Disentangling tumorigenesis-associated DNA methylation changes in colorectal tissues from those associated with ageing

References

• Arndt V, Feller A, Hauri D, et al. Swiss cancer report 2015. Neuchatel, Switzerland: Federal Statistical Office; 2016;
   Google Scholar
• Winawer SJ. Natural history of colorectal cancer. Am J Medicine. 1999;106:3–6.
   Google Scholar
• Lash RH, Genta RM, Schuler CM. Sessile serrated adenomas: prevalence of dysplasia and carcinoma in 2139 patients. J Clin Pathol. 2010;63:681.
   Google Scholar
• Hassan C, Quintero E, Dumonceau J-M, et al. Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy. 2013;45:842–864.
   Google Scholar
• Carr PR, Weigl K, Edelmann D, et al. Estimation of absolute risk of colorectal cancer based on healthy lifestyle, genetic risk, and colonoscopy status in a population-based study. Gastroenterology. 2020;159:129–138.e9.
   Google Scholar
• Mendelsohn RB, Winawer SJ, Ahnen DJ. Incidence of colorectal cancer matters. Gastroenterology. 2019;158:1191–1195.
   Google Scholar
• Kaltenbach T, Anderson JC, Burke CA, et al. Endoscopic removal of colorectal lesions—recommendations by the US multi-society task force on colorectal cancer. Gastroenterology. 2020;158:1095–1129.
   Google Scholar
• Potter NT, Hurban P, White MN, et al. Validation of a real-time PCR–based qualitative assay for the detection of methylated SEPT9 DNA in human plasma. Clin Chem. 2014;60:1183–1191.
   Google Scholar
• Imperiale TF, Ransohoff DF, Itzkowitz SH, et al. Multitarget stool DNA testing for colorectal-cancer screening. New Engl J Medicine. 2014;370:1287–1297.
   Google Scholar
• Wolf AMD, Fontham ETH, Church TR, et al. Colorectal cancer screening for average‐risk adults: 2018 guideline update from the American cancer society. Ca Cancer J Clin. 2018;68:250–281.
   Google Scholar
• Toyota M, Ho C, Ahuja N, et al. Identification of differentially methylated sequences in colorectal cancer by methylated CpG island amplification. Cancer Res. 1999;59:2307–2312.
   Google Scholar
• Herman JG, Umar A, Polyak K, et al. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc Natl Acad Sci. 1998;95:6870–6875.
   Google Scholar
• Truninger K, Menigatti M, Luz J, et al. Immunohistochemical analysis reveals high frequency of PMS2 defects in colorectal cancer. Gastroenterology. 2005;128:1160–1171.
   Google Scholar
• Hinoue T, Weisenberger DJ, Lange CPE, et al. Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res. 2012;22:271–282.
   Google Scholar
• Marra G, Schär P. Recognition of DNA alterations by the mismatch repair system. Biochem J. 1999;338:1–13.
   Google Scholar
• Jiricny J. The multifaceted mismatch-repair system. Nat Rev Mol Cell Bio. 2006;7:335–346.
   Google Scholar
• Rex DK, Ahnen DJ, Baron JA, et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol. 2012;107:1315–1329.
   Google Scholar
• Bettington M, Walker N, Clouston A, et al. The serrated pathway to colorectal carcinoma: current concepts and challenges. Histopathology. 2013;62:367–386.
   Google Scholar
• Parker HR, Orjuela S, Oliveira AM, et al. The proto CpG island methylator phenotype of sessile serrated adenomas/polyps. Epigenetics. 2018;13:1088–1105.
   Google Scholar
• Snover DC. Diagnostic and reporting issues of preneoplastic polyps of the large intestine with early carcinoma. Ann Diagn Pathol. 2018;39:1–14.
   Google Scholar
• Pai RK, Bettington M, Srivastava A, et al. An update on the morphology and molecular pathology of serrated colorectal polyps and associated carcinomas. Modern Pathol. 2019;32:1390–1415.
