Advanced search
Publication Cover
Expert Review of Molecular Diagnostics Volume 12, 2012 - Issue 1
Submit an article Journal homepage
343
Views
20
CrossRef citations to date
0
Altmetric
Review

DNA methylation testing and marker validation using PCR: diagnostic applications

Gerda Egger Clinical Institute of Pathology, Medical University of Vienna, Waehringer Guertel 18–20, 1090 Vienna, Austria
,
Matthias Wielscher Molecular Medicine, Austrian Institute of Technology, Muthgasse 11, 1190 Vienna, Austria
,
Walter Pulverer Molecular Medicine, Austrian Institute of Technology, Muthgasse 11, 1190 Vienna, Austria
,
Albert Kriegner Molecular Medicine, Austrian Institute of Technology, Muthgasse 11, 1190 Vienna, Austria
&
Andreas Weinhäusel Molecular Medicine, Austrian Institute of Technology, Muthgasse 11, 1190 Vienna, Austria;[email protected]
Pages 75-92 | Published online: 09 Jan 2014

References

  • Lister R, Pelizzola M, Dowen RH et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature462(7271), 315–322 (2009).
  • DNA Methylation: Methods and Protocols Second Edition. Tost J (Ed.). Humana Press, NY, USA (2009).
  • Jacinto FV, Ballestar E, Esteller, M. Methyl-DNA immunoprecipitation (MeDIP): hunting down the DNA methylome. Biotechniques44(1), 35, 37, 39 (2008).
  • Hashimoto K, Kokubun S, Itoi E, Roach HI. Improved quantification of DNA methylation using methylation-sensitive restriction enzymes and real-time PCR. Epigenetics2(2), 86–91 (2007).
  • Lopez CA, Nakamori M, Thornton CA, Pearson CE. Identification of restriction endonucleases sensitive to 5-cytosine methylation at non-CpG sites, including expanded (CAG)n/(CTG)n repeats. Epigenetics6(4), 416–420 (2011).
  • Tarasova GV, Nayakshina TN, Degtyarev SK. Substrate specificity of new methyl-directed DNA endonuclease GlaI. BMC Mol. Biol.9, 7 (2008).
  • Weinhaeusel A, Thiele S, Hofner M, Hiort O, Noehammer C. PCR-based analysis of differentially methylated regions of GNAS enables convenient diagnostic testing of pseudohypoparathyroidism type Ib. Clin. Chem.54(9), 1537–1545 (2008).
  • Preusser M, Plumer S Dirnberger E, Hainfellner JA, Mannhalter C. Fixation of brain tumor biopsy specimens with RCL2 results in well-preserved histomorphology, immunohistochemistry and nucleic acids. Brain Pathol.20(6), 1010–1020 (2010).
  • Schumacher A, Weinhausl A, Petronis A. Application of microarrays for DNA methylation profiling. Methods Mol. Biol.439, 109–129 (2008).
  • Nygren AO, Ameziane N, Duarte HM et al. Methylation-specific MLPA (MS-MLPA): simultaneous detection of CpG methylation and copy number changes of up to 40 sequences. Nucleic Acids Res.33(14), e128 (2005).
  • Procter M, Chou LS, Tang W, Jama M, Mao R. Molecular diagnosis of Prader–Willi and Angelman syndromes by methylation-specific melting analysis and methylation-specific multiplex ligation-dependent probe amplification. Clin. Chem.52(7), 1276–1283 (2006).
  • Jeuken JW, Cornelissen SJ, Vriezen M et al. MS-MLPA: an attractive alternative laboratory assay for robust, reliable, and semiquantitative detection of MGMT promoter hypermethylation in gliomas. Lab. Invest.87(10), 1055–1065 (2007).
  • Weber M, Davies JJ, Wittig D et al. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat. Genet.37(8), 853–862 (2005).
  • Down TA, Rakyan VK, Turner DJ et al. A Bayesian deconvolution strategy for immunoprecipitation-based DNA methylome analysis. Nat. Biotechnol.26(7), 779–785 (2008).
  • Cross SH, Charlton JA, Nan X, Bird AP. Purification of CpG islands using a methylated DNA binding column. Nat. Genet.6(3), 236–244 (1994).
  • Rauch T, Li H, Wu X, Pfeifer GP. MIRA-assisted microarray analysis, a new technology for the determination of DNA methylation patterns, identifies frequent methylation of homeodomain-containing genes in lung cancer cells. Cancer Res.66(16), 7939–7947 (2006).
  • Weng YI, Huang TH, Yan PS. Methylated DNA immunoprecipitation and microarray-based analysis: detection of DNA methylation in breast cancer cell lines. Methods Mol. Biol.590, 165–176 (2009).
