Abstract
Colorectal cancer is a leading cause of cancer related deaths worldwide. One of the hallmarks of cancer and a fundamental trait of virtually all gastrointestinal cancers is altered genomic and epigenomic DNA. The genetic and epigenetic alterations drive the initiation and progression of the cancers by altering the molecular and cell biological process of the colon epithelial cells. These alterations, as well as other host and microenvironment factors, ultimately mediate the initiation and progression of cancers, including colorectal cancer. Epigenetic alterations, which include changes affecting DNA methylation, histone modifications, chromatin structure, and noncoding RNA expression, have been revealed to be a major class of molecular alteration in colon polyps and colorectal cancer over last 30 year. The classes of epigenetic alterations, their status in colorectal polyps and cancer, their effects on neoplasm biology, and their application to clinical care will be discussed.
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Abbreviations
- CRC :
-
Colorectal cancer
- SSL :
-
Serrated sessile lesions
- miRNAs :
-
microRNA
- MSI :
-
Microsatellite instability
- DNMTs :
-
DNA methyltransferases
- MBD :
-
Methyl-CpG-binding domain
- CIMP :
-
CpG island methylator phenotype
- TET :
-
Ten-eleven translocation
- IDH1:
-
Isocitrate dehydrogenase
- SSP :
-
Sessile serrated polyps
- FIT :
-
Fecal immunochemical test
- SWI/SNF :
-
Switching defective/sucrosenon-fermenting complex
- PR C2:
-
Polycomb repressive complex 2
- Ago-2:
-
Argonaute-2
- DMA :
-
Direct miRNA analysis
References
Ahn JB, Chung WB, Maeda O et al (2011) DNA methylation predicts recurrence from resected stage III proximal colon cancer. Cancer. 117(9):1847–1854. https://doi.org/10.1002/cncr.25737
Akao Y, Noguchi S, Iio A, Kojima K, Takagi T, Naoe T (2011) Dysregulation of microRNA-34a expression causes drug-resistance to 5-FU in human colon cancer DLD-1 cells. Cancer Lett. 300(2):197–204. https://doi.org/10.1016/j.canlet.2010.10.006
Antelo M, Balaguer F, Shia J et al (2012) A High Degree of LINE-1 Hypomethylation Is a Unique Feature of Early-Onset Colorectal Cancer. PLOS ONE. 7(9):e45357. https://doi.org/10.1371/journal.pone.0045357
Arndt GM, Dossey L, Cullen LM et al (2009) Characterization of global microRNA expression reveals oncogenic potential of miR-145 in metastatic colorectal cancer. BMC Cancer. 9(1):374. https://doi.org/10.1186/1471-2407-9-374
Arroyo JD, Chevillet JR, Kroh EM et al (2011) Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci. 108(12):5003–5008. https://doi.org/10.1073/pnas.1019055108
Baba Y, Nosho K, Shima K et al (2010) HIF1A Overexpression Is Associated with Poor Prognosis in a Cohort of 731 Colorectal Cancers. Am J Pathol. 176(5):2292–2301. https://doi.org/10.2353/ajpath.2010.090972
Bardelli A, Siena S (2010) Molecular Mechanisms of Resistance to Cetuximab and Panitumumab in Colorectal Cancer. J Clin Oncol. 28(7):1254–1261. https://doi.org/10.1200/JCO.2009.24.6116
Barták BK, Kalmár A, Péterfia B et al (2017) Colorectal adenoma and cancer detection based on altered methylation pattern of SFRP1, SFRP2, SDC2, and PRIMA1 in plasma samples. Epigenetics. 12(9):751–763. https://doi.org/10.1080/15592294.2017.1356957
Bartke T, Kouzarides T (2011) Decoding the chromatin modification landscape. Cell Cycle. 10(2):182–182. https://doi.org/10.4161/cc.10.2.14477
Bártová E, Krejčí J, Harničarová A, Galiová G, Kozubek S (2008) Histone Modifications and Nuclear Architecture: A Review. J Histochem Cytochem. 56(8):711–721. https://doi.org/10.1369/jhc.2008.951251
Baylin SB, Herman JG (2000) DNA hypermethylation in tumorigenesis: epigenetics joins genetics. Trends Genet. 16(4):168–174. https://doi.org/10.1016/S0168-9525(99)01971-X
Baylin SB, Jones PA (2011) A decade of exploring the cancer epigenome — biological and translational implications. Nat Rev Cancer. 11(10):726–734. https://doi.org/10.1038/nrc3130
Benard A, Goossens-Beumer IJ, van Hoesel AQ et al (2014a) Histone trimethylation at H3K4, H3K9 and H4K20 correlates with patient survival and tumor recurrence in early-stage colon cancer. BMC Cancer. 14(1):531. https://doi.org/10.1186/1471-2407-14-531
Benard A, Goossens-Beumer IJ, van Hoesel AQ et al (2015) Nuclear expression of histone deacetylases and their histone modifications predicts clinical outcome in colorectal cancer. Histopathology. 66(2):270–282. https://doi.org/10.1111/his.12534
Benard A, Goossens-Beumer IJ, van Hoesel AQ et al (2014b) Prognostic value of polycomb proteins EZH2, BMI1 and SUZ12 and histone modification H3K27me3 in colorectal cancer. Plos One. 9(9):e108265. https://doi.org/10.1371/journal.pone.0108265
Benson AB, Schrag D, Somerfield MR et al (2004) American Society of Clinical Oncology Recommendations on Adjuvant Chemotherapy for Stage II Colon Cancer. J Clin Oncol. 22(16):3408–3419. https://doi.org/10.1200/JCO.2004.05.063
Bersaglieri C, Santoro R (2019) Genome Organization in and around the Nucleolus. Cells. 8(6):579. https://doi.org/10.3390/cells8060579
Bettington M, Rosty C, Whitehall V et al (2018) A morphological and molecular study of proposed early forms of traditional serrated adenoma. Histopathology. 73(6):1023–1029. https://doi.org/10.1111/his.13714
Bettington M, Walker N, Clouston A, Brown I, Leggett B, Whitehall V (2013) The serrated pathway to colorectal carcinoma: current concepts and challenges. Histopathology. 62(3):367–386. https://doi.org/10.1111/his.12055
Bi F, Wang Q, Dong Q, Wang Y, Zhang L, Zhang J (2020) Circulating tumor DNA in colorectal cancer: opportunities and challenges. Am J Transl Res. 12(3):1044–1055
Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev. 16(1):6–21. https://doi.org/10.1101/gad.947102
Bitarte N, Bandres E, Boni V et al (2011) MicroRNA-451 Is Involved in the Self-renewal, Tumorigenicity, and Chemoresistance of Colorectal Cancer Stem Cells. Stem Cells. 29(11):1661–1671. https://doi.org/10.1002/stem.741
Boni V, Bitarte N, Cristobal I et al (2010) miR-192/miR-215 Influence 5-Fluorouracil Resistance through Cell Cycle-Mediated Mechanisms Complementary to Its Post-transcriptional Thymidilate Synthase Regulation. Mol Cancer Ther. 9(8):2265–2275. https://doi.org/10.1158/1535-7163.MCT-10-0061
Bovell LC, Shanmugam C, Putcha BDK et al (2013) The Prognostic Value of MicroRNAs Varies with Patient Race/Ethnicity and Stage of Colorectal Cancer. Clin Cancer Res. 19(14):3955–3965. https://doi.org/10.1158/1078-0432.CCR-12-3302
