1,085
Views
0
CrossRef citations to date
0
Altmetric
Review

DNA Methylation as a Molecular Biomarker in Gastric Cancer

&
Pages 475-486 | Published online: 16 Jun 2015

References

  • Ferlay J , BrayF , ParkinDM , PisaniP ( Eds ). Gobocan 2000: Cancer Incidence and Mortality Worldwide (IARC Cancer Bases No. 5) . Lyon: IARC Press ( 2001 ).
  • Lau M , LeA , El-SeragHB . Noncardia gastric adenocarcinoma remains an important and deadly cancer in the United States: secular trends in incidence and survival . Am. J. Gastroenterol.101 ( 11 ), 2485 – 2492 ( 2006 ).
  • Nashimoto A , AkazawaK , IsobeYet al. Gastric cancer treated in 2002 in Japan: 2009 annual report of the JGCA nationwide registry . Gastric Cancer16 ( 1 ), 1 – 27 ( 2013 ).
  • Uemura N , OkamotoS , YamamotoSet al. Helicobacter pylori infection and the development of gastric cancer . N. Engl. J. Med.345 ( 11 ), 784 – 789 ( 2001 ).
  • Vogelstein B , PapadopoulosN , VelculescuVEet al. Cancer genome landscapes . Science339 , 1546 – 1558 ( 2013 ).
  • Ushijima T , AsadaK . Aberrant DNA methylation in contrast with mutations . Cancer Sci.101 , 300 – 305 ( 2010 ).
  • Calcagno DQ , GigekCO , ChenES , BurbanoRR , SmithMA . DNA and histone methylation in gastric carcinogenesis . World J. Gastroenterol.19 , 1182 – 1192 ( 2013 ).
  • Tsai KW , WuCW , HuLYet al. Epigenetic regulation of miR-34b and miR-129 expression in gastric cancer . Int. J. Cancer129 , 2600 – 2610 ( 2011 ).
  • Ziogas D , RoukosD . Epigenetics in gastric cancer: challenges for clinical implications . Ann. Surg. Oncol.16 , 2077 – 2078 ( 2009 ).
  • Wolffe AP , MatzkeMA . Epigenetics: regulation through repression . Science286 , 481 – 486 ( 1999 ).
  • Gama-Sosa MA , SlagelVA , TrewynRWet al. The 5-methylcytosine contentof DNA from human tumors . Nucleic Acids Res.11 , 6883 – 6894 ( 1983 ).
  • Dunn BK . Hypomethylation: one side of a larger picture . Ann. NY Acad. Sci.983 , 28 – 42 ( 2003 ).
  • Esteller M , HermanJG . Cancer as an epigenetic disease: DNA methylation and chromatin alterations in human tumours . J. Pathol.196 , 1 – 7 ( 2002 ).
  • Eden A , GaudetF , WaghmareA , JaenischR . Chromosomal instability and tumors promoted by DNA hypomethylation . Science300 , 455 ( 2003 ).
  • Gaudet F , HodgsonJG , EdenAet al. Induction of tumors in mice by genomic hypomethylation . Science300 , 489 – 492 ( 2003 ).
  • Ehrlich M . DNA methylation in cancer: too much, but also too little . Oncogene21 , 5400 – 5413 ( 2002 ).
  • Ehrlich M . DNA hypomethylation, cancer, the immunodeficiency, centromeric region instability, facial anomalies syndrome and chromosomal rearrangements . J. Nutr.132 , 2424S – 2429S ( 2002 ).
  • Berman BP , WeisenbergerDJ , AmanJFet al. Regions of focal DNA hypermethylation and long-range hypomethylation in colorectal cancer coincide with nuclear lamina-associated domains . Nat. Genet.44 ( 1 ), 40 – 46 ( 2011 ).
  • Timp W , FeinbergAP . Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host . Nat. Rev. Cancer13 ( 7 ), 497 – 510 ( 2013 ).
  • Jones PA , BaylinSB . The epigenomics of cancer . Cell128 ( 4 ), 683 – 692 ( 2007 ).
  • Toyota M , IssaJP . Epigenetic changes in solid and hematopoietic tumors . Semin. Oncol.32 ( 5 ), 521 – 530 ( 2005 ).