  • Serre D, Lee BH, Ting AH. MBD-isolated genome sequencing provides a high-throughput and comprehensive survey of DNA methylation in the human genome. Nucleic Acids Res.38(2), 391–399 (2010).
  • Bock C, Tomazou EM, Brinkman AB, et al. Quantitative comparison of genome-wide DNA methylation mapping technologies. Nat. Biotechnol.28(10), 1106–1114 (2010).
  • Harris RA, Wang T, Coarfa C et al. Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat. Biotechnol.28(10), 1097–1105 (2010).
  • Nestor C, Ruzov A, Meehan R, Dunican D. Enzymatic approaches and bisulfite sequencing cannot distinguish between 5-methylcytosine and 5-hydroxymethylcytosine in DNA. Biotechniques48(4), 317–319 (2010).
  • Frommer M, McDonald LE, Millar DS et 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).
  • Meissner A, Gnirke A, Bell GW, Ramsahoye B, Lander ES, Jaenisch R. Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res.33(18), 5868–5877 (2005).
  • Eads CA, Laird PW. Combined bisulfite restriction analysis (COBRA). Methods Mol. Biol.200, 71–85 (2002).
  • Wojdacz TK, Dobrovic A. Methylation-sensitive high resolution melting (MS-HRM): a new approach for sensitive and high-throughput assessment of methylation. Nucleic Acids Res.35(6), e41 (2007).
  • Gonzalgo ML, Jones PA. Quantitative methylation analysis using methylation-sensitive single-nucleotide primer extension (Ms-SNuPE). Methods27(2), 128–133 (2002).
  • Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc. Natl Acad. Sci. USA93(18), 9821–9826 (1996).
  • Shaw RJ, Akufo-Tetteh EK, Risk JM, Field JK, Liloglou T. Methylation enrichment pyrosequencing: combining the specificity of MSP with validation by pyrosequencing. Nucleic Acids Res.34(11), e78 (2006).
  • Campan M, Weisenberger DJ, Trinh B, Laird PW. MethyLight. Methods Mol. Biol.507, 325–337 (2009).
  • Cottrell SE, Distler J, Goodman NS et al. A real-time PCR assay for DNA-methylation using methylation-specific blockers. Nucleic Acids Res.32(1), e10 (2004).
  • Grutzmann R, Molnar B, Pilarsky C et al. Sensitive detection of colorectal cancer in peripheral blood by septin 9 DNA methylation assay. PLoS One3(11), e3759 (2008).
  • Grigg G, Clark, S. Sequencing 5-methylcytosine residues in genomic DNA. Bioessays16(6), 431–436 (1994).
  • Liloglou T, Field JK. Detection of DNA methylation changes in body fluids. Adv. Genet.71, 177–207 (2010).
  • White HE, Durston VJ, Harvey JF, Cross NC. Quantitative analysis of SNRPN(correction of SRNPN) gene methylation by pyrosequencing as a diagnostic test for Prader–Willi syndrome and Angelman syndrome. Clin. Chem.52(6), 1005–1013 (2006).
  • Ehrich M, Nelson MR, Stanssens P et al. Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc. Natl Acad. Sci. USA102(44), 15785–15790 (2005).
  • Martin-Subero JI, Esteller M. Profiling epigenetic alterations in disease. Adv. Exp. Med. Biol.711, 162–177 (2011).
  • Chan SW, Henderson IR, Jacobsen SE. Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat. Rev. Genet.6(5), 351–360 (2005).
  • Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science324(5929), 929–930 (2009).
  • Tahiliani M, Koh KP, Shen Y et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science324(5929), 930–935 (2009).
  • Veron N, Peters AH. Epigenetics: Tet proteins in the limelight. Nature473(7347), 293–294 (2011).
  • Munzel M, Globisch D, Carell T. 5-hydroxymethylcytosine, the sixth base of the genome. Angew. Chem. Int. Ed Engl.50(29), 6460–6468 (2011).
  • Krais AM, Park YJ, Plass C, Schmeiser HH. Determination of genomic 5-hydroxymethyl-2´-deoxycytidine in human DNA by capillary electrophoresis with laser induced fluorescence. Epigenetics6(5), 560–565 (2011).
  • Yuen RK, Jiang R, Penaherrera MS, McFadden DE, Robinson WP. Genome-wide mapping of imprinted differentially methylated regions by DNA methylation profiling of human placentas from triploidies. Epigenetics Chromatin4(1), 10 (2011).
