DNA Methylation Detection Technology and Plasma-Based Methylation Biomarkers in Screening of Gastrointestinal Carcinoma

References

• Raiber E-A , HardistyR , van DelftP , BalasubramanianS. Mapping and elucidating the function of modified bases in DNA. Nat. Rev. Chem.1(9), 1–13 (2017).
   Web of Science ®Google Scholar
• Ruppel WG . Zur Chemie der Tuberkelbacillen. Hoppe-Seyler´s Zeitschrift für Physiol. Chemie.26(3–4), 218–232 (1898).
   Google Scholar
• Greenberg MVC , Bourc’hisD. The diverse roles of DNA methylation in mammalian development and disease. Nat. Rev. Mol. Cell Biol.20(10), 590–607 (2019).
   PubMed Web of Science ®Google Scholar
• Deaton AM , BirdA. CpG islands and the regulation of transcription. Genes Dev.25(10), 1010–1022 (2011).
   PubMed Web of Science ®Google Scholar
• Tahiliani M , KohKP , ShenYet al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science324(5929), 930–935 (2009).
   PubMed Web of Science ®Google Scholar
• Ito S , ShenL , DaiQet al. TET proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science333(6047), 1300–1303 (2011).
   PubMed Web of Science ®Google Scholar
• Li E , ZhangY. DNA methylation in mammals. Cold Spring Harb. Perspect. Biol.6(5), a019133 (2014).
   PubMed Web of Science ®Google Scholar
• You JS , JonesPA. Cancer genetics and epigenetics: two sides of the same coin?Cancer Cell22(1), 9–20 (2012).
   PubMed Web of Science ®Google Scholar
• Baylin SB , JonesPA. A decade of exploring the cancer epigenome-biological and translational implications. Nat. Rev. Cancer.11(10), 726–734 (2011).
   PubMed Web of Science ®Google Scholar
• Hansen KD , TimpW , BravoHCet al. Increased methylation variation in epigenetic domains across cancer types. Nat. Genet.43(8), 768–775 (2011).
   PubMed Web of Science ®Google Scholar
• Bert SA , RobinsonMD , StrbenacDet al. Regional activation of the cancer genome by long-range epigenetic remodeling. Cancer Cell23(1), 9–22 (2013).
   PubMed Web of Science ®Google Scholar
• Jones PA , BaylinSB. The epigenomics of cancer. Cell128(4), 683–692 (2007).
   PubMed Web of Science ®Google Scholar
• Hur K , CejasP , FeliuJet al. Hypomethylation of long interspersed nuclear element-1 (LINE-1) leads to activation of protooncogenes in human colorectal cancer metastasis. Gut63(4), 635–646 (2014).
   PubMed Web of Science ®Google Scholar
• Heitzer E , HaqueIS , RobertsCES , SpeicherMR. Current and future perspectives of liquid biopsies in genomics-driven oncology. Nat. Rev. Genet.20(2), 71–88 (2019).
   PubMed Web of Science ®Google Scholar
• Wong IHN , LoYMD , ZhangJet al. Detection of aberrant p16 methylation in the plasma and serum of liver cancer patients. Cancer Res.59(1), 71–73 (1999).
   PubMed Web of Science ®Google Scholar
• Sung H , FerlayJ , SiegelRLet al. 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 (2021).
   PubMed Web of Science ®Google Scholar
• Frommer M , McDonaldLE , MillarDSet al. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc. Natl Acad. Sci. USA89(5), 1827–1831 (1992).
   PubMed Web of Science ®Google Scholar
• Lister R , PelizzolaM , DowenRHet al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature462(7271), 315–322 (2009).
   PubMed Web of Science ®Google Scholar
• Andrew Adey JS . Ultra-low-input, tagmentation-based whole-genome bisulfite sequencing. Genome Res.22(6), 1139–1143 (2012).
   PubMed Web of Science ®Google Scholar
• Kang S , LiQ , ChenQet al. CancerLocator: non-invasive cancer diagnosis and tissue-of-origin prediction using methylation profiles of cell-free DNA. Genome Biol.18(1), 53 (2017).
   PubMedGoogle Scholar
• Liu MC , OxnardGR , KleinEAet al. Sensitive and specific multi-cancer detection and localization using methylation signatures in cell-free DNA. Ann. Oncol.31(6), 745–759 (2020).
   PubMed Web of Science ®Google Scholar
• Tanaka K , OkamotoA. Degradation of DNA by bisulfite treatment. Bioorganic Med. Chem. Lett.17(7), 1912–1915 (2007).