  • Ushijima T . Detection and interpretation of altered methylation patterns in cancer cells . Nat. Rev. Cancer5 ( 3 ), 223 – 231 ( 2005 ).
  • Bird AP , WolffeAP . Methylation-induced repression–belts, braces, and chromatin . Cell99 ( 5 ), 451 – 454 ( 1999 ).
  • Jones PA , LairdPW . Cancer epigenetics comes of age . Nat. Genet.21 ( 2 ), 163 – 7 ( 1999 ).
  • Toyota M , AhujaN , Ohe-ToyotaM , HermanJG , BaylinSB , IssaJP . CpG island methylator phenotype in colorectal cancer . Proc. Natl Acad. Sci. USA96 ( 15 ), 8681 – 8686 ( 1999 ).
  • Kusano M , ToyotaM , SuzukiHet al. Genetic, epigenetic, and clinicopathologic features of gastric carcinomas with the CpG island methylator phenotype and an association with Epstein-Barr virus . Cancer106 ( 7 ), 1467 – 1479 ( 2006 ).
  • Cancer Genome Atlas Network . Comprehensive molecular characterization of gastric adenocarcinoma . Nature513 ( 7517 ), 202 – 209 ( 2014 ).
  • Maekita T , NakazawaK , MiharaMet al. High levels of aberrant DNA methylation in Helicobacter pylori-infected gastric mucosae and its possible association with gastric cancer risk . Clin. Cancer Res.12 ( 3 Pt 1 ), 989 – 995 ( 2006 ).
  • Tahara T , ArisawaT , ShibataTet al. Increased number of methylated CpG islands correlates with Helicobacter pylori infection, histological and serological severity of chronic gastritis . Eur. J. Gastroenterol. Hepatol.21 ( 6 ), 613 – 619 ( 2009 ).
  • Tahara T , ShibataT , NakamuraMet al. Increased number of CpG island hypermethylation in tumor suppressor genes of non-neoplastic gastric mucosa correlates with higher risk of gastric cancer . Digestion82 ( 1 ), 27 – 36 ( 2010 ).
  • Nakajima T , MaekitaT , OdaIet al. Higher methylation levels in gastric mucosae significantly correlate with higher risk of gastric cancers . Cancer Epidemiol. Biomarkers Prev.15 ( 11 ), 2317 – 2321 ( 2006 ).
  • Marsit CJ , KoestlerDC , ChristensenBC , KaragasMR , HousemanEA , KelseyKT . DNA methylation array analysis identifies profiles of blood-derived DNA methylation associated with bladder cancer . J. Clin. Oncol.29 ( 9 ), 1133 – 1139 ( 2011 ).
  • Wong EM , SoutheyMC , FoxSBet al. Constitutional methylation of the BRCA1 promoter is specifically associated with BRCA1 mutation-associated pathology in early-onset breast cancer . Cancer Prev. Res. (Phila).4 ( 1 ), 23 – 33 ( 2011 ).
  • Tahara T , MaegawaS , ChungWet al. Examination of whole blood DNA methylation as a potential risk marker for gastric cancer . Cancer. Prev. Res. (Phila).6 ( 10 ), 1093 – 1100 ( 2013 ).
  • Yuasa Y , NagasakiH , OzeIet al. Insulin-like growth factor 2 hypomethylation of blood leukocyte DNA is associated with gastric cancer risk . Int. J. Cancer131 ( 11 ), 2596 – 2603 ( 2012 ).
  • Laird PW . The power and the promise of DNA methylation markers . Nat. Rev. Cancer3 ( 4 ), 253 – 266 ( 2003 ).
  • Suzuki H , TokinoT , ShinomuraY , ImaiK , ToyotaM . DNA methylation and cancer pathways in gastrointestinal tumors . Pharmacogenomics9 ( 12 ), 1917 – 1928 ( 2008 ).
  • Shen L , ToyotaM , KondoYet al. Integrated genetic and epigenetic analysis identifies three different subclasses of colon cancer . Proc. Natl Acad. Sci. USA104 ( 47 ), 18654 – 18659 ( 2007 ).