  • Baysal BE. Genomic imprinting and environment in hereditary paraganglioma. Am. J. Med. Genet. C. Semin. Med. Genet.129C(1), 85–90 (2004).
  • Zeschnigk M, Lich C, Buiting K, Doerfler W, Horsthemke B. A single-tube PCR test for the diagnosis of Angelman and Prader–Willi syndrome based on allelic methylation differences at the SNRPN locus. Eur. J. Hum. Genet.5(2), 94–98 (1997).
  • Bliek J, Maas SM, Ruijter JM et al. Increased tumour risk for BWS patients correlates with aberrant H19 and not KCNQ1OT1 methylation: occurrence of KCNQ1OT1 hypomethylation in familial cases of BWS. Hum. Mol. Genet.10(5), 467–476 (2001).
  • Priolo M, Sparago A, Mammi C, Cerrato F, Lagana C, Riccio A. MS-MLPA is a specific and sensitive technique for detecting all chromosome 11p15.5 imprinting defects of BWS and SRS in a single-tube experiment. Eur. J. Hum. Genet.16(5), 565–571 (2008).
  • Gicquel C, Rossignol S, Cabrol S et al. Epimutation of the telomeric imprinting center region on chromosome 11p15 in Silver–Russell syndrome. Nat. Genet.37(9), 1003–1007 (2005).
  • Kosaki K, Kosaki R, Robinson WP et al. Diagnosis of maternal uniparental disomy of chromosome 7 with a methylation specific PCR assay. J. Med. Genet.37(9), E19 (2000).
  • Weinhausel A, Haas OA. Evaluation of the fragile X (FRAXA) syndrome with methylation-sensitive PCR. Hum. Genet.108(6), 450–458 (2001).
  • Hagerman RJ, Leehey M, Heinrichs W et al. Intention tremor, parkinsonism, and generalized brain atrophy in male carriers of fragile X. Neurology57(1), 127–130 (2001).
  • Jacquemont S, Hagerman RJ, Hagerman PJ, Leehey MA. Fragile-X syndrome and fragile X-associated tremor/ataxia syndrome: two faces of FMR1. Lancet Neurol.6(1), 45–55 (2007).
  • Strelnikov V, Nemtsova M, Chesnokova G, Kuleshov N, Zaletayev D. A simple multiplex FRAXA, FRAXE, and FRAXF PCR assay convenient for wide screening programs. Hum. Mutat.13(2), 166–169 (1999).
  • Kubota T, Nonoyama S, Tonoki H et al. A new assay for the analysis of X-chromosome inactivation based on methylation-specific PCR. Hum. Genet.104(1), 49–55 (1999).
  • Lukusa T, Fryns JP. Human chromosome fragility. Biochim. Biophys. Acta1779(1), 3–16 (2008).
  • Weinhaeusel A, Morris MA, Antonarakis SE, Haas OA. DNA deamination enables direct PCR amplification of the cystatin B (CSTB) gene-associated dodecamer repeat expansion in myoclonus epilepsy type Unverricht-Lundborg. Hum. Mutat.22(5), 404–408 (2003).
  • Leithner A, Weinhaeusel A, Zeitlhofer P et al. Evidence of a polyclonal nature of myositis ossificans. Virchows Arch.446(4), 438–441 (2005).
  • Rakyan VK, Down TA, Balding DJ, Beck S. Epigenome-wide association studies for common human diseases. Nat. Rev. Genet.12(8), 529–541 (2011).
  • Portela A, Esteller M. Epigenetic modifications and human disease. Nat. Biotechnol.28(10), 1057–1068 (2010).
  • Feinberg AP, Tycko B. The history of cancer epigenetics. Nat. Rev. Cancer4(2), 143–153 (2004).
  • Rodriguez-Paredes M, Esteller M. Cancer epigenetics reaches mainstream oncology. Nat. Med.17(3), 330–339 (2011).
  • Jones PA, Laird PW. Cancer epigenetics comes of age. Nat. Genet.21(2), 163–167 (1999).
  • Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP. CpG island methylator phenotype in colorectal cancer. Proc. Natl Acad. Sci. USA96(15), 8681–8686 (1999).
  • 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.38(7), 787–793 (2006).
  • Nosho K, Irahara N, Shima K et al. Comprehensive biostatistical analysis of CpG island methylator phenotype in colorectal cancer using a large population-based sample. PLoS One3(11), e3698 (2008).
  • Ogino S, Kawasaki T, Kirkner GJ, Loda M, Fuchs CS. CpG island methylator phenotype-low (CIMP-low) in colorectal cancer: possible associations with male sex and KRAS mutations. J. Mol. Diagn.8(5), 582–588 (2006).
