of monoallelically methylated miRNA loci in precancerous colorectal lesions. Oncogenesis. 2013 Jul 15;2:e56. PubMed PMID: 23857251; PubMed Central PMCID: PMCPMC3740287.
  • Suzuki H, Watkins DN, Jair KW, et al. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet. 2004 Apr;36(4):417–422. PubMed PMID: 15034581.
  • Nikolaev SI, Sotiriou SK, Pateras IS, et al. A single-nucleotide substitution mutator phenotype revealed by exome sequencing of human colon adenomas. Cancer Res. 2012 Dec 1;72(23):6279–6289. PubMed PMID: 23204322.
  • Lin SH, Raju GS, Huff C, et al. The somatic mutation landscape of premalignant colorectal adenoma. Gut. 2017 Jun 12. doi: 10.1136/gutjnl-2016-313573. PubMed PMID: 28607096.
  • Dehghanizadeh S, Khoddami V, Mosbruger TL, et al. Active BRAF-V600E is the key player in generation of a sessile serrated polyp-specific DNA methylation profile. PLoS One. 2018;13(3):e0192499. PubMed PMID: 29590112; PubMed Central PMCID: PMCPMC5873940.
  • Di Pietro M, Bellver JS, Menigatti M, et al. Defective DNA mismatch repair determines a characteristic transcriptional profile in proximal colon cancers. Gastroenterology. 2005 Sep;129(3):1047–1059. PubMed PMID: 16143142.
  • Lin JC, Jeong S, Liang G, et al. Role of nucleosomal occupancy in the epigenetic silencing of the MLH1 CpG island. Cancer Cell. 2007 Nov;12(5):432–444. PubMed PMID: 17996647; PubMed Central PMCID: PMCPMC4657456.
  • Jones PA Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012 May 29;13(7):484–492. PubMed PMID: 22641018.
  • Kim YH, Kakar S, Cun L, et al. Distinct CpG island methylation profiles and BRAF mutation status in serrated and adenomatous colorectal polyps. Int J Cancer. 2008 Dec 01;123(11):2587–2593. PubMed PMID: 18798261.
  • Vaughn CP, Wilson AR, Samowitz WS Quantitative evaluation of CpG island methylation in hyperplastic polyps. Mod Pathol. 2010 Jan;23(1):151–156. PubMed PMID: 19855373.
  • Maeda T, Suzuki K, Togashi K, et al. Sessile serrated adenoma shares similar genetic and epigenetic features with microsatellite unstable colon cancer in a location-dependent manner. Exp Ther Med. 2011 Jul;2(4):695–700. PubMed PMID: 22977561; PubMed Central PMCID: PMCPMC3440750.
  • Dhir M, Yachida S, Van Neste L, et al. Sessile serrated adenomas and classical adenomas: an epigenetic perspective on premalignant neoplastic lesions of the gastrointestinal tract. Int J Cancer. 2011 Oct 15;129(8):1889–1898. PubMed PMID: 21154739; PubMed Central PMCID: PMCPMC3206997.
  • Burnett-Hartman AN, Newcomb PA, Potter JD, et al. Genomic aberrations occurring in subsets of serrated colorectal lesions but not conventional adenomas. Cancer Res. 2013 May 1;73(9):2863–2872. PubMed PMID: 23539450; PubMed Central PMCID: PMCPMC3815695.
  • Fernando WC, Miranda MS, Worthley DL, et al. The CIMP phenotype in BRAF mutant serrated polyps from a prospective colonoscopy patient cohort. Gastroenterol Res Pract. 2014;2014:1–10. PubMed PMID: 24812557; PubMed Central PMCID: PMCPMC4000649.
  • Yamamoto E, Suzuki H, Yamano HO, et al. Molecular dissection of premalignant colorectal lesions reveals early onset of the CpG island methylator phenotype. Am J Pathol. 2012 Nov;181(5):1847–1861. PubMed PMID: 22995252.