   PubMed Web of Science ®Google Scholar
• Olova N , KruegerF , AndrewsSet al. Comparison of whole-genome bisulfite sequencing library preparation strategies identifies sources of biases affecting DNA methylation data. Genome Biol.19(1), 1–19 (2018).
   PubMedGoogle Scholar
• Jin SG , KadamS , PfeiferGP. Examination of the specificity of DNA methylation profiling techniques towards 5-methylcytosine and 5-hydroxymethylcytosine. Nucleic Acids Res.38(11), 1–7 (2010).
   PubMed Web of Science ®Google Scholar
• Zhao LY , SongJ , LiuY , SongCX , YiC. Mapping the epigenetic modifications of DNA and RNA. Protein Cell11(11), 792–808 (2020).
   PubMed Web of Science ®Google Scholar
• Peng X , WuJ , BrunmeirRet al. TELP, a sensitive and versatile library construction method for next-generation sequencing. Nucleic Acids Res.43(6), e35 (2015).
   PubMed Web of Science ®Google Scholar
• Gansauge MT , GerberT , GlockeIet al. Single-stranded DNA library preparation from highly degraded DNA using T4 DNA ligase. Nucleic Acids Res.45(10), e79 (2017).
   PubMed Web of Science ®Google Scholar
• Herman JG , GraffJR , MyöhänenS , NelkinBD , BaylinSB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc. Natl Acad. Sci. USA93(18), 9821–9826 (1996).
   PubMed Web of Science ®Google Scholar
• Meissner A , GnirkeA , BellGW , RamsahoyeB , LanderES , JaenischR. Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res.33(18), 5868–5877 (2005).
   PubMed Web of Science ®Google Scholar
• Gu H , SmithZD , BockC , BoyleP , GnirkeA , MeissnerA. Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. Nat. Protoc.6(4), 468–481 (2011).
   PubMed Web of Science ®Google Scholar
• Wang L , SunJ , WuHet al. Systematic assessment of reduced representation bisulfite sequencing to human blood samples: a promising method for large-sample-scale epigenomic studies. J. Biotechnol.157(1), 1–6 (2012).
   PubMed Web of Science ®Google Scholar
• Yim JH , ChoiAH , LiAXet al. Identification of tissue-specific DNA methylation signatures for thyroid nodule diagnostics. Clin. Cancer Res.25(2), 544–551 (2019).
   PubMed Web of Science ®Google Scholar
• Guo S , DiepD , PlongthongkumNet al. Identification of methylation haplotype blocks aids in deconvolution of heterogeneous tissue samples and tumor tissue-of-origin mapping from plasma DNA. Nat. Genet.49(4), 635–642 (2017).
   PubMed Web of Science ®Google Scholar
• Sun Z , CunninghamJ , SlagerS , KocherJP. Base resolution methylome profiling: considerations in platform selection, data preprocessing and analysis. Epigenomics.7(5), 813–828 (2015).
   PubMed Web of Science ®Google Scholar
• Ball MP , LiJB , GaoYet al. Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat. Biotechnol.27(4), 361–368 (2009).
   PubMed Web of Science ®Google Scholar
• Luo H , ZhaoQ , WeiWet al. Circulating tumor DNA methylation profiles enable early diagnosis, prognosis prediction, and screening for colorectal cancer. Sci. Transl. Med.12(540), 1–12 (2020).
   Web of Science ®Google Scholar
• Booth MJ , BrancoMR , FiczG , OxleyD , KruegerF. Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science336(6083), 934–937 (2012).
   PubMed Web of Science ®Google Scholar
• Yu M , HonGC , SzulwachKEet al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell149(6), 1368–1380 (2012).
   PubMed Web of Science ®Google Scholar
• Wen L , LiJ , GuoHet al. Genome-scale detection of hypermethylated CpG islands in circulating cell-free DNA of hepatocellular carcinoma patients. Cell Res.25(11), 1250–1264 (2015).
   PubMed Web of Science ®Google Scholar
• Liu X , RenJ , LuoNet al. Comprehensive DNA methylation analysis of tissue of origin of plasma cell-free DNA by methylated CpG tandem amplification and sequencing (MCTA-Seq). Clin. Epigenetics.11(1), 1–13 (2019).
   PubMedGoogle Scholar
• Li J , LiY , LiWet al. Guide positioning sequencing identifies aberrant DNA methylation patterns that alter cell identity and tumor-immune surveillance networks. Genome Res.29(2), 270–280 (2019).
   PubMed Web of Science ®Google Scholar
• Weber M , DaviesJJ , WittigDet al. Chromosome-wide and promoter-specific analysis identify sites of differential DNA methylation in normal and transformed human cells. Nat. Genet.37(8), 853–862 (2005).