  • Shen L, Toyota M, Kondo Y et al. Integrated genetic and epigenetic analysis identifies three different subclasses of colon cancer. Proc. Natl Acad. Sci. USA104(47), 18654–18659 (2007).
  • Yagi K, Akagi K, Hayashi H et al. Three DNA methylation epigenotypes in human colorectal cancer. Clin. Cancer Res.16(1), 21–33 (2010).
  • Hinoue T, Weisenberger DJ, Lange CP et al. Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res. doi:10.1101/gr.117523.110 (2011) (Epub ahead of print).
  • Lechner M, Boshoff C, Beck S. Cancer epigenome. Adv. Genet.70, 247–276 (2010).
  • Fernandez AF, Assenov Y, Martin-Subero J et al. A DNA methylation fingerprint of 1,628 human samples. Genome Res. doi:10.1101/gr.119867.110 (2011) (Epub ahead of print).
  • Laird PW. Principles and challenges of genomewide DNA methylation analysis. Nat. Rev. Genet.11(3), 191–203 (2010).
  • Kneip C, Schmidt B, Seegebarth A et al. SHOX2 DNA methylation is a biomarker for the diagnosis of lung cancer in plasma. J. Thorac. Oncol.6(10), 1632–1638 (2011).
  • Schmidt B, Liebenberg V, Dietrich D et al. SHOX2 DNA methylation is a biomarker for the diagnosis of lung cancer based on bronchial aspirates. BMC Cancer10, 600 (2010).
  • Ned RM, Melillo S, Marrone M. Fecal DNA testing for colorectal cancer screening: the ColoSure test. PLoS Curr.3, RRN1220 (2011).
  • Muller HM, Widschwendter A, Fiegl H et al. DNA methylation in serum of breast cancer patients: an independent prognostic marker. Cancer Res.63(22), 7641–7645 (2003).
  • Ju HX, An B, Okamoto Y et al. Distinct profiles of epigenetic evolution between colorectal cancers with and without metastasis. Am. J. Pathol.178(4), 1835–1846 (2011).
  • Deng D, Liu Z, Du Y. Epigenetic alterations as cancer diagnostic, prognostic, and predictive biomarkers. Adv. Genet.71, 125–176 (2010).
  • Esteller M, Corn PG, Baylin SB, Herman JG. A gene hypermethylation profile of human cancer. Cancer Res.61(8), 3225–3229 (2001).
  • Maruyama R, Toyooka S, Toyooka KO et al. Aberrant promoter methylation profile of prostate cancers and its relationship to clinicopathological features. Clin. Cancer Res.8(2), 514–519 (2002).
  • Fukushima T, Takeshima H, Kataoka H. Anti-glioma therapy with temozolomide and status of the DNA-repair gene MGMT. Anticancer Res.29(11), 4845–4854 (2009).
  • Metellus P, Coulibaly B, Nanni I et al. Prognostic impact of O6-methylguanine-DNA methyltransferase silencing in patients with recurrent glioblastoma multiforme who undergo surgery and carmustine wafer implantation: a prospective patient cohort. Cancer115(20), 4783–4794 (2009).
  • Hegi ME, Diserens AC, Gorlia T et al.MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med.352(10), 997–1003 (2005).
  • Maier S, Nimmrich I, Koenig T et al. DNA-methylation of the homeodomain transcription factor PITX2 reliably predicts risk of distant disease recurrence in tamoxifen-treated, node-negative breast cancer patients – technical and clinical validation in a multi-centre setting in collaboration with the European Organisation for Research and Treatment of Cancer (EORTC) PathoBiology group. Eur. J. Cancer43(11), 1679–1686 (2007).
  • Scartozzi M, Bearzi I, Mandolesi A et al. Epidermal growth factor receptor (EGFR) gene promoter methylation and cetuximab treatment in colorectal cancer patients. Br. J. Cancer104(11), 1786–1790 (2011).
  • Hewagama A, Richardson B. The genetics and epigenetics of autoimmune diseases. J. Autoimmun.33(1), 3–11 (2009).
  • Fernandez-Morera JL, Calvanese V, Rodriguez-Rodero S, Menendez-Torre E, Fraga MF. Epigenetic regulation of the immune system in health and disease. Tissue Antigens76(6), 431–439 (2010).
  • Fraga MF, Ballestar E, Paz MF et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl Acad. Sci. USA102(30), 10604–10609 (2005).
  • Bell JT, Spector TD. A twin approach to unraveling epigenetics. Trends Genet.27(3), 116–125 (2011).
  • Issa JP, Ottaviano YL, Celano P, Hamilton SR, Davidson NE, Baylin SB. Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat. Genet.7(4), 536–540 (1994).