   Google Scholar
• Menigatti M, Truninger K, Gebbers J-O, et al. Normal colorectal mucosa exhibits sex- and segment-specific susceptibility to DNA methylation at the hMLH1 and MGMT promoters. Oncogene. 2009;28:899–909.
   Google Scholar
• Ahuja N, Li Q, Mohan AL, et al. Aging and DNA methylation in colorectal mucosa and cancer. Cancer Res. 1998;58:5489–5494.
   Google Scholar
• Toyota M, Issa J-PJ. CpG island methylator phenotypes in aging and cancer. Semin Cancer Biol. 1999;9:349–357.
   Google Scholar
• Feinberg AP, Ohlsson R, Henikoff S. The epigenetic progenitor origin of human cancer. Nat Rev Genet. 2006;7:21–33.
   Google Scholar
• Issa J-P. Aging and epigenetic drift: a vicious cycle. J Clin Invest. 2014;124:24–29.
   Google Scholar
• Maegawa S, Gough SM, Watanabe-Okochi N, et al. Age-related epigenetic drift in the pathogenesis of MDS and AML. Genome Res. 2014;24:580–591.
   Google Scholar
• Hannum G, Guinney J, Zhao L, et al. Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell. 2013;49:359–367.
   Google Scholar
• Kaz AM, Wong C-J, Dzieciatkowski S, et al. Patterns of DNA methylation in the normal colon vary by anatomical location, gender, and age. Epigenetics. 2014;9:492–502.
   Google Scholar
• Singmann P, Shem-Tov D, Wahl S, et al. Characterization of whole-genome autosomal differences of DNA methylation between men and women. Epigenet Chromatin. 2015;8:43.
   Google Scholar
• Luebeck GE, Hazelton WD, Curtius K, et al. Implications of epigenetic drift in colorectal neoplasia. Cancer Res. 2019;79:495–504.
   Google Scholar
• Ohm JE, McGarvey KM, Yu X, et al. A stem cell–like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet. 2007;39:237–242.
   Google Scholar
• 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;39:232–236.
   Google Scholar
• Widschwendter M, Fiegl H, Egle D, et al. Epigenetic stem cell signature in cancer. Nat Genet. 2007;39:157–158.
   Google Scholar
• Horvath S. DNA methylation age of human tissues and cell types. Genome Biol. 2013;14:3156.
   Google Scholar
• Christensen BC, Houseman EA, Marsit CJ, et al. Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. Plos Genet. 2009;5:e1000602.
   Google Scholar
• Michalak EM, Burr ML, Bannister AJ, et al. The roles of DNA, RNA and histone methylation in ageing and cancer. Nat Rev Mol Cell Bio. 2019;20:573–589.
   Google Scholar
• Klutstein M, Nejman D, Greenfield R, et al. DNA methylation in cancer and aging. Cancer Res. 2016;76:3446–3450.
   Google Scholar
• Klutstein M, Moss J, Kaplan T, et al. Contribution of epigenetic mechanisms to variation in cancer risk among tissues. Proc Natl Acad Sci. 2017;114:2230–2234.
   Google Scholar
• Horvath S, Zhang Y, Langfelder P, et al. Aging effects on DNA methylation modules in human brain and blood tissue. Genome Biol. 2012;13:R97.
   Google Scholar
• Maegawa S, Hinkal G, Kim HS, et al. Widespread and tissue specific age-related DNA methylation changes in mice. Genome Res. 2010;20:332–340.
   Google Scholar
• Beerman I, Bock C, Garrison BS, et al. Proliferation-dependent alterations of the DNA methylation landscape underlie hematopoietic stem cell aging. Cell Stem Cell. 2013;12:413–425.
   Google Scholar
• Petkovich DA, Podolskiy DI, Lobanov AV, et al. Using DNA methylation profiling to evaluate biological age and longevity interventions. Cell Metab. 2017;25(954–960.e6).