   PubMed Web of Science ®Google Scholar
• Shen SY , SinghaniaR , FehringerGet al. Sensitive tumor detection and classification using plasma cell-free DNA methylomes. Nature563(7732), 579–583 (2018).
   PubMed Web of Science ®Google Scholar
• Shen SY , BurgenerJM , BratmanSV , DeCarvalho DD. Preparation of cfMeDIP-seq libraries for methylome profiling of plasma cell-free DNA. Nat. Protoc.14(10), 2749–2780 (2019).
   PubMed Web of Science ®Google Scholar
• Flusberg BA , WebsterDR , LeeJHet al. Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat. Methods.7(6), 461–465 (2010).
   PubMed Web of Science ®Google Scholar
• Clark TA , MurrayIA , MorganRDet al. Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing. Nucleic Acids Res.40(4), e29 (2012).
   PubMed Web of Science ®Google Scholar
• Murray IA , ClarkTA , MorganRDet al. The methylomes of six bacteria. Nucleic Acids Res.40(22), 11450–11462 (2012).
   PubMed Web of Science ®Google Scholar
• Eid J , FehrA , GrayJet al. Real-time DNA sequencing from single polymerase molecules. Science323(5910), 133–138 (2009).
   PubMed Web of Science ®Google Scholar
• Jain M , OlsenHE , PatenB , AkesonM. The Oxford Nanopore MinION: delivery of nanopore sequencing to the genomics community. Genome Biol.17(1), 1–11 (2016).
   PubMedGoogle Scholar
• Michael E . An ace in the hole for DNA sequencing. Nature550(7675), 285–288 (2017).
   PubMed Web of Science ®Google Scholar
• Schreiber J , WescoeZL , Abu-ShumaysRet al. Error rates for nanopore discrimination among cytosine, methylcytosine, and hydroxymethylcytosine along individual DNA strands. Proc. Natl Acad. Sci. USA110(47), 18910–18915 (2013).
   PubMed Web of Science ®Google Scholar
• Wescoe ZL , SchreiberJ , AkesonM. Nanopores discriminate among five C5-cytosine variants in DNA. J. Am. Chem. Soc.136(47), 16582–16587 (2014).
   PubMed Web of Science ®Google Scholar
• Euskirchen P , BielleF , LabrecheKet al. Same-day genomic and epigenomic diagnosis of brain tumors using real-time nanopore sequencing. Acta Neuropathol.134(5), 691–703 (2017).
   PubMed Web of Science ®Google Scholar
• Ewing AD , SmitsN , Sanchez-LuqueFJet al. Nanopore sequencing enables comprehensive transposable element epigenomic profiling. Mol. Cell.80(5), 915–928.e5 (2020).
   PubMed Web of Science ®Google Scholar
• Giesselmann P , BrändlB , RaimondeauEet al. Analysis of short tandem repeat expansions and their methylation state with nanopore sequencing. Nat. Biotechnol.37(12), 1478–1481 (2019).
   PubMed Web of Science ®Google Scholar
• Rand AC , JainM , EizengaJMet al. Mapping DNA methylation with high-throughput nanopore sequencing. Nat. Methods14(4), 411–413 (2017).
   PubMed Web of Science ®Google Scholar
• Krishnakumar R , SinhaA , BirdSWet al. Systematic and stochastic influences on the performance of the MinION nanopore sequencer across a range of nucleotide bias. Sci. Rep.8(1), 1–13 (2018).
   PubMedGoogle Scholar
• van Dijk EL , JaszczyszynY , NaquinD , ThermesC. The third revolution in sequencing technology. Trends Genet.34(9), 666–681 (2018).
   PubMed Web of Science ®Google Scholar
• Noakes MT , BrinkerhoffH , LaszloAHet al. Increasing the accuracy of nanopore DNA sequencing using a time-varying cross membrane voltage. Nat. Biotechnol.37(6), 651–656 (2019).
   PubMed Web of Science ®Google Scholar
• Wilson BD , EisensteinM , SohHT. High-fidelity nanopore sequencing of ultra-short DNA targets. Anal. Chem.91(10), 6783–6789 (2019).
   PubMed Web of Science ®Google Scholar
• Liu Y , Siejka-ZielińskaP , VelikovaGet al. Bisulfite-free direct detection of 5-methylcytosine and 5-hydroxymethylcytosine at base resolution. Nat. Biotechnol.37(4), 424–429 (2019).