  • 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.20(4), 440–446 (2010).
  • Milosavljevic A. Emerging patterns of epigenomic variation. Trends Genet.27(6), 242–250 (2011).
  • Gal-Yam EN, Jeong S, Tanay A, Egger G, Lee AS, Jones PA. Constitutive nucleosome depletion and ordered factor assembly at the GRP78 promoter revealed by single molecule footprinting. PLoS Genet.2(9), e160 (2006).
  • Knudsen GP. Gender bias in autoimmune diseases: x chromosome inactivation in women with multiple sclerosis. J. Neurol. Sci.286(1–2), 43–46 (2009).
  • Javierre BM, Fernandez AF, Richter J et al. Changes in the pattern of DNA methylation associate with twin discordance in systemic lupus erythematosus. Genome Res.20(2), 170–179 (2010)
  • Javierre BM, Richardson B. A new epigenetic challenge: systemic lupus erythematosus. Adv. Exp. Med. Biol.711, 117–136 (2011).
  • Baranzini SE, Mudge J, van Velkinburgh JC et al. Genome, epigenome and RNA sequences of monozygotic twins discordant for multiple sclerosis. Nature464(7293), 1351–1356 (2010).
  • Handunnetthi L, Handel AE, Ramagopalan SV. Contribution of genetic, epigenetic and transcriptomic differences to twin discordance in multiple sclerosis. Expert Rev. Neurother.10(9), 1379–1381 (2010).
  • van Vlodrop IJ, Niessen HE, Derks S et al. Analysis of promoter CpG island hypermethylation in cancer: location, location, location! Clin. Cancer Res.17(13), 4225–4231 (2011).
  • Chim SS, Jin S, Lee TY et al. Systematic search for placental DNA-methylation markers on chromosome 21: toward a maternal plasma-based epigenetic test for fetal trisomy 21. Clin. Chem.54(3), 500–511 (2008).
  • Della Ragione F, Mastrovito P, Campanile C et al. Differential DNA methylation as a tool for noninvasive prenatal diagnosis (NIPD) of X chromosome aneuploidies. J. Mol. Diagn.12(6), 797–807 (2010).
  • Old RW, Crea F, Puszyk W, Hulten MA. Candidate epigenetic biomarkers for non-invasive prenatal diagnosis of Down syndrome. Reprod. Biomed. Online15(2), 227–235 (2007).
  • Papageorgiou EA, Fiegler H, Rakyan V et al. Sites of differential DNA methylation between placenta and peripheral blood: molecular markers for noninvasive prenatal diagnosis of aneuploidies. Am. J. Pathol.174(5), 1609–1618 (2009).
  • Tsui DW, Lam YM Lee, WS et al. Systematic identification of placental epigenetic signatures for the noninvasive prenatal detection of Edwards syndrome. PLoS One5(11), e15069 (2010).
  • Papageorgiou EA, Karagrigoriou A, Tsaliki E, Velissariou V, Carter NP, Patsalis PC. Fetal-specific DNA methylation ratio permits noninvasive prenatal diagnosis of trisomy 21. Nat. Med.17(4), 510–513 (2011).
  • Chan KC, Ding C, Gerovassili A et al. Hypermethylated RASSF1A in maternal plasma: a universal fetal DNA marker that improves the reliability of noninvasive prenatal diagnosis. Clin. Chem.52(12), 2211–2218 (2006).
  • Chim SS, Tong YK, Chiu RW et al. Detection of the placental epigenetic signature of the maspin gene in maternal plasma. Proc. Natl Acad. Sci. USA102(41), 14753–14758 (2005).
  • Hahn S, Rusterholz C, Hosli I, Lapaire O. Cell-free nucleic acids as potential markers for preeclampsia. Placenta32(Suppl.), S17–S20 (2011).
  • Zhong XY, Hahn S, Kiefer V, Holzgreve W. Is the quantity of circulatory cell-free DNA in human plasma and serum samples associated with gender, age and frequency of blood donations? Ann. Hematol.86(2), 139–143 (2007).
  • Tan EM, Schur PH, Carr RI, Kunkel HG. Deoxybonucleic acid (DNA) and antibodies to DNA in the serum of patients with systemic lupus erythematosus. J. Clin. Invest.45(11), 1732–1740 (1966).
  • Kaiser J. Medicine. Keeping tabs on tumor DNA. Science327(5969), 1074 (2010).
  • Schwarzenbach H, Hoon DS, Pantel K. Cell-free nucleic acids as biomarkers in cancer patients. Nat. Rev. Cancer11(6), 426–437 (2011).