Cairns RA, Mak TW (2013) Oncogenic Isocitrate Dehydrogenase Mutations: Mechanisms, Models, and Clinical Opportunities. Cancer Discov. 3(7):730–741. https://doi.org/10.1158/2159-8290.CD-13-0083
Calin GA, Croce CM (2006) MicroRNA signatures in human cancers. Nat Rev Cancer. 6(11):857–866. https://doi.org/10.1038/nrc1997
Calin GA, Dumitru CD, Shimizu M et al (2002) Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci. 99(24):15524–15529. https://doi.org/10.1073/pnas.242606799
Carethers JM, Jung BH (2015) Genetics and Genetic Biomarkers in Sporadic Colorectal Cancer. Gastroenterology. 149(5):1177–1190.e3. https://doi.org/10.1053/j.gastro.2015.06.047
Chan AOO, Broaddus RR, Houlihan PS, Issa JPJ, Hamilton SR, Rashid A (2002) CpG Island Methylation in Aberrant Crypt Foci of the Colorectum. Am J Pathol. 160(5):1823–1830. https://doi.org/10.1016/S0002-9440(10)61128-5
Chen JH, Herlong FR, Stroehlein J, Mishra L (2016) Mutations of Chromatin Structure Regulating Genes in Human Malignancies. Curr Protein Pept Sci. 17(5):411–437
Chen RZ, Pettersson U, Beard C, Jackson-Grusby L, Jaenisch R (1998) DNA hypomethylation leads to elevated mutation rates. Nature. 395(6697):89–93. https://doi.org/10.1038/25779
Chen WD, Han ZJ, Skoletsky J et al (2005) Detection in fecal DNA of colon cancer–specific methylation of the nonexpressed vimentin gene. JNCI J Natl Cancer Inst. 97(15):1124–1132. https://doi.org/10.1093/jnci/dji204
Cohen I, Poręba E, Kamieniarz K, Schneider R (2011) Histone modifiers in cancer: friends or foes? Genes Cancer. 2(6):631–647. https://doi.org/10.1177/1947601911417176
Creemers EE, Tijsen AJ, Pinto YM, van Rooij E (2012) Circulating MicroRNAs. Circ Res. 110(3):483–495. https://doi.org/10.1161/CIRCRESAHA.111.247452
Crockett SD, Nagtegaal ID (2019) Terminology, molecular features, epidemiology, and management of serrated colorectal neoplasia. Gastroenterology. 157(4):949–966.e4. https://doi.org/10.1053/j.gastro.2019.06.041
Cui H, Onyango P, Brandenburg S, Wu Y, Hsieh CL, Feinberg AP (2002) Loss of imprinting in colorectal cancer linked to hypomethylation of H19 and IGF2. Cancer Res. 62(22):6442–6446
Cunningham D, Humblet Y, Siena S et al (2004) Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer. N Engl J Med. 351(4):337–345. https://doi.org/10.1056/NEJMoa033025
Deng J, Lei W, Fu JC, Zhang L, Li JH, Xiong JP (2014) Targeting miR-21 enhances the sensitivity of human colon cancer HT-29 cells to chemoradiotherapy in vitro. Biochem Biophys Res Commun. 443(3):789–795. https://doi.org/10.1016/j.bbrc.2013.11.064
Dhir M, Yachida S, Neste LV et al (2011) Sessile serrated adenomas and classical adenomas: An epigenetic perspective on premalignant neoplastic lesions of the gastrointestinal tract. Int J Cancer. 129(8):1889–1898. https://doi.org/10.1002/ijc.25847
Draht MXG, Smits KM, Tournier B et al (2014) Promoter CpG island methylation of RET predicts poor prognosis in stage II colorectal cancer patients. Mol Oncol. 8(3):679–688. https://doi.org/10.1016/j.molonc.2014.01.011
Duran-Sanchon S, Moreno L, Augé JM et al (2020) Identification and validation of microRNA profiles in fecal samples for detection of colorectal cancer. Gastroenterology. 158(4):947–957.e4. https://doi.org/10.1053/j.gastro.2019.10.005
Duran-Sanchon S, Moreno L, Gómez-Matas J et al (2021) Fecal MicroRNA-based algorithm increases effectiveness of fecal immunochemical test–based screening for colorectal cancer. Clin Gastroenterol Hepatol. 19(2):323–330.e1. https://doi.org/10.1016/j.cgh.2020.02.043
Ebert MPA, Model F, Mooney S et al (2006) Aristaless-like homeobox-4 gene methylation is a potential marker for colorectal adenocarcinomas. Gastroenterology. 131(5):1418–1430. https://doi.org/10.1053/j.gastro.2006.08.034
Ebert MPA, Tänzer M, Balluff B et al (2012) TFAP2E–DKK4 and chemoresistance in colorectal cancer. N Engl J Med. 366(1):44–53. https://doi.org/10.1056/NEJMoa1009473
El Messaoudi S, Mouliere F, Du Manoir S et al (2016) Circulating DNA as a strong multimarker prognostic tool for metastatic colorectal cancer patient management care. Clin Cancer Res. 22(12):3067–3077. https://doi.org/10.1158/1078-0432.CCR-15-0297
Estécio MRH, Gharibyan V, Shen L et al (2007) LINE-1 Hypomethylation in cancer is highly variable and inversely correlated with microsatellite instability. PLOS ONE. 2(5):e399. https://doi.org/10.1371/journal.pone.0000399
Esteller M, Toyota M, Sanchez-Cespedes M et al (2000) Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is associated with G to A mutations in K-ras in colorectal tumorigenesis. Cancer Res. 60(9):2368–2371
Faltejskova P, Besse A, Sevcikova S et al (2012) Clinical correlations of miR-21 expression in colorectal cancer patients and effects of its inhibition on DLD1 colon cancer cells. Int J Colorectal Dis. 27(11):1401–1408. https://doi.org/10.1007/s00384-012-1461-3
Fang L, Li H, Wang L et al (2014) MicroRNA-17-5p promotes chemotherapeutic drug resistance and tumour metastasis of colorectal cancer by repressing PTEN expression. Oncotarget. 5(10):2974–2987. https://doi.org/10.18632/oncotarget.1614
Fearon ER, Vogelstein B (1990) A genetic model for colorectal tumorigenesis. Cell. 61(5):759–767. https://doi.org/10.1016/0092-8674(90)90186-I
Figueredo A, Coombes ME, Mukherjee S (2008) Adjuvant therapy for completely resected stage II colon cancer. Cochrane Database Syst Rev. 3. https://doi.org/10.1002/14651858.CD005390.pub2
Finger FP (2002) One ring to bind them: septins and actin assembly. Dev Cell. 3(6):761–763. https://doi.org/10.1016/S1534-5807(02)00371-4
Fraga MF, Ballestar E, Villar-Garea A et al (2005) Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet. 37(4):391–400. https://doi.org/10.1038/ng1531
Gallois C, Taieb J, Le Corre D et al (2018) Prognostic value of methylator phenotype in stage III colon cancer treated with oxaliplatin-based adjuvant chemotherapy. Clin Cancer Res. 24(19):4745–4753. https://doi.org/10.1158/1078-0432.CCR-18-0866
Gaudet F, Hodgson JG, Eden A et al (2003) Induction of tumors in mice by genomic hypomethylation. Science. 300(5618):489–492. https://doi.org/10.1126/science.1083558
Gezer U, Üstek D, Yörüker EE et al (2013) Characterization of H3K9me3- and H4K20me3-associated circulating nucleosomal DNA by high-throughput sequencing in colorectal cancer. Tumor Biol. 34(1):329–336. https://doi.org/10.1007/s13277-012-0554-5
Gilbert N (2019) Biophysical regulation of local chromatin structure. Curr Opin Genet Dev. 55:66–75. https://doi.org/10.1016/j.gde.2019.06.001