  • Worthley DL, Whitehall VL, Buttenshaw RL, et al. DNA methylation within the normal colorectal mucosa is associated with pathway-specific predisposition to cancer. Oncogene. 2010 Mar 18;29(11):1653–1662. PubMed PMID: 19966864.
  • Park SJ, Rashid A, Lee JH, et al. Frequent CpG island methylation in serrated adenomas of the colorectum. Am J Pathol. 2003 Mar;162(3):815–822. PubMed PMID: 12598316.
  • Imperiale TF, Ransohoff DF, Itzkowitz SH, et al. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med. 2014 Apr 03;370(14):1287–1297. PubMed PMID: 24645800.
  • Herman JG, Umar A, Polyak K, et al. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6870–6875. PubMed PMID: 9618505.
  • Truninger K, Menigatti M, Luz J, et al. Immunohistochemical analysis reveals high frequency of PMS2 defects in colorectal cancer. Gastroenterology. 2005 May;128(5):1160–1171. PubMed PMID: 15887099.
  • Reed KR, Korobko IV, Ninkina N, et al. Hunk/Mak-v is a negative regulator of intestinal cell proliferation. BMC Cancer. 2015 Mar 8;15:110. doi: 10.1186/s12885-015-1087-2. PubMed PMID: 25881306; PubMed Central PMCID: PMCPMC4367870.
  • Yeh ES, Belka GK, Vernon AE, et al. Hunk negatively regulates c-myc to promote Akt-mediated cell survival and mammary tumorigenesis induced by loss of pten. Proc Natl Acad Sci U S A. 2013 Apr 9;110(15):6103–6108. PubMed PMID: 23520049; PubMed Central PMCID: PMCPMC3625285.
  • Bergman Y, Cedar H DNA methylation dynamics in health and disease. Nat Struct Mol Biol. 2013 Mar;20(3):274–281. PubMed PMID: 23463312.
  • Schlesinger Y, Straussman R, Keshet I, et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet. 2007 Feb;39(2):232–236. PubMed PMID: 17200670.
  • Widschwendter M, Fiegl H, Egle D, et al. Epigenetic stem cell signature in cancer. Nat Genet. 2007 Feb;39(2):157–158. PubMed PMID: 17200673.
  • Mohn F, Weber M, Rebhan M, et al. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell. 2008 Jun 20;30(6):755–766. PubMed PMID: 18514006.
  • Reddington JP, Pennings S, Meehan RR Non-canonical functions of the DNA methylome in gene regulation. Biochem J. 2013 Apr 1;451(1):13–23. PubMed PMID: 23489368.
  • Manzo M, Wirz J, Ambrosi C, et al. Isoform-specific localization of DNMT3A regulates DNA methylation fidelity at bivalent CpG islands. Embo J. 2017 Dec 1;36(23):3421–3434. PubMed PMID: 29074627; PubMed Central PMCID: PMCPMC5709737.
  • Easwaran H, Johnstone SE, Van Neste L, et al. A DNA hypermethylation module for the stem/progenitor cell signature of cancer. Genome Res. 2012 May;22(5):837–849. PubMed PMID: 22391556; PubMed Central PMCID: PMCPMC3337430.
  • Ong CT, Corces VG CTCF: an architectural protein bridging genome topology and function. Nat Rev Genet. 2014 Apr;15(4):234–246. PubMed PMID: 24614316; PubMed Central PMCID: PMCPMC4610363.
  • Yin Y, Morgunova E, Jolma A, et al. Impact of cytosine methylation on DNA binding specificities of human transcription factors. Science. 2017 May 05;356(6337). doi: 10.1126/science.aaj2239. PubMed PMID: 28473536.
  • Flavahan WA, Drier Y, Liau BB, et al. Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature. 2016 Jan 07;529(7584):110–114. PubMed PMID: 26700815; PubMed Central PMCID: PMCPMC4831574.
  • Wang H, Maurano MT, Qu H, et al. Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res. 2012 Sep;22(9):1680–1688. PubMed PMID: 22955980; PubMed Central PMCID: PMCPMC3431485.