  • Ahn JB , ChungWB , MaedaOet al. DNA methylation predicts recurrence from resected stage III proximal colon cancer . Cancer117 ( 9 ), 1847 – 1854 ( 2011 ).
  • Ogino S , NoshoK , KirknerGJet al. CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer . Gut58 ( 1 ), 90 – 96 ( 2009 ).
  • Hughes LA , MelotteV , de SchrijverJet al. The CpG island methylator phenotype: what’s in a name? Cancer Res. 73 ( 19 ), 5858 – 5868 ( 2013 ).
  • Toyota M , AhujaN , SuzukiHet al. Aberrant methylation in gastric cancer associated with the CpG island methylator phenotype . Cancer Res.59 ( 21 ), 5438 – 5442 ( 1999 ).
  • Kim H , KimYH , KimSE , KimNG , NohSH , KimH . Concerted promoter hypermethylation of hMLH1, p16INK4A, and E-cadherin in gastric carcinomas with microsatellite instability . J. Pathol.200 ( 1 ), 23 – 31 ( 2003 ).
  • An C , ChoiIS , YaoJCet al. Prognostic significance of CpG island methylator phenotype and microsatellite instability in gastric carcinoma . Clin. Cancer Res.11 ( 2 Pt 1 ), 656 – 663 ( 2005 ).
  • Enomoto S , MaekitaT , TsukamotoTet al. Lack of association between CpG island methylator phenotype in human gastric cancers and methylation in their background non-cancerous gastric mucosae . Cancer Sci.98 ( 12 ), 1853 – 1861 ( 2007 ).
  • Park SY , KookMC , KimYWet al. CpG island hypermethylator phenotype in gastric carcinoma and its clinicopathological features . Virchows Arch.457 ( 4 ), 415 – 422 ( 2010 ).
  • Chen HY , ZhuBH , ZhangCHet al. High CpG island methylator phenotype is associated with lymph node metastasis and prognosis in gastric cancer . Cancer Sci.103 ( 1 ), 73 – 79 ( 2012 ).
  • Zouridis H , DengN , IvanovaTet al. Methylation subtypes and large-scale epigenetic alterations in gastric cancer . Sci. Transl. Med.4 ( 156 ), 156ra140 ( 2012 ).
  • Widschwendter M , FieglH , EgleDet al. Epigenetic stem cell signature in cancer . Nat. Genet.39 , 157 – 158 ( 2007 ).
  • Loh M , LiemN , VaithilingamAet al. DNA methylation subgroups and the CpG island methylator phenotype in gastric cancer: a comprehensive profiling approach . BMC Gastroenterol.14 , 55 ( 2014 ).
  • Matsusaka K , KanedaA , NagaeGet al. Classification of Epstein-Barr virus-positive gastric cancers by definition of DNA methylation epigenotypes . Cancer Res.71 ( 23 ), 7187 – 7197 ( 2011 ).
  • Noushmehr H , WeisenbergerDJ , DiefesKet al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma . Cancer Cell17 ( 5 ), 510 – 522 ( 2010 ).
  • Figueroa ME , Abdel-WahabO , LuCet al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation . Cancer Cell18 ( 6 ), 553 – 567 ( 2010 ).
  • Tahara T , YamamotoE , MadireddiPet al. Colorectal carcinomas with CpG island methylator phenotype 1 frequently contain mutations in chromatin regulators . Gastroenterology146 ( 2 ), 530 – 538.e5 ( 2014 ).
  • Wang K , KanJ , YuenSTet al. Exome sequencing identifies frequent mutation of ARID1A in molecular subtypes of gastric cancer . Nat. Genet.43 ( 12 ), 1219 – 1223 ( 2011 ).
  • Zang ZJ , CutcutacheI , PoonSLet al. Exome sequencing of gastric adenocarcinoma identifies recurrent somatic mutations in cell adhesion and chromatin remodeling genes . Nat. Genet.44 ( 5 ), 570 – 574 ( 2012 ).
  • Satoh A , ToyotaM , ItohFet al. Epigenetic inactivation of CHFR and sensitivity to microtubule inhibitors in gastric cancer . Cancer Res.63 ( 24 ), 8606 – 8613 ( 2003 ).