Glöckner SC, Dhir M, Yi JM et al (2009) Methylation of TFPI2 in Stool DNA: a potential novel biomarker for the detection of colorectal cancer. Cancer Res. 69(11):4691–4699. https://doi.org/10.1158/0008-5472.CAN-08-0142
Goel A, Xicola RM, Nguyen T et al (2010) Aberrant DNA methylation in hereditary nonpolyposis colorectal cancer without mismatch repair deficiency. Gastroenterology. 138(5):1854–1862.e1. https://doi.org/10.1053/j.gastro.2010.01.035
Grady WM, Carethers JM (2008) Genomic and epigenetic instability in colorectal cancer pathogenesis. Gastroenterology. 135(4):1079–1099. https://doi.org/10.1053/j.gastro.2008.07.076
Grady WM, Parkin RK, Mitchell PS et al (2008) Epigenetic silencing of the intronic microRNA hsa-miR-342 and its host gene EVL in colorectal cancer. Oncogene. 27(27):3880–3888. https://doi.org/10.1038/onc.2008.10
Gregory PA, Bracken CP, Smith E et al (2011) An autocrine TGF-β/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol Biol Cell. 22(10):1686–1698. https://doi.org/10.1091/mbc.e11-02-0103
Guo ST, Jiang CC, Wang GP et al (2013) MicroRNA-497 targets insulin-like growth factor 1 receptor and has a tumour suppressive role in human colorectal cancer. Oncogene. 32(15):1910–1920. https://doi.org/10.1038/onc.2012.214
Hadley M, Noonepalle S, Banik D, Villagra A (2019) Functional analysis of HDACs in tumorigenesis. In: Brosh RM (ed) Protein acetylation: methods and protocols, Methods in molecular biology. Springer, pp 279–307. https://doi.org/10.1007/978-1-4939-9434-2_17
Hampel H, Frankel WL, Martin E et al (2005) Screening for the lynch syndrome (hereditary nonpolyposis colorectal cancer). N Engl J Med. 352(18):1851–1860. https://doi.org/10.1056/NEJMoa043146
Hampel H, Frankel WL, Martin E et al (2008) Feasibility of screening for lynch syndrome among patients with colorectal cancer. J Clin Oncol. 26(35):5783–5788. https://doi.org/10.1200/JCO.2008.17.5950
Hansen TF, Kjær-Frifeldt S, Christensen RD et al (2014) Redefining high-risk patients with stage II colon cancer by risk index and microRNA-21: results from a population-based cohort. Br J Cancer. 111(7):1285–1292. https://doi.org/10.1038/bjc.2014.409
Hawkins N, Norrie M, Cheong K et al (2002) CpG island methylation in sporadic colorectal cancers and its relationship to microsatellite instability. Gastroenterology. 122(5):1376–1387. https://doi.org/10.1053/gast.2002.32997
He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet. 5(7):522–531. https://doi.org/10.1038/nrg1379
Herbst A, Rahmig K, Stieber P et al (2011) Methylation of NEUROG1 in serum is a sensitive marker for the detection of early colorectal cancer. Off J Am Coll Gastroenterol ACG. 106(6):1110. https://doi.org/10.1038/ajg.2011.6
Holm TM, Jackson-Grusby L, Brambrink T, Yamada Y, Rideout WM, Jaenisch R (2005) Global loss of imprinting leads to widespread tumorigenesis in adult mice. Cancer Cell. 8(4):275–285. https://doi.org/10.1016/j.ccr.2005.09.007
Huang Z, Huang D, Ni S, Peng Z, Sheng W, Du X (2010) Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer. Int J Cancer. 127(1):118–126. https://doi.org/10.1002/ijc.25007
Hur K, Cejas P, Feliu J et al (2014) Hypomethylation of long interspersed nuclear element-1 (LINE-1) leads to activation of proto-oncogenes in human colorectal cancer metastasis. Gut. 63(4):635–646. https://doi.org/10.1136/gutjnl-2012-304219
Hurwitz H, Fehrenbacher L, Novotny W et al (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med. 350(23):2335–2342. https://doi.org/10.1056/NEJMoa032691
Igarashi H, Kurihara H, Mitsuhashi K et al (2015) Association of microRNA-31-5p with clinical efficacy of anti-EGFR therapy in patients with metastatic colorectal cancer. Ann Surg Oncol. 22(8):2640–2648. https://doi.org/10.1245/s10434-014-4264-7
Imperiale TF, Ransohoff DF, Itzkowitz SH et al (2014) Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med. 370(14):1287–1297. https://doi.org/10.1056/NEJMoa1311194
Issa JPJ, Ottaviano YL, Celano P, Hamilton SR, Davidson NE, Baylin SB (1994) Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat Genet. 7(4):536–540. https://doi.org/10.1038/ng0894-536
Ito M, Mitsuhashi K, Igarashi H et al (2014) MicroRNA-31 expression in relation to BRAF mutation, CpG island methylation and colorectal continuum in serrated lesions. Int J Cancer. 135(11):2507–2515. https://doi.org/10.1002/ijc.28920
Itzkowitz S, Brand R, Jandorf L et al (2008) A simplified, noninvasive stool dna test for colorectal cancer detection. Off J Am Coll Gastroenterol ACG. 103(11):2862
Itzkowitz SH, Jandorf L, Brand R et al (2007) Improved fecal DNA test for colorectal cancer screening. Clin Gastroenterol Hepatol. 5(1):111–117. https://doi.org/10.1016/j.cgh.2006.10.006
Jin P, Kang Q, Wang X et al (2015) Performance of a second-generation methylated SEPT9 test in detecting colorectal neoplasm. J Gastroenterol Hepatol. 30(5):830–833. https://doi.org/10.1111/jgh.12855
Jinushi T, Shibayama Y, Kinoshita I et al (2014) Low expression levels of microRNA-124-5p correlated with poor prognosis in colorectal cancer via targeting of SMC4. Cancer Med. 3(6):1544–1552. https://doi.org/10.1002/cam4.309
Johnson SM, Grosshans H, Shingara J et al (2005) RAS Is Regulated by the let-7 MicroRNA Family. Cell. 120(5):635–647. https://doi.org/10.1016/j.cell.2005.01.014
Josse C, Bouznad N, Geurts P et al (2014) Identification of a microRNA landscape targeting the PI3K/Akt signaling pathway in inflammation-induced colorectal carcinogenesis. Am J Physiol-Gastrointest Liver Physiol. 306(3):G229–G243. https://doi.org/10.1152/ajpgi.00484.2012
Jover R, Nguyen T, Pérez-Carbonell L et al (2011) 5-fluorouracil adjuvant chemotherapy does not increase survival in patients with CpG island methylator phenotype colorectal cancer. Gastroenterology. 140(4):1174–1181. https://doi.org/10.1053/j.gastro.2010.12.035
Juo YY, Johnston FM, Zhang DY et al (2014) Prognostic value of CpG island methylator phenotype among colorectal cancer patients: a systematic review and meta-analysis. Ann Oncol. 25(12):2314–2327. https://doi.org/10.1093/annonc/mdu149
Kamakaka RT, Biggins S (2005) Histone variants: deviants? Genes Dev. 19(3):295–316. https://doi.org/10.1101/gad.1272805
Kamiyama H, Suzuki K, Maeda T et al (2012) DNA demethylation in normal colon tissue predicts predisposition to multiple cancers. Oncogene. 31(48):5029–5037. https://doi.org/10.1038/onc.2011.652
Kanaan Z, Rai SN, Eichenberger MR et al (2012) Plasma MiR-21: A Potential Diagnostic Marker of Colorectal Cancer. Ann Surg. 256(3):544. https://doi.org/10.1097/SLA.0b013e318265bd6f