  • Yan H, Tang G, Wang H, et al. DNA methylation reactivates GAD1 expression in cancer by preventing CTCF-mediated polycomb repressive complex 2 recruitment. Oncogene. 2016 Jul 28;35(30):3995–4008. PubMed PMID: 26549033.
  • Neri F, Rapelli S, Krepelova A, et al. Intragenic DNA methylation prevents spurious transcription initiation. Nature. 2017 Mar 2;543(7643):72–77. PubMed PMID: 28225755.
  • Maunakea AK, Nagarajan RP, Bilenky M, et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature. 2010 Jul 8;466(7303):253–257. PubMed PMID: 20613842; PubMed Central PMCID: PMCPMC3998662.
  • Kim JH, Kim KJ, Rhee YY, et al. Gastric-type expression signature in serrated pathway-associated colorectal tumors. Hum Pathol. 2015 May;46(5):643–656. PubMed PMID: 25704805.
  • Delker DA, McGettigan BM, Kanth P, et al. RNA sequencing of sessile serrated colon polyps identifies differentially expressed genes and immunohistochemical markers. PLoS One. 2014;9(2):e88367. PubMed PMID: 24533081; PubMed Central PMCID: PMCPMC3922809.
  • Sajanti SA, Vayrynen JP, Sirnio P, et al. Annexin A10 is a marker for the serrated pathway of colorectal carcinoma. Virchows Arch. 2015 Jan;466(1):5–12. PubMed PMID: 25395067.
  • Caruso M, Moore J, Goodall GJ, et al. Over-expression of cathepsin E and trefoil factor 1 in sessile serrated adenomas of the colorectum identified by gene expression analysis. Virchows Arch. 2009 Mar;454(3):291–302. PubMed PMID: 19172291.
  • Gonzalo DH, Lai KK, Shadrach B, et al. Gene expression profiling of serrated polyps identifies annexin A10 as a marker of a sessile serrated adenoma/polyp. J Pathol. 2013 Aug;230(4):420–429. PubMed PMID: 23595865.
  • De Sousa E Melo F, Wang X, Jansen M, et al. Poor-prognosis colon cancer is defined by a molecularly distinct subtype and develops from serrated precursor lesions. Nat Med. 2013 May;19(5):614–618. PubMed PMID: 23584090.
  • Kanth P, Bronner MP, Boucher KM, et al. Gene signature in sessile serrated polyps identifies colon cancer subtype. Cancer Prev Res (Phila). 2016 Jun;9(6):456–465. doi: 10.1158/1940-6207.CAPR-15-0363. PubMed PMID: 27026680; PubMed Central PMCID: PMCPMC4941619.
  • Rahmatallah Y, Khaidakov M, Lai KK, et al. Platform-independent gene expression signature differentiates sessile serrated adenomas/polyps and hyperplastic polyps of the colon. BMC Med Genomics. 2017 Dec 28;10(1):81. doi: 10.1186/s12920-017-0317-7. PubMed PMID: 29284484; PubMed Central PMCID: PMCPMC5745747.
  • Endoscopic Classification Review Group. Update on the Paris classification of superficial neoplastic lesions in the digestive tract. Endoscopy. 2005 Jun;37(6):570–578. PubMed PMID: 15933932.
  • Krueger F, Andrews SR Bismark: a flexible aligner and methylation caller for bisulfite-seq applications. Bioinformatics. 2011 Jun 1;27(11):1571–1572. PubMed PMID: 21493656; PubMed Central PMCID: PMCPMC3102221.
  • Patro R, Duggal G, Love MI, et al. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017 Apr;14(4):417–419. PubMed PMID: 28263959; PubMed Central PMCID: PMCPMC5600148.
  • Hebestreit K, Dugas M, Klein HU. Detection of significantly differentially methylated regions in targeted bisulfite sequencing data. Bioinformatics. 2013 Jul 1;29(13):1647–1653. PubMed PMID: 23658421.
  • Robinson MD, McCarthy DJ, Smyth GK edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010 Jan 1;26(1):139–140. PubMed PMID: 19910308; PubMed Central PMCID: PMCPMC2796818.