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Research Article

MiR-377 Reverses Cancerous Phenotypes of Pancreatic Cells Via Suppressing DNMT1 and Demethylating Tumor Suppressor Genes

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Pages 1059-1075 | Received 13 Dec 2016, Accepted 04 May 2017, Published online: 31 Jul 2017

References

  • Siegel R , NaishadhamD , JemalA . Cancer statistics, 2013 . CA Cancer J. Clin.63 ( 1 ), 11 – 30 ( 2013 ).
  • Li J , WientjesMG , AuJL . Pancreatic cancer: pathobiology, treatment options, and drug delivery . AAPS J.12 ( 2 ), 223 – 232 ( 2010 ).
  • Werner J , CombsSE , SpringfeldC , HartwigW , HackertT , BuchlerMW . Advanced-stage pancreatic cancer: therapy options . Nat. Rev. Clin. Oncol.10 ( 6 ), 323 – 333 ( 2013 ).
  • Ryan DP , HongTS , BardeesyN . Pancreatic adenocarcinoma . N. Engl. J. Med.371 ( 11 ), 1039 – 1049 ( 2014 ).
  • Delpu Y , HanounN , LulkaHet al. Genetic and epigenetic alterations in pancreatic carcinogenesis . Curr. Genomics12 ( 1 ), 15 – 24 ( 2011 ).
  • Arai E , KanaiY . DNA methylation profiles in precancerous tissue and cancers: carcinogenetic risk estimation and prognostication based on DNA methylation status . Epigenomics2 ( 3 ), 467 – 481 ( 2010 ).
  • Jair KW , BachmanKE , SuzukiHet al. De novo CpG island methylation in human cancer cells . Cancer Res.66 ( 2 ), 682 – 692 ( 2006 ).
  • Denis H , NdlovuMN , FuksF . Regulation of mammalian DNA methyltransferases: a route to new mechanisms . EMBO Rep.12 ( 7 ), 647 – 656 ( 2011 ).
  • Ting AH , JairKW , SchuebelKE , BaylinSB . Differential requirement for DNA methyltransferase 1 in maintaining human cancer cell gene promoter hypermethylation . Cancer Res.66 ( 2 ), 729 – 735 ( 2006 ).
  • Li A , OmuraN , HongSM , GogginsM . Pancreatic cancer DNMT1 expression and sensitivity to DNMT1 inhibitors . Cancer Biol. Ther.9 ( 4 ), 321 – 329 ( 2010 ).
  • Goyal R , RathertP , LaserH , GowherH , JeltschA . Phosphorylation of serine-515 activates the mammalian maintenance methyltransferase Dnmt1 . Epigenetics2 ( 3 ), 155 – 160 ( 2007 ).
  • Kanai Y , HirohashiS . Alterations of DNA methylation associated with abnormalities of DNA methyltransferases in human cancers during transition from a precancerous to a malignant state . Carcinogenesis28 ( 12 ), 2434 – 2442 ( 2007 ).
  • Etoh T , KanaiY , UshijimaSet al. Increased DNA methyltransferase 1 (DNMT1) protein expression correlates significantly with poorer tumor differentiation and frequent DNA hypermethylation of multiple CpG islands in gastric cancers . Am. J. Pathol.164 ( 2 ), 689 – 699 ( 2004 ).
  • Saito Y , KanaiY , NakagawaTet al. Increased protein expression of DNA methyltransferase (DNMT) 1 is significantly correlated with the malignant potential and poor prognosis of human hepatocellular carcinomas . Int. J. Cancer105 ( 4 ), 527 – 532 ( 2003 ).
  • Peng DF , KanaiY , SawadaMet al. Increased DNA methyltransferase 1 (DNMT1) protein expression in precancerous conditions and ductal carcinomas of the pancreas . Cancer Sci.96 ( 7 ), 403 – 408 ( 2005 ).
  • Sun M , HurstLD , CarmichaelGG , ChenJ . Evidence for a preferential targeting of 3′-UTRs by cis-encoded natural antisense transcripts . Nucleic Acids Res.33 ( 17 ), 5533 – 5543 ( 2005 ).
  • Bartel DP . MicroRNAs: genomics, biogenesis, mechanism, and function . Cell116 ( 2 ), 281 – 297 ( 2004 ).