Kanaan Z, Roberts H, Eichenberger MR et al (2013) A plasma microRNA panel for detection of colorectal adenomas: a step toward more precise screening for colorectal cancer. Ann Surg. 258(3):400. https://doi.org/10.1097/SLA.0b013e3182a15bcc
Kanwal R, Gupta S (2010) Epigenetics and cancer. J Appl Physiol. 109(2):598–605. https://doi.org/10.1152/japplphysiol.00066.2010
Karaayvaz M, Zhai H, Ju J (2013) miR-129 promotes apoptosis and enhances chemosensitivity to 5-fluorouracil in colorectal cancer. Cell Death Dis. 4(6):e659–e659. https://doi.org/10.1038/cddis.2013.193
Kawakami K, Ruszkiewicz A, Bennett G et al (2006) DNA hypermethylation in the normal colonic mucosa of patients with colorectal cancer. Br J Cancer. 94(4):593–598. https://doi.org/10.1038/sj.bjc.6602940
Kim JK, Samaranayake M, Pradhan S (2008) Epigenetic mechanisms in mammals. Cell Mol Life Sci. 66(4):596. https://doi.org/10.1007/s00018-008-8432-4
Kim ST, Raymond VM, Park JO et al (2019) Abstract 916: Combined genomic and epigenomic assessment of cell-free circulating tumor DNA (ctDNA) improves assay sensitivity in early-stage colorectal cancer (CRC). Cancer Res. 79(13_Supplement):916. https://doi.org/10.1158/1538-7445.AM2019-916
King CE, Cuatrecasas M, Castells A, Sepulveda AR, Lee JS, Rustgi AK (2011) LIN28B promotes colon cancer progression and metastasis. Cancer Res. 71(12):4260–4268. https://doi.org/10.1158/0008-5472.CAN-10-4637
Kjaer-Frifeldt S, Hansen TF, Nielsen BS et al (2012) The prognostic importance of miR-21 in stage II colon cancer: a population-based study. Br J Cancer. 107(7):1169–1174. https://doi.org/10.1038/bjc.2012.365
Koga Y, Yamazaki N, Yamamoto Y et al (2013) Fecal miR-106a Is a useful marker for colorectal cancer patients with false-negative results in immunochemical fecal occult blood test. Cancer Epidemiol Biomarkers Prev. 22(10):1844–1852. https://doi.org/10.1158/1055-9965.EPI-13-0512
Kohonen-Corish MRJ, Sigglekow ND, Susanto J et al (2007) Promoter methylation of the mutated in colorectal cancer gene is a frequent early event in colorectal cancer. Oncogene. 26(30):4435–4441. https://doi.org/10.1038/sj.onc.1210210
Komor MA, Bosch LJ, Bounova G et al (2018) Consensus molecular subtype classification of colorectal adenomas. J Pathol. 246(3):266–276. https://doi.org/10.1002/path.5129
Kouzarides T (2007) Chromatin Modifications and Their Function. Cell. 128(4):693–705. https://doi.org/10.1016/j.cell.2007.02.005
Kriaucionis S, Heintz N (2009) The nuclear DNA Base 5-hydroxymethylcytosine is present in purkinje neurons and the brain. Science. 324(5929):929–930. https://doi.org/10.1126/science.1169786
Kriegl L, Neumann J, Vieth M et al (2011) Up and downregulation of p16Ink4a expression in BRAF-mutated polyps/adenomas indicates a senescence barrier in the serrated route to colon cancer. Mod Pathol. 24(7):1015–1022. https://doi.org/10.1038/modpathol.2011.43
Kuipers EJ, Grady WM, Lieberman D et al (2015) Colorectal cancer. Nat Rev Dis Primer. 1(1):1–25. https://doi.org/10.1038/nrdp.2015.65
Kulda V, Pesta M, Topolcan O et al (2010) Relevance of miR-21 and miR-143 expression in tissue samples of colorectal carcinoma and its liver metastases. Cancer Genet Cytogenet. 200(2):154–160. https://doi.org/10.1016/j.cancergencyto.2010.04.015
Kurokawa K, Tanahashi T, Iima T et al (2012) Role of miR-19b and its target mRNAs in 5-fluorouracil resistance in colon cancer cells. J Gastroenterol. 47(8):883–895. https://doi.org/10.1007/s00535-012-0547-6
Laiho P, Kokko A, Vanharanta S et al (2007) Serrated carcinomas form a subclass of colorectal cancer with distinct molecular basis. Oncogene. 26(2):312–320. https://doi.org/10.1038/sj.onc.1209778
Lee BB, Lee EJ, Jung EH et al (2009) Aberrant methylation of APC, MGMT, RASSF2A, and Wif-1 genes in plasma as a biomarker for early detection of colorectal cancer. Clin Cancer Res. 15(19):6185–6191. https://doi.org/10.1158/1078-0432.CCR-09-0111
Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 75(5):843–854. https://doi.org/10.1016/0092-8674(93)90529-y
Lee S, Cho NY, Yoo EJ, Kim JH, Kang GH (2008) CpG Island methylator phenotype in colorectal cancers: comparison of the new and classic CpG Island methylator phenotype marker panels. Arch Pathol Lab Med. 132(10):1657–1665. https://doi.org/10.5858/2008-132-1657-CIMPIC
Leighton G, Williams DC (2020) The Methyl-CpG–binding domain 2 and 3 proteins and formation of the nucleosome remodeling and deacetylase complex. J Mol Biol. 432(6):1624–1639. https://doi.org/10.1016/j.jmb.2019.10.007
Leszinski G, Gezer U, Siegele B, Stoetzer O, Holdenrieder S (2012) Relevance of histone marks H3K9me3 and H4K20me3 in cancer. Anticancer Res. 32(5):2199–2205
Leung WK, To KF, Man EPS et al (2005) Quantitative detection of promoter hypermethylation in multiple genes in the serum of patients with colorectal cancer. Off J Am Coll Gastroenterol ACG. 100(10):2274
Leung WK, To KF, Man EPS et al (2007) Detection of hypermethylated DNA or cyclooxygenase-2 messenger RNA in fecal samples of patients with colorectal cancer or polyps. Off J Am Coll Gastroenterol ACG. 102(5):1070
Li H, Myeroff L, Smiraglia D et al (2003) SLC5A8, a sodium transporter, is a tumor suppressor gene silenced by methylation in human colon aberrant crypt foci and cancers. Proc Natl Acad Sci. 100(14):8412–8417. https://doi.org/10.1073/pnas.1430846100
Li W, Liu M (2011) Distribution of 5-hydroxymethylcytosine in different human tissues. J Nucleic Acids. 2011:e870726. https://doi.org/10.4061/2011/870726
Lidgard GP, Domanico MJ, Bruinsma JJ et al (2013) Clinical performance of an automated stool DNA assay for detection of colorectal neoplasia. Clin Gastroenterol Hepatol. 11(10):1313–1318. https://doi.org/10.1016/j.cgh.2013.04.023
Link A, Balaguer F, Shen Y et al (2010) Fecal MicroRNAs as novel biomarkers for colon cancer screening. Cancer Epidemiol Biomarkers Prev. 19(7):1766–1774. https://doi.org/10.1158/1055-9965.EPI-10-0027
Liu F, Kong X, Lv L, Gao J (2015) TGF-β1 acts through miR-155 to down-regulate TP53INP1 in promoting epithelial-mesenchymal transition and cancer stem cell phenotypes. Cancer Lett. 359(2):288–298. https://doi.org/10.1016/j.canlet.2015.01.030
Liu GH, Zhou ZG, Chen R et al (2013a) Serum miR-21 and miR-92a as biomarkers in the diagnosis and prognosis of colorectal cancer. Tumor Biol. 34(4):2175–2181. https://doi.org/10.1007/s13277-013-0753-8
Liu H, Du L, Wen Z et al (2013b) Up-regulation of miR-182 expression in colorectal cancer tissues and its prognostic value. Int J Colorectal Dis. 28(5):697–703. https://doi.org/10.1007/s00384-013-1674-0