  • Du W , WangS , ZhouQet al. ADAMTS9 is a functional tumor suppressor through inhibiting AKT/mTOR pathway and associated with poor survival in gastric cancer . Oncogene32 ( 28 ), 3319 – 3328 ( 2013 ).
  • Cheng AS , LiMS , KangWet al. Helicobacter pylori causes epigenetic dysregulation of FOXD3 to promote gastric carcinogenesis . Gastroenterology144 ( 1 ), 122 – 133.e9 ( 2013 ).
  • Li X , CheungKF , MaXet al. Epigenetic inactivation of paired box gene 5, a novel tumor suppressor gene, through direct upregulation of p53 is associated with prognosis in gastric cancer patients . Oncogene31 ( 29 ), 3419 – 3430 ( 2012 ).
  • Weisenberger DJ , SiegmundKD , CampanMet al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer . Nat. Genet.38 , 787 – 793 ( 2006 ).
  • Ogino S , KawasakiT , KirknerGJ , KraftP , LodaM , FuchsCS . Evaluation of markers for CpG island methylator phenotype (CIMP) in colorectal cancer by a large population-based sample . J. Mol. Diagn.9 , 305 – 314 ( 2007 ).
  • Zong L , SetoY . CpG island methylator phenotype, Helicobacter pylori, Epstein-Barr virus, and microsatellite instability and prognosis in gastric cancer: a systematic review and meta-analysis . PLoS ONE9 ( 1 ), e86097 ( 2014 ).
  • Jover R , NguyenTP , Perez-CarbonellLet al. 5-Fluorouracil adjuvant chemotherapy does not increase survival in patients with CpG island methylator phenotype colorectal cancer . Gastroenterology140 ( 4 ), 1174 – 1181 ( 2011 ).
  • Wang M , FurutaT , TakashimaMet al. Relation between interleukin-1beta messenger RNA in gastric fundic mucosa and gastric juice pH in patients infected with Helicobacter pylori . J. Gastroenterol.34 ( Suppl. 11 ), 10 – 17 ( 1999 ).
  • Yamaoka Y , KitaM , KodamaT , SawaiN , KashimaK , ImanishiJ . Induction of various cytokines and development of severe mucosal inflammation by cagA gene positive Helicobacter pylori strains . Gut41 ( 4 ), 442 – 451 ( 1997 ).
  • Kang GH , ShimYH , JungHY , KimWH , RoJY , RhyuMG . CpG island methylation in premalignant stages of gastric carcinoma . Cancer Res.61 ( 7 ), 2847 – 2851 ( 2001 ).
  • Kang GH , LeeHJet al. Aberrant CpG island hypermethylation of chronic gastritis, in relation to aging, gender, intestinal metaplasia, and chronic inflammation . Am. J. Pathol.163 ( 4 ), 1551 – 1556 ( 2003 ).
  • Li WQ , PanKF , ZhangYet al. RUNX3 methylation and expression associated with advanced precancerous gastric lesions in a Chinese population . Carcinogenesis32 ( 3 ), 406 – 410 ( 2011 ).
  • Kaise M , YamasakiT , YonezawaJ , MiwaJ , OhtaY , TajiriH . CpG island hypermethylation of tumor-suppressor genes in H. pylori-infected non-neoplastic gastric mucosa is linked with gastric cancer risk . Helicobacter13 ( 1 ), 35 – 41 ( 2008 ).
  • Yamashita M , ToyotaM , SuzukiHet al. DNA methylation of interferon regulatory factors in gastric cancer and noncancerous gastric mucosae . Cancer Sci.101 ( 7 ), 1708 – 1716 ( 2010 ).
  • Yamamoto E , ToyotaM , SuzukiHet al. 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 ( 2008 ).
  • Suzuki H , YamamotoE , NojimaMet al. Methylation-associated silencing of microRNA-34b/c in gastric cancer and its involvement in an epigenetic field defect . Carcinogenesis31 ( 12 ), 2066 – 2073 ( 2010 ).