  • Fleischhacker M, Schmidt B. Circulating nucleic acids (CNAs) and cancer – a survey. Biochim. Biophys. Acta1775(1), 181–232 (2007).
  • Cairns P. Gene methylation and early detection of genitourinary cancer: the road ahead. Nat. Rev. Cancer7(7), 531–543 (2007).
  • Calistri D, Rengucci C, Casadei GA et al. Fecal DNA for noninvasive diagnosis of colorectal cancer in immunochemical fecal occult blood test-positive individuals. Cancer Epidemiol. Biomarkers Prev.19(10), 2647–2654 (2010).
  • Anglim PP, Alonzo TA, Laird-Offringa IA. DNA methylation-based biomarkers for early detection of non-small cell lung cancer: an update. Mol. Cancer7, 81 (2008).
  • Palmisano WA, Divine KK, Saccomanno G et al. Predicting lung cancer by detecting aberrant promoter methylation in sputum. Cancer Res.60(21), 5954–5958 (2000).
  • Board RE, Knight L, Greystoke A et al. DNA methylation in circulating tumour DNA as a biomarker for cancer. Biomark. Insights2, 307–319 (2008).
  • Jung K, Fleischhacker M, Rabien A. Cell-free DNA in the blood as a solid tumor biomarker – a critical appraisal of the literature. Clin. Chim. Acta411(21–22), 1611–1624 (2010).
  • Tan SH, Ida H, Lau QC et al. Detection of promoter hypermethylation in serum samples of cancer patients by methylation-specific polymerase chain reaction for tumour suppressor genes including RUNX3. Oncol. Rep.18(5), 1225–1230 (2007).
  • Belinsky SA, Klinge DM, Dekker JD et al. Gene promoter methylation in plasma and sputum increases with lung cancer risk. Clin. Cancer Res.11(18), 6505–6511 (2005).
  • Van dAI, Elst HJ, Van Laere SJ et al. The presence of circulating total DNA and methylated genes is associated with circulating tumour cells in blood from breast cancer patients. Br. J. Cancer100(8), 1277–1286 (2009).
  • Bailey VJ, Keeley BP, Razavi CR, Griffiths E, Carraway HE, Wang TH. DNA methylation detection using MS-qFRET, a quantum dot-based nanoassay. Methods52(3), 237–241 (2010).
  • Distler J. Quantification of methylated DNA by HeavyMethyl duplex PCR. Methods Mol. Biol.507, 339–346 (2009).
  • Li M, Chen WD, Papadopoulos N et al. Sensitive digital quantification of DNA methylation in clinical samples. Nat. Biotechnol.27(9), 858–863 (2009).
  • Arányi T, Váradi A, Simon I, Tusnády GE. The BiSearch web server. BMC Bioinformatics7, 431 (2006).
  • Pattyn F, Hoebeeck J, Robbrecht P et al. methBLAST and methPrimerDB: web-tools for PCR based methylation analysis. BMC Bioinformatics7, 496 (2006).
  • Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics18(11), 1427–1431 (2002).
  • Brandes JC, Carraway H, Herman JG. Optimal primer design using the novel primer design program: MSPprimer provides accurate methylation analysis of the ATM promoter. Oncogene26(42), 6229–6237 (2007).
  • Marshall OJ. PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics20(15), 2471–2472 (2004).
  • Srivastava GP, Guo J, Shi H, Xu D. PRIMEGENS-v2: genome-wide primer design for analyzing DNA methylation patterns of CpG islands. Bioinformatics24(17), 1837–1842 (2008).
  • Rohde C, Zhang Y, Reinhardt R, Jeltsch A. BISMA – fast and accurate bisulfite sequencing data analysis of individual clones from unique and repetitive sequences. BMC Bioinformatics11, 230 (2010).
  • Ponger L, Mouchiroud D. CpGProD: identifying CpG islands associated with transcription start sites in large genomic mammalian sequences. Bioinformatics18(4), 631–633 (2002).
  • You FM, Huo N, Gu YQ et al. BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinformatics9, 253 (2008).
  • Ongenaert M, Van Neste L, De Meyer T, Menschaert G, Bekaert S, Van Criekinge W. PubMeth: a cancer methylation database combining text-mining and expert annotation. Nucleic Acids Res.36, D842–D846 (2006).
  • Grunau C, Renault E, Rosenthal A, Roizes G. MethDB – a public database for DNA methylation data. Nucleic Acids Res.29(1), 270–274 (2001).
  • Lauss M, Visne I, Weinhaeusel A, Vierlinger K, Noehammer C, Kriegner A. MethCancerDB – aberrant DNA methylation in human cancer. Br. J. Cancer98(4), 816–817 (2008).