  • Friedman RC , FarhKK , BurgeCB , BartelDP . Most mammalian mRNAs are conserved targets of microRNAs . Genome Res.19 ( 1 ), 92 – 105 ( 2009 ).
  • Suzuki H , MaruyamaR , YamamotoE , KaiM . DNA methylation and microRNA dysregulation in cancer . Mol. Oncol.6 ( 6 ), 567 – 578 ( 2012 ).
  • Rachagani S , KumarS , BatraSK . MicroRNA in pancreatic cancer: pathological, diagnostic and therapeutic implications . Cancer Lett.292 ( 1 ), 8 – 16 ( 2010 ).
  • Vasilatou D , PapageorgiouSG , DimitriadisG , PappaV . Epigenetic alterations and microRNAs: new players in the pathogenesis of myelodysplastic syndromes . Epigenetics8 ( 6 ), 561 – 570 ( 2013 ).
  • Hildebrandt MA , GuJ , LinJet al. Hsa-miR-9 methylation status is associated with cancer development and metastatic recurrence in patients with clear cell renal cell carcinoma . Oncogene29 ( 42 ), 5724 – 5728 ( 2010 ).
  • Kozaki K , ImotoI , MogiS , OmuraK , InazawaJ . Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer . Cancer Res.68 ( 7 ), 2094 – 2105 ( 2008 ).
  • Hanoun N , DelpuY , SuriawinataAAet al. The silencing of microRNA 148a production by DNA hypermethylation is an early event in pancreatic carcinogenesis . Clin. Chem.56 ( 7 ), 1107 – 1118 ( 2010 ).
  • Stumpel DJ , SchotteD , Lange-TurenhoutEAet al. Hypermethylation of specific microRNA genes in MLL-rearranged infant acute lymphoblastic leukemia: major matters at a micro scale . Leukemia25 ( 3 ), 429 – 439 ( 2011 ).
  • Kita Y , VincentK , NatsugoeS , Berindan-NeagoeI , CalinGA . Epigenetically regulated microRNAs and their prospect in cancer diagnosis . Expert Rev. Mol. Diagn.14 ( 6 ), 673 – 683 ( 2014 ).
  • Lomberk GA , IovannaJ , UrrutiaR . The promise of epigenomic therapeutics in pancreatic cancer . Epigenomics8 ( 6 ), 831 – 842 ( 2016 ).
  • Braconi C , HuangN , PatelT . MicroRNA-dependent regulation of DNA methyltransferase-1 and tumor suppressor gene expression by interleukin-6 in human malignant cholangiocytes . Hepatology51 ( 3 ), 881 – 890 ( 2010 ).
  • Azizi M , Teimori-ToolabiL , ArzananiMKet al. MicrRNA-148b and microRNA-152 reactivate tumor suppressor genes through suppressin of DNA methyltransferase-1 gene in panvreatic cancer cell line . Cancer Biol. Ther.14 ( 5 ), 419 – 427 ( 2014 ).
  • Pfaffl MW , HorganGW , DempfleL . Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR . Nucleic Acids Res.30 ( 9 ), e36 ( 2002 ).
  • Chen C , RidzonDA , BroomerAJet al. Real-time quantification of microRNAs by stem-loop RT-PCR . Nucleic Acids Res.33 ( 20 ), e179 ( 2005 ).
  • Mohammadi-Yeganeh S , ParyanM , MirabSamieeSet al. Development of a robust, low cost stem-loop real-time quantification PCR technique for miRNA expression analysis . Mol. Biol. Rep.40 ( 5 ), 3665 – 3674 ( 2013 ).
  • The mfold Web Server . http://mfold.rna.albany.edu/?q=mfold/ .
  • DataBase of CpG islands and Analytical Tools (DBCAT) . http://dbcat.cgm.ntu.edu.tw/ .
  • John B , EnrightAJ , AravinA , TuschlT , SanderC , MarksDS . Human microRNA targets . PLoS Biol.2 ( 11 ), e363 ( 2004 ).
  • Lewis BP , ShihI-H , Jones-RhoadesMW , BartelDP , BurgeCB . Prediction of mammalian microRNA targets . Cell115 ( 7 ), 787 – 798 ( 2003 ).
  • Krek A , GrünD , PoyMNet al. Combinatorial microRNA target predictions . Nat. Genetics37 ( 5 ), 495 – 500 ( 2005 ).
  • Omura N , GogginsM . Epigenetics and epigenetic alterations in pancreatic cancer . Int. J. Clin. Exp. Pathol.2 ( 4 ), 310 – 326 ( 2009 ).