Liu K, Li G, Fan C, Zhou X, Wu B, Li J (2011) Increased expression of MicroRNA-21 and its association with chemotherapeutic response in human colorectal cancer. J Int Med Res. 39(6):2288–2295. https://doi.org/10.1177/147323001103900626
Liu Y, Sethi NS, Hinoue T et al (2018) Comparative molecular analysis of gastrointestinal adenocarcinomas. Cancer Cell. 33(4):721–735.e8. https://doi.org/10.1016/j.ccell.2018.03.010
Lochhead P, Kuchiba A, Imamura Y et al (2013) Microsatellite instability and BRAF mutation testing in colorectal cancer prognostication. JNCI J Natl Cancer Inst. 105(15):1151–1156. https://doi.org/10.1093/jnci/djt173
Lofton-Day C, Model F, DeVos T et al (2008) DNA methylation biomarkers for blood-based colorectal cancer screening. Clin Chem. 54(2):414–423. https://doi.org/10.1373/clinchem.2007.095992
Luo X, Stock C, Burwinkel B, Brenner H (2013) Identification and evaluation of plasma microRNAs for early detection of colorectal cancer. PLOS ONE. 8(5):e62880. https://doi.org/10.1371/journal.pone.0062880
Luo Y, Yu M, Grady WM (2014) Field cancerization in the colon: a role for aberrant DNA methylation? Gastroenterol Rep. 2(1):16–20. https://doi.org/10.1093/gastro/got039
Manceau G, Imbeaud S, Thiébaut R et al (2014) Hsa-miR-31-3p Expression Is Linked to Progression-free Survival in Patients with KRAS Wild-type Metastatic Colorectal Cancer Treated with Anti-EGFR Therapy. Clin Cancer Res. 20(12):3338–3347. https://doi.org/10.1158/1078-0432.CCR-13-2750
Mendell JT (2005) MicroRNAs: critical regulators of development, cellular physiology and malignancy. Cell Cycle. 4(9):1179–1184. https://doi.org/10.4161/cc.4.9.2032
Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T (2007) MicroRNA-21 Regulates Expression of the PTEN Tumor Suppressor Gene in Human Hepatocellular Cancer. Gastroenterology. 133(2):647–658. https://doi.org/10.1053/j.gastro.2007.05.022
Mills AA (2010) Throwing the cancer switch: reciprocal roles of polycomb and trithorax proteins. Nat Rev Cancer. 10(10):669–682. https://doi.org/10.1038/nrc2931
Min BH, Bae JM, Lee EJ et al (2011) The CpG island methylator phenotype may confer a survival benefit in patients with stage II or III colorectal carcinomas receiving fluoropyrimidine-based adjuvant chemotherapy. BMC Cancer. 11(1):1–10. https://doi.org/10.1186/1471-2407-11-344
Moinova HR, Chen WD, Shen L et al (2002) HLTF gene silencing in human colon cancer. Proc Natl Acad Sci. 99(7):4562–4567. https://doi.org/10.1073/pnas.062459899
Motoyama K, Inoue H, Takatsuno Y et al (2009) Over- and under-expressed microRNAs in human colorectal cancer. Int J Oncol. 34(4):1069–1075. https://doi.org/10.3892/ijo_00000233
Moutinho C, Martinez-Cardús A, Santos C et al (2014) Epigenetic Inactivation of the BRCA1 interactor srbc and resistance to oxaliplatin in colorectal cancer. JNCI: J Natl Cancer Inst. 106(1):djt322. https://doi.org/10.1093/jnci/djt322
Myint NNM, Verma AM, Fernandez-Garcia D et al (2018) Circulating tumor DNA in patients with colorectal adenomas: assessment of detectability and genetic heterogeneity. Cell Death Dis. 9(9):1–16. https://doi.org/10.1038/s41419-018-0934-x
Nagasaka T, Sharp GB, Notohara K et al (2003) Hypermethylation of O6-methylguanine-DNA methyltransferase promoter may predict nonrecurrence after chemotherapy in colorectal cancer cases. Clin Cancer Res Off J Am Assoc Cancer Res. 9(14):5306–5312
Nagel R, le Sage C, Diosdado B et al (2008) Regulation of the adenomatous polyposis Coli gene by the miR-135 family in colorectal cancer. Cancer Res. 68(14):5795–5802. https://doi.org/10.1158/0008-5472.CAN-08-0951
Nakajima G, Hayashi K, Xi Y et al (2006) Non-coding MicroRNAs hsa-let-7g and hsa-miR-181b are associated with chemoresponse to S-1 in colon cancer. Cancer Genomics Proteomics. 3(5):317–324
Neri F, Dettori D, Incarnato D et al (2015) TET1 is a tumour suppressor that inhibits colon cancer growth by derepressing inhibitors of the WNT pathway. Oncogene. 34(32):4168–4176. https://doi.org/10.1038/onc.2014.356
Nielsen BS, Jørgensen S, Fog JU et al (2011) High levels of microRNA-21 in the stroma of colorectal cancers predict short disease-free survival in stage II colon cancer patients. Clin Exp Metastasis. 28(1):27–38. https://doi.org/10.1007/s10585-010-9355-7
Nikolaou S, Qiu S, Fiorentino F, Rasheed S, Tekkis P, Kontovounisios C (2018) Systematic review of blood diagnostic markers in colorectal cancer. Tech Coloproctology. 22(7):481–498. https://doi.org/10.1007/s10151-018-1820-3
Nilsson TK, Löf-Öhlin ZM, Sun XF (2013) DNA methylation of the p14ARF, RASSF1A and APC1A genes as an independent prognostic factor in colorectal cancer patients. Int J Oncol. 42(1):127–133. https://doi.org/10.3892/ijo.2012.1682
Nishida N, Yamashita S, Mimori K et al (2012) MicroRNA-10b is a prognostic indicator in colorectal cancer and confers resistance to the chemotherapeutic agent 5-fluorouracil in colorectal cancer cells. Ann Surg Oncol. 19(9):3065–3071. https://doi.org/10.1245/s10434-012-2246-1
Nosho K, Igarashi H, Nojima M et al (2014) Association of microRNA-31 with BRAF mutation, colorectal cancer survival and serrated pathway. Carcinogenesis. 35(4):776–783. https://doi.org/10.1093/carcin/bgt374
Oberg AL, French AJ, Sarver AL et al (2011) miRNA expression in colon polyps provides evidence for a multihit model of colon cancer. PLOS ONE. 6(6):e20465. https://doi.org/10.1371/journal.pone.0020465
Ogata-Kawata H, Izumiya M, Kurioka D et al (2014) Circulating exosomal microRNAs as biomarkers of colon cancer. PLOS ONE. 9(4):e92921. https://doi.org/10.1371/journal.pone.0092921
Ogino S, Kawasaki T, Nosho K et al (2008a) LINE-1 hypomethylation is inversely associated with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Int J Cancer. 122(12):2767–2773. https://doi.org/10.1002/ijc.23470
Ogino S, Meyerhardt JA, Kawasaki T et al (2007) CpG island methylation, response to combination chemotherapy, and patient survival in advanced microsatellite stable colorectal carcinoma. Virchows Arch. 450(5):529–537. https://doi.org/10.1007/s00428-007-0398-3
Ogino S, Nosho K, Kirkner GJ et al (2008b) A cohort study of tumoral LINE-1 hypomethylation and prognosis in colon cancer. JNCI J Natl Cancer Inst. 100(23):1734–1738. https://doi.org/10.1093/jnci/djn359
Okugawa Y, Grady WM, Goel A (2015) Epigenetic alterations in colorectal cancer: emerging biomarkers. Gastroenterology. 149(5):1204–1225.e12. https://doi.org/10.1053/j.gastro.2015.07.011
Oue N, Anami K, Schetter AJ et al (2014) High miR-21 expression from FFPE tissues is associated with poor survival and response to adjuvant chemotherapy in colon cancer. Int J Cancer. 134(8):1926–1934. https://doi.org/10.1002/ijc.28522