  • He X, Chang S, Zhang J et al. MethyCancer: the database of human DNA methylation and cancer. Nucleic Acids Res.36, D836–D841 (2008).
  • Hackenberg M, Barturen G, Oliver JL. NGSmethDB: a database for next-generation sequencing single-cytosine-resolution DNA methylation data. Nucleic Acids Res.39, D75–D79 (2011).
  • Fingerman IM, McDaniel L, Zhang X et al. NCBI Epigenomics: a new public resource for exploring epigenomic data sets. Nucleic Acids Res.39, D908–D912 (2011).
  • Kuo HC, Lin PY, Chung TC et al. DBCAT: database of CpG islands and analytical tools for identifying comprehensive methylation profiles in cancer cells. J. Comput. Biol.18(8), 1013–1017 (2011).
  • Karolchik D, Hinrichs AS, Kent WJ. The UCSC Genome Browser. Curr. Protoc. Bioinformatics Chapter 1, Unit 1.4 (2009).
  • Van der Auwera I, Elst HJ, Van Laere SJ et al. The presence of circulating total DNA and methylated genes is associated with circulating tumour cells in blood from breast cancer patients. Br. J. Cancer100(8), 1277–1286 (2009).
  • Lee BB, Lee EJ, Jung EH et al. 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 (2009).
  • Zhang Y, Wang R, Song H et al. Methylation of multiple genes as a candidate biomarker in non-small cell lung cancer. Cancer Lett.303(1), 21–28 (2011).
  • Ellinger J, El Kassem N, Heukamp LC et al. Hypermethylation of cell-free serum DNA indicates worse outcome in patients with bladder cancer. J. Urol.179(1), 346–352 (2008).
  • Leung WK, To KF, Chu ES et al. Potential diagnostic and prognostic values of detecting promoter hypermethylation in the serum of patients with gastric cancer. Br. J. Cancer92(12), 2190–2194 (2005).
  • Dulaimi E, Uzzo RG, Greenberg RE, Al-Saleem T, Cairns P. Detection of bladder cancer in urine by a tumor suppressor gene hypermethylation panel. Clin. Cancer Res.10(6), 1887–1893 (2004).
  • Hoque MO, Topaloglu O, Begum S et al. Quantitative methylation-specific polymerase chain reaction gene patterns in urine sediment distinguish prostate cancer patients from control subjects. J. Clin. Oncol.23(27), 6569–6575 (2005).
  • Leung WK, To KF, Man EP et al. Detection of hypermethylated DNA or cyclooxygenase-2 messenger RNA in fecal samples of patients with colorectal cancer or polyps. Am. J. Gastroenterol.102(5), 1070–1076 (2007).
  • Shivapurkar N, Stastny V, Suzuki M et al. Application of a methylation gene panel by quantitative PCR for lung cancers. Cancer Lett.247(1), 56–71 (2007).
  • Topaloglu O, Hoque MO, Tokumaru Y et al. Detection of promoter hypermethylation of multiple genes in the tumor and bronchoalveolar lavage of patients with lung cancer. Clin. Cancer Res.10(7), 2284–2288 (2004).
  • Yamamoto N, Nakayama T, Kajita M et al. Detection of aberrant promoter methylation of GSTP1, RASSF1A, and RARβ2 in serum DNA of patients with breast cancer by a newly established one-step methylation-specific PCR assay. Breast Cancer Res. Treat. doi:10.1007/s10549-011-1575-1572 (2011) (Epub ahead of print).
  • Hoffmann AC, Kaifi JT, Vallböhmer D et al. Lack of prognostic significance of serum DNA methylation of DAPK, MGMT, and GSTPI in patients with non-small cell lung cancer. J. Surg. Oncol.100(5), 414–417 (2009).
  • Sunami E, Shinozaki M, Higano CS et al. Multimarker circulating DNA assay for assessing blood of prostate cancer patients. Clin. Chem.55(3), 559–567 (2009). Erratum in Clin. Chem.55(6), 1258 (2009) Mizuno R (added).
  • Hoque MO, Begum S, Topaloglu O et al. Quantitation of promoter methylation of multiple genes in urine DNA and bladder cancer detection. J. Natl Cancer Inst.98(14), 996–1004 (2006).
  • Rouprêt M, Hupertan V, Yates DR et al. Molecular detection of localized prostate cancer using quantitative methylation-specific PCR on urinary cells obtained following prostate massage. Clin. Cancer Res.13(6), 1720–1725 (2007).