   Google Scholar
• Tm S, MJ B, A-k S, et al. Multi-tissue DNA methylation age predictor in mouse. Genome Biol. 2017;18:68.
   Google Scholar
• Raj K, Horvath S. Current perspectives on the cellular and molecular features of epigenetic ageing. Exp Biol Med. 2020;245:1532–1542.
   Google Scholar
• Niehrs C, Calkhoven CF. Emerging role of C/EBPβ and epigenetic DNA methylation in ageing. Trends Genet. 2020;36:71–80.
   Google Scholar
• Zhang W, Qu J, Liu G-H, et al. The ageing epigenome and its rejuvenation. Nat Rev Mol Cell Bio. 2020;21:137–150.
   Google Scholar
• Xie W, Kagiampakis I, Pan L, et al. DNA methylation patterns separate senescence from transformation potential and indicate cancer risk. Cancer Cell. 2018;33(309–321.e5).
   Google Scholar
• Noreen F, Küng T, Tornillo L, et al. DNA methylation instability by BRAF-mediated TET silencing and lifestyle-exposure divides colon cancer pathways. Clin Epigenetics. 2019;11:196.
   Google Scholar
• Noreen F, Röösli M, Gaj P, et al. Modulation of age- and cancer-associated DNA methylation change in the healthy colon by aspirin and lifestyle. J Natl Cancer Inst. 2014;106(7):dju161.
   Google Scholar
• Jung M, Pfeifer GP. Aging and DNA methylation. Bmc Biol. 2015;13:7.
   Google Scholar
• Yang Z, Wong A, Kuh D, et al. Correlation of an epigenetic mitotic clock with cancer risk. Genome Biol. 2016;17:205.
   Google Scholar
• Chen BH, Marioni RE, Colicino E, et al. DNA methylation-based measures of biological age: meta-analysis predicting time to death. Aging (Albany NY). 2016;8:1844–1865.
   Google Scholar
• Field AE, Robertson NA, Wang T, Havas A, Ideker T, Adams PD. DNA Methylation. Clocks in aging: categories, causes, and consequences. Mol Cell. 2018;71:882–895.
   Google Scholar
• Yu M, Hazelton WD, Luebeck GE, et al. Epigenetic aging: more than just a clock when it comes to cancer. Cancer Res. 2020;80:367–374.
   Google Scholar
• Sk L, Nachun D, Mg M, et al. DNA methylation analysis validates organoids as a viable model for studying human intestinal aging. Cell Mol Gastroenterol Hepatol. 2020;9:527–541.
   Google Scholar
• Teschendorff AE, Menon U, Gentry-Maharaj A, et al. Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res. 2010;20:440–446.
   Google Scholar
• Steegenga WT, Boekschoten MV, Lute C, et al. Genome-wide age-related changes in DNA methylation and gene expression in human PBMCs. Age (Omaha). 2014;36:9648.
   Google Scholar
• Affinito O, Palumbo D, Fierro A, et al. Nucleotide distance influences co-methylation between nearby CpG sites. Genomics. 2020;112:144–150.
   Google Scholar
• Zhang W, Spector TD, Deloukas P, et al. Predicting genome-wide DNA methylation using methylation marks, genomic position, and DNA regulatory elements. Genome Biol. 2015;16:14.
   Google Scholar
• Update on the Paris classification of superficial neoplastic lesions in the digestive tract. Endoscopy. 2005;37:570–578.
   Google Scholar
• Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011;27:1571–1572.
   Google Scholar
• Köster J, Rahmann S. Snakemake—a scalable bioinformatics workflow engine. Bioinformatics. 2012;28:2520–2522.
   Google Scholar
• Hansen KD, Langmead B, Irizarry RA. BSmooth: from whole genome bisulfite sequencing reads to differentially methylated regions. Genome Biol. 2012;13:R83.
   Google Scholar
• Korthauer K, Chakraborty S, Benjamini Y, et al. Detection and accurate false discovery rate control of differentially methylated regions from whole genome bisulfite sequencing. Biostatistics. 2018;20:367–383.