  • Meyer-ter-Vehn T , CovacciA , KistM , PahlHL . Helicobacter pylori activates mitogen-activated protein kinase cascades and induces expression of the proto-oncogenes c-fos and c-jun . J. Biol. Chem.275 ( 21 ), 16064 – 16072 ( 2000 ).
  • Issa JP , AhujaN , ToyotaM , BronnerMP , BrentnallTA . Accelerated age-related CpG island methylation in ulcerative colitis . Cancer Res.61 ( 9 ), 3573 – 357 ( 2001 ).
  • Nishida N , NagasakaT , NishimuraT , IkaiI , BolandCR , GoelA . Aberrant methylation of multiple tumor suppressor genes in aging liver, chronic hepatitis, and hepatocellular carcinoma . Hepatology47 ( 3 ), 908 – 918 ( 2008 ).
  • Niwa T , TsukamotoT , ToyodaTet al. Inflammatory processes triggered by Helicobacter pylori infection cause aberrant DNA methylation in gastric epithelial cells . Cancer Res.70 ( 4 ), 1430 – 1440 ( 2010 ).
  • Fukase K , KatoM , KikuchiSet al. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial . Lancet372 ( 9636 ), 392 – 397 ( 2008 ).
  • Nakajima T , EnomotoS , YamashitaSet al. Persistence of a component of DNA methylation in gastric mucosae after Helicobacter pylori eradication . J. Gastroenterol.45 ( 1 ), 37 – 44 ( 2010 ).
  • Shin CM , KimN , ParkJHet al. Prediction of the risk for gastric cancer using candidate methylation markers in the non-neoplastic gastric mucosae . J. Pathol.226 ( 4 ), 654 – 665 ( 2012 ).
  • Ichikawa D , KoikeH , IkomaHet al. Detection of aberrant methylation as a tumor marker in serum of patients with gastric cancer . Anticancer Res.24 ( 4 ), 2477 – 2481 ( 2004 ).
  • Kolesnikova EV , TamkovichSN , BryzgunovaOEet al. Circulating DNA in the blood of gastric cancer patients . Ann. NY Acad. Sci.1137 , 226 – 231 ( 2008 ).
  • Ikoma H , IchikawaD , DaitoIet al. Clinical application of methylation specific-polymerase chain reaction in serum of patients with gastric cancer . Hepatogastroenterology54 ( 75 ), 946 – 950 ( 2007 ).
  • Cheung KF , LamCN , WuKet al. Characterization of the gene structure, functional significance, and clinical application of RNF180, a novel gene in gastric cancer . Cancer118 ( 4 ), 947 – 959 ( 2012 ).
  • Yu QM , WangXB , LuoJet al. CDH1 methylation in preoperative peritoneal washes is an independent prognostic factor for gastric cancer . J. Surg. Oncol.106 ( 6 ), 765 – 771 ( 2012 ).
  • Watanabe Y , KimHS , CastoroRJet al. Sensitive and specific detection of early gastric cancer with DNA methylation analysis of gastric washes . Gastroenterology136 ( 7 ), 2149 – 2158 ( 2009 ).
  • Oishi Y , WatanabeY , YoshidaYet al. Hypermethylation of Sox17 gene is useful as a molecular diagnostic application in early gastric cancer . Tumour Biol.33 ( 2 ), 383 – 393 ( 2012 ).
  • Christensen BC , HousemanEA , MarsitCJet al. Aging and environmental exposures alter tissuespecific DNA methylation dependent upon CpG island context . PLoS Genet.5 ( 8 ), e1000602 ( 2009 ).
  • Teschendorff AE , MenonU , Gentry-MaharajAet al. Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer . Genome Res.20 ( 4 ), 440 – 446 ( 2012 ).
  • Hou L , WangH , SartoriSet al. Blood leukocyte DNA hypomethylation and gastric cancer risk in a high-risk Polish population . Int. J. Cancer127 ( 8 ), 1866 – 1874 ( 2010 ).
  • Gao Y , BaccarelliA , ShuXOet al. Blood leukocyte Alu and LINE-1 methylation and gastric cancer risk in the Shanghai Women’s Health Study . Br. J. Cancer106 ( 3 ), 585 – 591 ( 2012 ).

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:

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:

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.