   PubMed Web of Science ®Google Scholar
• Xia B , HanD , LuXet al. Bisulfite-free, base-resolution analysis of 5-formylcytosine at the genome scale. Nat. Methods12(11), 1047–1050 (2015).
   PubMed Web of Science ®Google Scholar
• Zhu C , GaoY , GuoHet al. Single-cell 5-formylcytosine landscapes of mammalian early embryos and ESCs at single-base resolution. Cell Stem Cell.20(5), 720–731.e5 (2017).
   PubMed Web of Science ®Google Scholar
• Song CX , ClarkTA , LuXYet al. Sensitive and specific single-molecule sequencing of 5-hydroxymethylcytosine. Nat. Methods9(1), 75–77 (2012).
   Web of Science ®Google Scholar
• Zeng H , HeB , XiaBet al. Bisulfite-free, nanoscale analysis of 5-hydroxymethylcytosine at single base resolution. J. Am. Chem. Soc.140(41), 13190–13194 (2018).
   PubMed Web of Science ®Google Scholar
• Liu Y , ChengJ , Siejka-ZielińskaPet al. Accurate targeted long-read DNA methylation and hydroxymethylation sequencing with TAPS. Genome Biol.21(1), 1–9 (2020).
   Web of Science ®Google Scholar
• Beikircher G , PulvererW , HofnerM , NoehammerC , WeinhaeuselA. Multiplexed and sensitive DNA methylation testing using methylation-sensitive restriction enzymes “MSRE-qPCR”. In: DNA Methylation Protocols.Humana Press, NY, USA407–424 (2018).
   Google Scholar
• Nam SY . Gastric cancer screening. In: Helicobacter pylori.Springer, Singapore495–500 (2016).
   Google Scholar
• Bass AJ , ThorssonV , ShmulevichIet al. Comprehensive molecular characterization of gastric adenocarcinoma. Nature513(7517), 202–209 (2014).
   PubMed Web of Science ®Google Scholar
• Bijlsma MF , SadanandamA , TanP , VermeulenL. Molecular subtypes in cancers of the gastrointestinal tract. Nat. Rev. Gastroenterol. Hepatol.14(6), 333–342 (2017).
   PubMed Web of Science ®Google Scholar
• Liu Y , SethiNS , HinoueTet al. Comparative molecular analysis of gastrointestinal adenocarcinomas. Cancer Cell33(4), 721–735 (2018).
   PubMed Web of Science ®Google Scholar
• Liang Q , YaoX , TangSet al. Integrative identification of Epstein-Barr virus-associated mutations and epigenetic alterations in gastric cancer. Gastroenterology147(6), 1350–1362.e4 (2014).
   PubMed Web of Science ®Google Scholar
• Servetas SL , BridgeDR , ScottMerrell D. Molecular mechanisms of gastric cancer initiation and progression by Helicobacter pylori. Curr. Opin. Infect. Dis.29(3), 304–310 (2016).
   PubMed Web of Science ®Google Scholar
• Matsuoka T , YashiroM. Biomarkers of gastric cancer: current topics and future perspective. World J. Gastroenterol.24(26), 2818–2832 (2018).
   PubMed Web of Science ®Google Scholar
• Hideura E , SuehiroY , NishikawaJ , ShutoT. Blood free-circulating DNA testing of methylated RUNX3 is useful for diagnosing early gastric cancer. Cancers (Basel)12(4), 789 (2020).
   PubMed Web of Science ®Google Scholar
• Amini M , ForoughiK , TalebiFet al. GHSR DNA hypermethylation is a new epigenetic biomarker for gastric adenocarcinoma and beyond. J. Cell. Physiol.234(9), 15320–15329 (2019).
   PubMed Web of Science ®Google Scholar
• Huang KK , RamnarayananK , ZhuFet al. Genomic and epigenomic profiling of high-risk intestinal metaplasia reveals molecular determinants of progression to gastric cancer. Cancer Cell33(1), 137–150.e5 (2018).
   PubMed Web of Science ®Google Scholar
• Anderson BW , SuhYS , ChoiBet al. Detection of gastric cancer with novel methylated DNA markers: discovery, tissue validation, and pilot testing in plasma. Clin. Cancer Res.24(22), 5724–5734 (2018).
   PubMed Web of Science ®Google Scholar
• Chen X , GoleJ , GoreAet al. Non-invasive early detection of cancer four years before conventional diagnosis using a blood test. Nat. Commun.11(1), 3475 (2020).
   PubMed Web of Science ®Google Scholar
• Toyota M , AhujaN , Ohe-ToyotaM , HermanJG , BaylinSB , IssaJP. CpG island methylator phenotype in colorectal cancer. Proc. Natl Acad. Sci. USA96(15), 8681–8686 (1999).