Pagliuca A, Valvo C, Fabrizi E et al (2013) Analysis of the combined action of miR-143 and miR-145 on oncogenic pathways in colorectal cancer cells reveals a coordinate program of gene repression. Oncogene. 32(40):4806–4813. https://doi.org/10.1038/onc.2012.495
Pai RK, Bettington M, Srivastava A, Rosty C (2019) An update on the morphology and molecular pathology of serrated colorectal polyps and associated carcinomas. Mod Pathol. 32(10):1390–1415. https://doi.org/10.1038/s41379-019-0280-2
Papagiannakopoulos T, Shapiro A, Kosik KS (2008) MicroRNA-21 Targets a Network of Key Tumor-Suppressive Pathways in Glioblastoma Cells. Cancer Res. 68(19):8164–8172. https://doi.org/10.1158/0008-5472.CAN-08-1305
Park SJ, Kim S, Hong YS et al (2015) TFAP2E Methylation Status and Prognosis of Patients with Radically Resected Colorectal Cancer. Oncology. 88(2):122–132. https://doi.org/10.1159/000362820
Peng L, Hu J, Li S et al (2013) Aberrant methylation of the PTCH1 gene promoter region in aberrant crypt foci. Int J Cancer. 132(2):E18–E25. https://doi.org/10.1002/ijc.27812
Petko Z, Ghiassi M, Shuber A et al (2005) Aberrantly methylated CDKN2A, MGMT, and MLH1 in colon polyps and in Fecal DNA from patients with colorectal polyps. Clin Cancer Res. 11(3):1203–1209. https://doi.org/10.1158/1078-0432.1203.11.3
Picardo F, Romanelli A, Muinelo-Romay L et al (2019) Diagnostic and prognostic value of B4GALT1 hypermethylation and its clinical significance as a novel circulating cell-free DNA biomarker in colorectal cancer. Cancers. 11(10):1598. https://doi.org/10.3390/cancers11101598
Popat S, Hubner R, Houlston RS (2005) Systematic review of microsatellite instability and colorectal cancer prognosis. J Clin Oncol Off J Am Soc Clin Oncol. 23(3):609–618. https://doi.org/10.1200/JCO.2005.01.086
Portela A, Esteller M (2010) Epigenetic modifications and human disease. Nat Biotechnol. 28(10):1057–1068. https://doi.org/10.1038/nbt.1685
Poston GJ, Figueras J, Giuliante F et al (2008) Urgent need for a new staging system in advanced colorectal cancer. J Clin Oncol. 26(29):4828–4833. https://doi.org/10.1200/JCO.2008.17.6453
Pritchard CC, Grady WM (2011) Colorectal cancer molecular biology moves into clinical practice. Gut. 60(1):116–129. https://doi.org/10.1136/gut.2009.206250
Qi J, Zhu YQ, Luo J, Tao WH (2006) Hypermethylation and expression regulation of secreted frizzled-related protein genes in colorectal tumor. World J Gastroenterol. 12(44):7113–7117. https://doi.org/10.3748/wjg.v12.i44.7113
Qian X, Yu J, Yin Y et al (2013) MicroRNA-143 inhibits tumor growth and angiogenesis and sensitizes chemosensitivity to oxaliplatin in colorectal cancers. Cell Cycle. 12(9):1385–1394. https://doi.org/10.4161/cc.24477
Reinert T, Henriksen TV, Christensen E et al (2019) Analysis of plasma cell-free DNA by ultradeep sequencing in patients with stages I to III colorectal cancer. JAMA Oncol. 5(8):1124–1131. https://doi.org/10.1001/jamaoncol.2019.0528
Reinert T, Schøler LV, Thomsen R et al (2016) Analysis of circulating tumour DNA to monitor disease burden following colorectal cancer surgery. Gut. 65(4):625–634. https://doi.org/10.1136/gutjnl-2014-308859
Rex DK, Ahnen DJ, Baron JA et al (2012) Serrated lesions of the colorectum: review and recommendations from an expert panel. Off J Am Coll Gastroenterol ACG. 107(9):1315. https://doi.org/10.1038/ajg.2012.161
Rhee YY, Kim MJ, Bae JM et al (2012) Clinical outcomes of patients with microsatellite-unstable colorectal carcinomas depend on L1 methylation level. Ann Surg Oncol. 19(11):3441–3448. https://doi.org/10.1245/s10434-012-2410-7
van Rijnsoever M, Grieu F, Elsaleh H, Joseph D, Iacopetta B (2002) Characterisation of colorectal cancers showing hypermethylation at multiple CpG islands. Gut. 51(6):797–802. https://doi.org/10.1136/gut.51.6.797
Saltz LB, Meropol NJ, Loehrer PJ, Needle MN, Kopit J, Mayer RJ (2004) Phase II trial of cetuximab in patients with refractory colorectal cancer that expresses the epidermal growth factor receptor. J Clin Oncol. 22(7):1201–1208. https://doi.org/10.1200/JCO.2004.10.182
Samowitz WS, Albertsen H, Herrick J et al (2005) Evaluation of a large, population-based sample supports a CpG Island methylator phenotype in colon cancer. Gastroenterology. 129(3):837–845. https://doi.org/10.1053/j.gastro.2005.06.020
Schee K, Lorenz S, Worren MM et al (2013) Deep sequencing the MicroRNA transcriptome in colorectal cancer. PLOS ONE. 8(6):e66165. https://doi.org/10.1371/journal.pone.0066165
Schepeler T, Reinert JT, Ostenfeld MS et al (2008) Diagnostic and prognostic MicroRNAs in stage II colon cancer. Cancer Res. 68(15):6416–6424. https://doi.org/10.1158/0008-5472.CAN-07-6110
Schetter AJ, Leung SY, Sohn JJ et al (2008) MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA. 299(4):425–436. https://doi.org/10.1001/jama.299.4.425
Schmitz KJ, Hey S, Schinwald A et al (2009) Differential expression of microRNA 181b and microRNA 21 in hyperplastic polyps and sessile serrated adenomas of the colon. Virchows Arch. 455(1):49–54. https://doi.org/10.1007/s00428-009-0804-0
Shang J, Yang F, Wang Y et al (2014) MicroRNA-23a antisense enhances 5-fluorouracil chemosensitivity through APAF-1/Caspase-9 apoptotic pathway in colorectal cancer cells. J Cell Biochem. 115(4):772–784. https://doi.org/10.1002/jcb.24721
Sheffield PJ, Oliver CJ, Kremer BE, Sheng S, Shao Z, Macara IG (2003) Borg/septin interactions and the assembly of mammalian septin heterodimers, trimers, and filaments*. J Biol Chem. 278(5):3483–3488. https://doi.org/10.1074/jbc.M209701200
Shen L, Catalano PJ, Benson AB III, O’Dwyer P, Hamilton SR, Issa JPJ (2007) Association between DNA methylation and shortened survival in patients with advanced colorectal cancer treated with 5-fluorouracil–based chemotherapy. Clin Cancer Res. 13(20):6093–6098. https://doi.org/10.1158/1078-0432.CCR-07-1011
Shen L, Kondo Y, Rosner GL et al (2005) MGMT promoter methylation and field defect in sporadic colorectal cancer. JNCI J Natl Cancer Inst. 97(18):1330–1338. https://doi.org/10.1093/jnci/dji275
Shibuya H, Iinuma H, Shimada R, Horiuchi A, Watanabe T (2010) Clinicopathological and prognostic value of MicroRNA-21 and MicroRNA-155 in colorectal cancer. Oncology. 79(3-4):313–320. https://doi.org/10.1159/000323283
Shiovitz S, Bertagnolli MM, Renfro LA et al (2014) CpG Island methylator phenotype is associated with response to adjuvant irinotecan-based therapy for stage III colon cancer. Gastroenterology. 147(3):637–645. https://doi.org/10.1053/j.gastro.2014.05.009