  • Mizuno S , ChijiwaT , OkamuraTet al. Expression of DNA methyltransferases DNMT1, 3A, and 3B in normal hematopoiesis and in acute and chronic myelogenous leukemia . Blood97 ( 5 ), 1172 – 1179 ( 2001 ).
  • Nguyen T , KuoC , NichollMBet al. Downregulation of microRNA-29c is associated with hypermethylation of tumor-related genes and disease outcome in cutaneous melanoma . Epigenetics6 ( 3 ), 388 – 394 ( 2011 ).
  • Huang J , WangY , GuoY , SunS . Down-regulated microRNA-152 induces aberrant DNA methylation in hepatitis B virus-related hepatocellular carcinoma by targeting DNA methyltransferase 1 . Hepatology52 ( 1 ), 60 – 70 ( 2010 ).
  • Formosa A , MarkertEK , LenaAMet al. MicroRNAs, miR-154, miR-299–5p, miR-376a, miR-376c, miR-377, miR-381, miR-487b, miR-485–3p, miR-495 and miR-654–3p, mapped to the 14q32.31 locus, regulate proliferation, apoptosis, migration and invasion in metastatic prostate cancer cells . Oncogene33 ( 44 ), 5173 – 5182 ( 2013 ).
  • Zhang L , VoliniaS , BonomeTet al. Genomic and epigenetic alterations deregulate microRNA expression in human epithelial ovarian cancer . Proc. Natl Acad. Sci. USA105 ( 19 ), 7004 – 7009 ( 2008 ).
  • Wong KY , YuL , ChimCS . DNA methylation of tumor suppressor miRNA genes: a lesson from the miR-34 family . Epigenomics3 ( 1 ), 83 – 92 ( 2011 ).
  • Zhang S , HaoJ , XieFet al. Downregulation of miR-132 by promoter methylation contributes to pancreatic cancer development . Carcinogenesis32 ( 8 ), 1183 – 1189 ( 2011 ).
  • Guo X , XiaJ , YanJ . Promoter methylated microRNAs: potential therapeutic targets in gastric cancer (Review) . Mol. Med. Rep.11 ( 2 ), 759 – 765 ( 2015 ).
  • Manuyakorn A , PaulusR , FarrellJet al. Cellular histone modification patterns predict prognosis and treatment response in resectable pancreatic adenocarcinoma: results from RTOG 9704 . J. Clin. Oncol.28 ( 8 ), 1358 – 1365 ( 2010 ).
  • Zhang W , DahlbergJE , TamW . MicroRNAs in tumorigenesis: a primer . Am. J. Pathol.171 ( 3 ), 728 – 738 ( 2007 ).
  • Venturelli S , BergerA , WeilandTet al. Differential induction of apoptosis and senescence by the DNA methyltransferase inhibitors 5-azacytidine and 5-aza-2′-deoxycytidine in solid tumor cells . Mol. Cancer Ther.12 ( 10 ), 2226 – 2236 ( 2013 ).
  • Azad MB , GibsonSB . Role of BNIP3 in proliferation and hypoxia-induced autophagy: implications for personalized cancer therapies . Ann. New York Acad. Sci.1210 , 8 – 16 ( 2010 ).
  • Okami J , SimeoneDM , LogsdonCD . Silencing of the hypoxia-inducible cell death protein BNIP3 in pancreatic cancer . Cancer Res.64 ( 15 ), 5338 – 5346 ( 2004 ).
  • Abe T , ToyotaM , SuzukiHet al. Upregulation of BNIP3 by 5-aza-2′-deoxycytidine sensitizes pancreatic cancer cells to hypoxia-mediated cell death . J. Gastroenterol.40 ( 5 ), 504 – 510 ( 2005 ).
  • Sato N , FukushimaN , MaeharaNet al. SPARC/osteonectin is a frequent target for aberrant methylation in pancreatic adenocarcinoma and a mediator of tumor-stromal interactions . Oncogene22 ( 32 ), 5021 – 5030 ( 2003 ).
  • Puolakkainen PA , BrekkenRA , MuneerS , SageEH . Enhanced growth of pancreatic tumors in SPARC-null mice is associated with decreased deposition of extracellular matrix and reduced tumor cell apoptosis . Mol. Cancer Res.2 ( 4 ), 215 – 224 ( 2004 ).
  • Mahadevan D , Von HoffDD . Tumor–stroma interactions in pancreatic ductal adenocarcinoma . Mol. Cancer Ther.6 ( 4 ), 1186 – 1197 ( 2007 ).

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