  • Wang YC, Yu ZH, Liu C et al. Detection of RASSF1A promoter hypermethylation in serum from gastric and colorectal adenocarcinoma patients. World J. Gastroenterol.14(19), 3074–3080 (2008).
  • Fujiwara K, Fujimoto N, Tabata M et al. Identification of epigenetic aberrant promoter methylation in serum DNA is useful for early detection of lung cancer. Clin. Cancer Res.11(3), 1219–1225 (2005).
  • Misawa A, Tanaka S, Yagyu S et al. RASSF1A hypermethylation in pretreatment serum DNA of neuroblastoma patients: a prognostic marker. Br. J. Cancer100(2), 399–404 (2009).
  • Friedrich MG, Weisenberger DJ, Cheng JC et al. Detection of methylated apoptosis-associated genes in urine sediments of bladder cancer patients. Clin. Cancer Res.10(22), 7457–7465 (2004).
  • Criel B, Dujardin B. Front-line epidemiology. J. Trop. Pediatr.38(3), 137–138 (1992).
  • Radpour R, Barekati Z, Kohler C et al. Hypermethylation of tumor suppressor genes involved in critical regulatory pathways for developing a blood-based test in breast cancer. PLoS One6(1), e16080 (2011).
  • Nakayama H, Hibi K, Takase T et al. Molecular detection of p16 promoter methylation in the serum of recurrent colorectal cancer patients. Int. J. Cancer105(4), 491–493 (2003).
  • Zhang Y, Wang R, Song H et al. Methylation of multiple genes as a candidate biomarker in non-small cell lung cancer. Cancer Lett.303(1), 21–28 (2011).
  • Valenzuela MT, Galisteo R, Zuluaga A et al. Assessing the use of p16(INK4a) promoter gene methylation in serum for detection of bladder cancer. Eur. Urol.42(6), 622–628; discussion 628–630 (2002).
  • Schwarzenbach H, Chun FK, Isbarn H, Huland H, Pantel K. Genomic profiling of cell-free DNA in blood and bone marrow of prostate cancer patients. J. Cancer Res. Clin. Oncol.137(5), 811–819 (2001).
  • Wakabayashi T, Natsume A, Hatano H et al. p16 promoter methylation in the serum as a basis for the molecular diagnosis of gliomas. Neurosurgery64(3), 455–461; discussion 461–462 (2009).
  • Abbaszadegan MR, Moaven O, Sima HR et al. p16 promoter hypermethylation: a useful serum marker for early detection of gastric cancer. World J. Gastroenterol.14(13), 2055–2060 (2008).
  • Serizawa RR, Ralfkiaer U, Steven K et al. Integrated genetic and epigenetic analysis of bladder cancer reveals an additive diagnostic value of FGFR3 mutations and hypermethylation events. Int. J. Cancer129(1), 78–87 (2011).
  • Petko Z, Ghiassi M, Shuber A et al. 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 (2005).
  • Belinsky SA, Klinge DM, Dekker JD et al. Gene promoter methylation in plasma and sputum increases with lung cancer risk. Clin. Cancer Res.11(18), 6505–6511 (2005).
  • Liu BL, Cheng JX, Zhang W et al. Quantitative detection of multiple gene promoter hypermethylation in tumor tissue, serum, and cerebrospinal fluid predicts prognosis of malignant gliomas. Neuro. Oncol.12(6), 540–548 (2010).
  • Taback B, Giuliano AE, Lai R et al. Epigenetic analysis of body fluids and tumor tissues: application of a comprehensive molecular assessment for early-stage breast cancer patients. Ann. NY Acad. Sci.1075, 211–221 (2006).
  • Lavon I, Refael M, Zelikovitch B, Shalom E, Siegal T. Serum DNA can define tumor-specific genetic and epigenetic markers in gliomas of various grades. Neuro. Oncol.12(2), 173–180 (2010).
  • Jing F, Yuping W, Yong C et al. CpG island methylator phenotype of multigene in serum of sporadic breast carcinoma. Tumour Biol.31(4), 321–331 (2010).
  • Wong TS, Kwong DL, Sham JS, Wei WI, Kwong YL, Yuen AP. Quantitative plasma hypermethylated DNA markers of undifferentiated nasopharyngeal carcinoma. Clin. Cancer Res.10(7), 2401–2406 (2004).

Patents

  • Weinhaeusel A, Noehammer C. Methylation Assay. EP 09450020.4 (2009).
  • Weinhaeusel A. Lung Cancer Methylation Markers. WO2010086388 (2010).
  • Weinhäusel A, Haas OA. Method for detecting and evaluating a potentially aberrantly methylated DNS region on the X chromosome or the clonality. WO0140507 (1999).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.