Sidransky D, Tokino T, Hamilton SR et al (1992) Identification of ras oncogene mutations in the stool of patients with curable colorectal tumors. Science. 256(5053):102–105. https://doi.org/10.1126/science.1566048
Siemens H, Jackstadt R, Kaller M, Hermeking H (2013) Repression of c-Kit by p53 is mediated by miR-34 and is associated with reduced chemoresistance, migration and stemness. Oncotarget. 4(9):1399–1415. https://doi.org/10.18632/oncotarget.1202
Siravegna G, Mussolin B, Buscarino M et al (2015) Erratum: clonal evolution and resistance to EGFR blockade in the blood of colorectal cancer patients. Nat Med. 21(7):827–827. https://doi.org/10.1038/nm0715-827b
Slaby O, Svoboda M, Michalek J, Vyzula R (2009) MicroRNAs in colorectal cancer: translation of molecular biology into clinical application. Mol Cancer. 8(1):102. https://doi.org/10.1186/1476-4598-8-102
Song B, Wang Y, Xi Y et al (2009) Mechanism of chemoresistance mediated by miR-140 in human osteosarcoma and colon cancer cells. Oncogene. 28(46):4065–4074. https://doi.org/10.1038/onc.2009.274
Stachler MD, Rinehart E, Lindeman N, Odze R, Srivastava A (2015) Novel molecular insights from routine genotyping of colorectal carcinomas. Hum Pathol. 46(4):507–513. https://doi.org/10.1016/j.humpath.2015.01.005
Sun D, Yu F, Ma Y et al (2013) MicroRNA-31 Activates the RAS Pathway and Functions as an Oncogenic MicroRNA in Human Colorectal Cancer by Repressing RAS p21 GTPase Activating Protein 1 (RASA1) *. J Biol Chem. 288(13):9508–9518. https://doi.org/10.1074/jbc.M112.367763
Sung H, Ferlay J, Siegel RL et al (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 71(3):209–249. https://doi.org/10.3322/caac.21660
Suzuki H, Igarashi S, Nojima M et al (2010) IGFBP7 is a p53-responsive gene specifically silenced in colorectal cancer with CpG island methylator phenotype. Carcinogenesis. 31(3):342–349. https://doi.org/10.1093/carcin/bgp179
Suzuki H, Watkins DN, Jair KW et al (2004) Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet. 36(4):417–422. https://doi.org/10.1038/ng1330
Suzuki K, Suzuki I, Leodolter A et al (2006) Global DNA demethylation in gastrointestinal cancer is age dependent and precedes genomic damage. Cancer Cell. 9(3):199–207. https://doi.org/10.1016/j.ccr.2006.02.016
Tahiliani M, Koh KP, Shen Y et al (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 324(5929):930–935. https://doi.org/10.1126/science.1170116
Takahashi M, Cuatrecasas M, Balaguer F et al (2012) The clinical significance of MiR-148a as a predictive biomarker in patients with advanced colorectal cancer. PLOS ONE. 7(10):e46684. https://doi.org/10.1371/journal.pone.0046684
Tamagawa H, Oshima T, Numata M et al (2013) Global histone modification of H3K27 correlates with the outcomes in patients with metachronous liver metastasis of colorectal cancer. Eur J Surg Oncol. 39(6):655–661. https://doi.org/10.1016/j.ejso.2013.02.023
Tamagawa H, Oshima T, Shiozawa M et al (2012) The global histone modification pattern correlates with overall survival in metachronous liver metastasis of colorectal cancer. Oncol Rep. 27(3):637–642. https://doi.org/10.3892/or.2011.1547
Tan S, Davey CA (2011) Nucleosome structural studies. Curr Opin Struct Biol. 21(1):128–136. https://doi.org/10.1016/j.sbi.2010.11.006
Tang W, Zhu Y, Gao J et al (2014) MicroRNA-29a promotes colorectal cancer metastasis by regulating matrix metalloproteinase 2 and E-cadherin via KLF4. Br J Cancer. 110(2):450–458. https://doi.org/10.1038/bjc.2013.724
Tazawa H, Tsuchiya N, Izumiya M, Nakagama H (2007) Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci. 104(39):15472–15477. https://doi.org/10.1073/pnas.0707351104
Tessarz P, Kouzarides T (2014) Histone core modifications regulating nucleosome structure and dynamics. Nat Rev Mol Cell Biol. 15(11):703–708. https://doi.org/10.1038/nrm3890
Tie J, Cohen JD, Wang Y et al (2019) Circulating tumor DNA analyses as markers of recurrence risk and benefit of adjuvant therapy for stage III colon cancer. JAMA Oncol. 5(12):1710–1717. https://doi.org/10.1001/jamaoncol.2019.3616
Toden S, Okugawa Y, Jascur T et al (2015) Curcumin mediates chemosensitization to 5-fluorouracil through miRNA-induced suppression of epithelial-to-mesenchymal transition in chemoresistant colorectal cancer. Carcinogenesis. 36(3):355–367. https://doi.org/10.1093/carcin/bgv006
Toiyama Y, Takahashi M, Hur K et al (2013) Serum miR-21 as a diagnostic and prognostic biomarker in colorectal cancer. JNCI J Natl Cancer Inst. 105(12):849–859. https://doi.org/10.1093/jnci/djt101
Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JPJ (1999) CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci. 96(15):8681–8686. https://doi.org/10.1073/pnas.96.15.8681
Toyota M, Ohe-Toyota M, Ahuja N, Issa JPJ (2000) Distinct genetic profiles in colorectal tumors with or without the CpG island methylator phenotype. Proc Natl Acad Sci. 97(2):710–715. https://doi.org/10.1073/pnas.97.2.710
Tu HC, Schwitalla S, Qian Z et al (2015) LIN28 cooperates with WNT signaling to drive invasive intestinal and colorectal adenocarcinoma in mice and humans. Genes Dev. 29(10):1074–1086. https://doi.org/10.1101/gad.256693.114
Turchinovich A, Weiz L, Langheinz A, Burwinkel B (2011) Characterization of extracellular circulating microRNA. Nucleic Acids Res. 39(16):7223–7233. https://doi.org/10.1093/nar/gkr254
Valeri N, Gasparini P, Braconi C et al (2010) MicroRNA-21 induces resistance to 5-fluorouracil by down-regulating human DNA MutS homolog 2 (hMSH2). Proc Natl Acad Sci. 107(49):21098–21103. https://doi.org/10.1073/pnas.1015541107
Valladares-Ayerbes M, Blanco M, Haz M et al (2011) Prognostic impact of disseminated tumor cells and microRNA-17-92 cluster deregulation in gastrointestinal cancer. Int J Oncol. 39(5):1253–1264. https://doi.org/10.3892/ijo.2011.1112
Van Rijnsoever M, Elsaleh H, Joseph D, McCaul K, Iacopetta B (2003) CpG island methylator phenotype is an independent predictor of survival benefit from 5-fluorouracil in stage III colorectal cancer. Clin Cancer Res Off J Am Assoc Cancer Res. 9(8):2898–2903
Vasudevan S, Tong Y, Steitz JA (2007) Switching from repression to activation: micrornas can up-regulate translation. Science. 318(5858):1931–1934. https://doi.org/10.1126/science.1149460
Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT (2011) MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 13(4):423–433. https://doi.org/10.1038/ncb2210