   Google Scholar
• Lawrence M, Huber W, Pagès H, et al. Software for computing and annotating genomic ranges. Plos Comput Biol. 2013;9:e1003118.
   Google Scholar
• Lee S, Cook D, Lawrence M. plyranges: a grammar of genomic data transformation. Genome Biol. 2019;20:4.
   Google Scholar
• Wickham H. ggplot2, elegant graphics for data analysis. Switzerland: Springer-Verlag; 2016.
   Google Scholar
• Gu Z, Eils R, Schlesner M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics. 2016;32:2847–2849.
   Google Scholar
• Cavalcante RG, Sartor MA. annotatr: genomic regions in context. Bioinformatics. 2017;33:2381–2383.
   Google Scholar
• Zhu LJ, Gazin C, Lawson ND, et al. ChIPpeakAnno: a Bioconductor package to annotate ChIP-seq and ChIP-chip data. Bmc Bioinformatics. 2010;11:237.
   Google Scholar
• Luo Y, Wong C-J, Kaz AM, et al. Differences in DNA methylation signatures reveal multiple pathways of progression from adenoma to colorectal cancer. Gastroenterology. 2014;147(418–429.e8).
   Google Scholar
• Díez-Villanueva A, Sanz-Pamplona R, Carreras-Torres R, et al. DNA methylation events in transcription factors and gene expression changes in colon cancer. Epigenomics. 2020;12:1593–1610.
   Google Scholar
• Aryee MJ, Jaffe AE, Corrada-Bravo H, et al. Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics. 2014;30:1363–1369.
   Google Scholar
• Robin X, Turck N, Hainard A, et al. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics. 2011;12:77.
   Google Scholar
• Phipps AI, Limburg PJ, Baron JA, et al. Association between molecular subtypes of colorectal cancer and patient survival. Gastroenterology. 2015;148(77–87.e2).
   Google Scholar
• Rakyan VK, Down TA, Maslau S, et al. Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res. 2010;20:434–439.
   Google Scholar
• Easwaran H, Johnstone SE, Neste LV, et al. A DNA hypermethylation module for the stem/progenitor cell signature of cancer. Genome Res. 2012;22:837–849.
   Google Scholar
• Bracken AP, Dietrich N, Pasini D, et al. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Gene Dev. 2006;20:1123–1136.
   Google Scholar
• Mohn F, Weber M, Rebhan M, et al. Targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell. 2008;30:755–766.
   Google Scholar
• Reddington JP, Sproul D, Meehan RR. DNA methylation reprogramming in cancer: does it act by re‐configuring the binding landscape of Polycomb repressive complexes? Bioessays. 2014;36:134–140.
   Google Scholar
• Easwaran H, Tsai H-C, Baylin SB. Cancer epigenetics: tumor heterogeneity, plasticity of stem-like states, and drug resistance. Mol Cell. 2014;54:716–727.
   Google Scholar
• Serra RW, Fang M, Park SM, et al. A KRAS-directed transcriptional silencing pathway that mediates the CpG island methylator phenotype. Elife. 2014;3:e02313.
   Google Scholar
• 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;55:904–915.
   Google Scholar
• Malta TM, de Souza CF, Sabedot TS, et al. Glioma CpG island methylator phenotype (G-CIMP): biological and clinical implications. Neuro Oncol. 2017;20:608–620.
   Google Scholar
• Liu Y, Sethi NS, Hinoue T, et al. Comparative molecular analysis of gastrointestinal adenocarcinomas. Cancer Cell. 2018;33(721–735.e8).
   Google Scholar
• Tao Y, Kang B, Petkovich DA, et al. Aging-like spontaneous epigenetic silencing facilitates wnt activation, stemness, and braf V600E-induced tumorigenesis. Cancer Cell. 2019;35(315–328.e6).
   Google Scholar