   PubMed Web of Science ®Google Scholar
• Jung G , Hernández-IllánE , MoreiraL , BalaguerF , GoelA. Epigenetics of colorectal cancer: biomarker and therapeutic potential. Nat. Rev. Gastroenterol. Hepatol.17(2), 111–130 (2020).
   PubMed Web of Science ®Google Scholar
• Li M , ChenWD , PapadopoulosNet al. Sensitive digital quantification of DNA methylation in clinical samples. Nat. Biotechnol.27(9), 858–863 (2009).
   PubMed Web of Science ®Google Scholar
• Locke WJ , GuanzonD , MaCet al. DNA methylation cancer biomarkers: translation to the clinic. Front. Genet.10, 1150 (2019).
   PubMed Web of Science ®Google Scholar
• Barták BK , KalmárA , PéterfiaBet al. Colorectal adenoma and cancer detection based on altered methylation pattern of SFRP1, SFRP2, SDC2, and PRIMA1 in plasma samples. Epigenetics12(9), 751–763 (2017).
   PubMed Web of Science ®Google Scholar
• Pedersen SK , SymondsEL , BakerRTet al. Evaluation of an assay for methylated BCAT1 and IKZF1 in plasma for detection of colorectal neoplasia. BMC Cancer15(1), 1 (2015).
   PubMedGoogle Scholar
• Symonds EL , PedersenSK , BakerRTet al. A blood test for methylated BCAT1 and IKZF1 vs. a fecal immunochemical test for detection of colorectal neoplasia. Clin. Transl. Gastroenterol.7(1), e137 (2016).
   PubMed Web of Science ®Google Scholar
• Musher BL , MelsonJE , AmatoGet al. Evaluation of circulating tumor DNA for methylated BCAT1 and IKZF1 to detect recurrence of stage II/stage III colorectal cancer (CRC). Cancer Epidemiol. Biomarkers Prev.29(12), 2702–2709 (2020).
   PubMed Web of Science ®Google Scholar
• Jensen SØ , ØrntoftM-BW , ØgaardNet al. Novel DNA methylation biomarkers show high sensitivity and specificity for blood-based detection of colorectal cancer – a clinical biomarker discovery and validation study. Clin. Epigenetics11(1), 158 (2019).
   PubMed Web of Science ®Google Scholar
• Sui J , WuX , WangCet al. Discovery and validation of methylation signatures in blood-based circulating tumor cell-free DNA in early detection of colorectal carcinoma: a case–control study. Clin. Epigenetics13(1), 1–10 (2021).
   PubMed Web of Science ®Google Scholar
• Heimbach JK , KulikLM , FinnRSet al. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology67(1), 358–380 (2018).
   PubMed Web of Science ®Google Scholar
• Tzartzeva K , ObiJ , RichNEet al. Surveillance imaging and alpha fetoprotein for early detection of hepatocellular carcinoma in patients with cirrhosis: a meta-analysis. Gastroenterology154(6), 1706–1718.e1 (2018).
   PubMed Web of Science ®Google Scholar
• Wu X , LiJ , GassaAet al. Circulating tumor DNA as an emerging liquid biopsy biomarker for early diagnosis and therapeutic monitoring in hepatocellular carcinoma. Int. J. Biol. Sci.16(9), 1551–1562 (2020).
   PubMed Web of Science ®Google Scholar
• Li W , LiQ , KangSet al. CancerDetector: ultrasensitive and non-invasive cancer detection at the resolution of individual reads using cell-free DNA methylation sequencing data. Nucleic Acids Res.46(15), e89 (2018).
   PubMed Web of Science ®Google Scholar
• Xu RH , WeiW , KrawczykMet al. Circulating tumor DNA methylation markers for diagnosis and prognosis of hepatocellular carcinoma. Nat. Mater.16(11), 1155–1162 (2017).
   PubMed Web of Science ®Google Scholar
• Kisiel JB , DukekBA , KanipakamVSR Ret al. Hepatocellular carcinoma detection by plasma methylated DNA: discovery, phase I pilot, and phase II clinical validation. Hepatology69(3), 1180–1192 (2019).
   PubMed Web of Science ®Google Scholar
• Chalasani NP , RamasubramanianTS , BhattacharyaAet al. A novel blood-based panel of methylated DNA and protein markers for detection of early-stage hepatocellular carcinoma. Clin. Gastroenterol. Hepatol.S1542–3565(20), 31224–631226 (2020).
   Google Scholar