Vogelstein B, Fearon ER, Hamilton SR et al (1988) Genetic alterations during colorectal-tumor development. N Engl J Med. 319(9):525–532. https://doi.org/10.1056/NEJM198809013190901
Vogt M, Munding J, Grüner M et al (2011) Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch. 458(3):313–322. https://doi.org/10.1007/s00428-010-1030-5
Wallner M, Herbst A, Behrens A et al (2006) Methylation of serum DNA is an independent prognostic marker in colorectal cancer. Clin Cancer Res. 12(24):7347–7352. https://doi.org/10.1158/1078-0432.CCR-06-1264
Wang CJ, Stratmann J, Zhou ZG, Sun XF (2010) Suppression of microRNA-31 increases sensitivity to 5-FU at an early stage, and affects cell migration and invasion in HCT-116 colon cancer cells. BMC Cancer. 10(1):616. https://doi.org/10.1186/1471-2407-10-616
Wang DR, Tang D (2008) Hypermethylated SFRP2 gene in fecal DNA is a high potential biomarker for colorectal cancer noninvasive screening. World J Gastroenterol. 14(4):524–531. https://doi.org/10.3748/wjg.14.524
Wang J, Huang SK, Zhao M et al (2014a) Identification of a circulating microRNA signature for colorectal cancer detection. PLOS ONE. 9(4):e87451. https://doi.org/10.1371/journal.pone.0087451
Wang S, Xiang J, Li Z et al (2015) A plasma microRNA panel for early detection of colorectal cancer. Int J Cancer. 136(1):152–161. https://doi.org/10.1002/ijc.28136
Wang S, Yang MH, Wang XY, Lin J, Ding YQ (2014b) Increased expression of miRNA-182 in colorectal carcinoma: an independent and tissue-specific prognostic factor. Int J Clin Exp Pathol. 7(6):3498–3503
Wang Y, Li L, Cohen JD et al (2019) Prognostic potential of circulating tumor DNA measurement in postoperative surveillance of nonmetastatic colorectal cancer. JAMA Oncol. 5(8):1118–1123. https://doi.org/10.1001/jamaoncol.2019.0512
Ward R, Meagher A, Tomlinson I et al (2001) Microsatellite instability and the clinicopathological features of sporadic colorectal cancer. Gut. 48(6):821–829. https://doi.org/10.1136/gut.48.6.821
Weisenberger DJ, Siegmund KD, Campan M et al (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. https://doi.org/10.1038/ng1834
Wightman B, Ha I, Ruvkun G (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell. 75(5):855–862. https://doi.org/10.1016/0092-8674(93)90530-4
Wolin SL, Maquat LE (2019) Cellular RNA surveillance in health and disease. Science. 366(6467):822–827. https://doi.org/10.1126/science.aax2957
Wu CW, Ng SSM, Dong YJ et al (2012) Detection of miR-92a and miR-21 in stool samples as potential screening biomarkers for colorectal cancer and polyps. Gut. 61(5):739–745. https://doi.org/10.1136/gut.2011.239236
Xiong B, Cheng Y, Ma L, Zhang C (2013) MiR-21 regulates biological behavior through the PTEN/PI-3 K/Akt signaling pathway in human colorectal cancer cells. Int J Oncol. 42(1):219–228. https://doi.org/10.3892/ijo.2012.1707
Xu K, Liang X, Cui D, Wu Y, Shi W, Liu J (2013) miR-1915 inhibits Bcl-2 to modulate multidrug resistance by increasing drug-sensitivity in human colorectal carcinoma cells. Mol Carcinog. 52(1):70–78. https://doi.org/10.1002/mc.21832
Xu L, Zhang Y, Wang H, Zhang G, Ding Y, Zhao L (2014) Tumor suppressor miR-1 restrains epithelial-mesenchymal transition and metastasis of colorectal carcinoma via the MAPK and PI3K/AKT pathway. J Transl Med. 12(1):244. https://doi.org/10.1186/s12967-014-0244-8
Yamamoto E, Toyota M, Suzuki H et al (2008) LINE-1 hypomethylation is associated with increased CpG Island methylation in helicobacter pylori–related enlarged-fold gastritis. Cancer Epidemiol Biomarkers Prev. 17(10):2555–2564. https://doi.org/10.1158/1055-9965.EPI-08-0112
Yamauchi M, Lochhead P, Morikawa T et al (2012a) Colorectal cancer: a tale of two sides or a continuum? Gut. 61(6):794–797. https://doi.org/10.1136/gutjnl-2012-302014
Yamauchi M, Morikawa T, Kuchiba A et al (2012b) Assessment of colorectal cancer molecular features along bowel subsites challenges the conception of distinct dichotomy of proximal versus distal colorectum. Gut. 61(6):847–854. https://doi.org/10.1136/gutjnl-2011-300865
Yang MH, Yu J, Chen N et al (2013) Elevated MicroRNA-31 expression regulates colorectal cancer progression by repressing its target gene SATB2. PLOS ONE. 8(12):e85353. https://doi.org/10.1371/journal.pone.0085353
You JS, Jones PA (2012) Cancer genetics and epigenetics: two sides of the same coin? Cancer Cell. 22(1):9–20. https://doi.org/10.1016/j.ccr.2012.06.008
Yu G, Tang JQ, Tian ML et al (2012) Prognostic values of the miR-17-92 cluster and its paralogs in colon cancer. J Surg Oncol. 106(3):232–237. https://doi.org/10.1002/jso.22138
Zhang J, Guo H, Zhang H et al (2011) Putative tumor suppressor miR-145 inhibits colon cancer cell growth by targeting oncogene friend leukemia virus integration 1 gene. Cancer. 117(1):86–95. https://doi.org/10.1002/cncr.25522
Zhang JX, Song W, Chen ZH et al (2013a) Prognostic and predictive value of a microRNA signature in stage II colon cancer: a microRNA expression analysis. Lancet Oncol. 14(13):1295–1306. https://doi.org/10.1016/S1470-2045(13)70491-1
Zhang L, Pickard K, Jenei V et al (2013b) miR-153 Supports Colorectal Cancer Progression via Pleiotropic Effects That Enhance Invasion and Chemotherapeutic Resistance. Cancer Res. 73(21):6435–6447. https://doi.org/10.1158/0008-5472.CAN-12-3308
Zhang R, Kang KA, Piao MJ et al (2014) Epigenetic alterations are involved in the overexpression of glutathione S-transferase π-1 in human colorectal cancers. Int J Oncol. 45(3):1275–1283. https://doi.org/10.3892/ijo.2014.2522
Zhao L, Li Y, Xu T et al (2022) Dendritic cell-mediated chronic low-grade inflammation is regulated by the RAGE-TLR4-PKCβ1 signaling pathway in diabetic atherosclerosis. Mol Med. 28(1):4. https://doi.org/10.1186/s10020-022-00431-6
Zhou Y, Wan G, Spizzo R et al (2014) miR-203 induces oxaliplatin resistance in colorectal cancer cells by negatively regulating ATM kinase. Mol Oncol. 8(1):83–92. https://doi.org/10.1016/j.molonc.2013.09.004
Zlobec I, Kovac M, Erzberger P et al (2010) Combined analysis of specific KRAS mutation, BRAF and microsatellite instability identifies prognostic subgroups of sporadic and hereditary colorectal cancer. Int J Cancer. 127(11):2569–2575. https://doi.org/10.1002/ijc.25265
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Ko, B., Hanna, M., Yu, M., Grady, W.M. (2023). Epigenetic Alterations in Colorectal Cancer. In: Kalkan, R. (eds) Cancer Epigenetics. Epigenetics and Human Health, vol 11. Springer, Cham. https://doi.org/10.1007/978-3-031-42365-9_10
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