Epigenetic roles of PIWI‑interacting RNAs (piRNAs) in cancer metastasis (Review)
- Authors:
- Jia Liu
- Shujun Zhang
- Binglin Cheng
-
Affiliations: Department of Integrated Traditional Chinese and Western Medicine Oncology, The First Affiliated Hospital of Harbin Medical University, Harbin, Heilongjiang 150000, P.R. China, Department of Pathology, The Fourth Affiliated Hospital of Harbin Medical University, Harbin, Heilongjiang 150000, P.R. China - Published online on: September 6, 2018 https://doi.org/10.3892/or.2018.6684
- Pages: 2423-2434
This article is mentioned in:
Abstract
Li C, Vagin VV, Lee S, Xu J, Ma S, Xi H, Seitz H, Horwich MD, Syrzycka M, Honda BM, et al: Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell. 137:509–521. 2009. View Article : Google Scholar : PubMed/NCBI | |
Shrey K, Suchit A, Nishant M and Vibha R: RNA interference: Emerging diagnostics and therapeutics tool. Biochem Biophys Res Commun. 386:273–277. 2009. View Article : Google Scholar : PubMed/NCBI | |
Collins LJ and Penny D: The RNA infrastructure: Dark matter of the eukaryotic cell? Trends Genet. 25:120–128. 2009. View Article : Google Scholar : PubMed/NCBI | |
Malone CD and Hannon GJ: Small RNAs as guardians of the genome. Cell. 136:656–668. 2009. View Article : Google Scholar : PubMed/NCBI | |
Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, Sachidanandam R and Hannon GJ: Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell. 137:522–535. 2009. View Article : Google Scholar : PubMed/NCBI | |
Freedman JE, Gerstein M, Mick E, Rozowsky J, Levy D, Kitchen R, Das S, Shah R, Danielson K, Beaulieu L, et al: Diverse human extracellular RNAs are widely detected in human plasma. Nat Commun. 7:111062016. View Article : Google Scholar : PubMed/NCBI | |
Iliev R, Stanik M, Fedorko M, Poprach A, Vychytilova-Faltejskova P, Slaba K, Svoboda M, Fabian P, Pacik D, Dolezel J, et al: Decreased expression levels of PIWIL1, PIWIL2, and PIWIL4 are associated with worse survival in renal cell carcinoma patients. OncoTargets Ther. 9:217–222. 2016. | |
Lee JH, Schutte D, Wulf G, Füzesi L, Radzun HJ, Schweyer S, Engel W and Nayernia K: Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum Mol Genet. 15:201–211. 2006. View Article : Google Scholar : PubMed/NCBI | |
Taubert H, Greither T, Kaushal D, Würl P, Bache M, Bartel F, Kehlen A, Lautenschläger C, Harris L, Kraemer K, et al: Expression of the stem cell self-renewal gene Hiwi and risk of tumour-related death in patients with soft-tissue sarcoma. Oncogene. 26:1098–1100. 2007. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Liu Y, Shen X, Zhang X, Chen X, Yang C and Gao H: The PIWI protein acts as a predictive marker for human gastric cancer. Int J Clin Exp Pathol. 5:315–325. 2012.PubMed/NCBI | |
Cheng J, Guo JM, Xiao BX, Miao Y, Jiang Z, Zhou H and Li QN: piRNA, the new non-coding RNA, is aberrantly expressed in human cancer cells. Clin Chim Acta. 412:1621–1625. 2011. View Article : Google Scholar : PubMed/NCBI | |
Huang G, Hu H, Xue X, Shen S, Gao E, Guo G, Shen X and Zhang X: Altered expression of piRNAs and their relation with clinicopathologic features of breast cancer. Clin Transl Oncol. 15:563–568. 2013. View Article : Google Scholar : PubMed/NCBI | |
Law PT, Qin H, Ching AK, Lai KP, Co NN, He M, Lung RW, Chan AW, Chan TF and Wong N: Deep sequencing of small RNA transcriptome reveals novel non-coding RNAs in hepatocellular carcinoma. J Hepatol. 58:1165–1173. 2013. View Article : Google Scholar : PubMed/NCBI | |
Yan H, Wu QL, Sun CY, Ai LS, Deng J, Zhang L, Chen L, Chu ZB, Tang B, Wang K, et al: piRNA-823 contributes to tumorigenesis by regulating de novo DNA methylation and angiogenesis in multiple myeloma. Leukemia. 29:196–206. 2015. View Article : Google Scholar : PubMed/NCBI | |
Luteijn MJ and Ketting RF: PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nat Rev Genet. 14:523–534. 2013. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Wu X, Gao H, Jin JM, Li AX, Kim YS, Pal SK, Nelson RA, Lau CM, Guo C, et al: Piwi-Interacting RNAs (piRNAs) are dysregulated in renal cell carcinoma and associated with tumor metastasis and cancer-specific survival. Mol Med. 21:381–388. 2015. View Article : Google Scholar : PubMed/NCBI | |
Gigek CO, Chen ES, Calcagno DQ, Wisnieski F, Burbano RR and Smith MA: Epigenetic mechanisms in gastric cancer. Epigenomics. 4:279–294. 2012. View Article : Google Scholar : PubMed/NCBI | |
Potter VR: Initiation and promotion in cancer formation: the importance of studies on intercellular communication. Yale J Biol Med. 53:367–384. 1980.PubMed/NCBI | |
Lujambio A, Calin GA, Villanueva A, Ropero S, Sánchez-Céspedes M, Blanco D, Montuenga LM, Rossi S, Nicoloso MS, Faller WJ, et al: A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci USA. 105:13556–13561. 2008. View Article : Google Scholar : PubMed/NCBI | |
Tiwari VK, McGarvey KM, Licchesi JD, Ohm JE, Herman JG, Schübeler D and Baylin SB: PcG proteins, DNA methylation, and gene repression by chromatin looping. PLoS Biol. 6:2911–2927. 2008. View Article : Google Scholar : PubMed/NCBI | |
Nowacka-Zawisza M and Wisnik E: DNA methylation and histone modifications as epigenetic regulation in prostate cancer (Review). Oncol Rep. 38:2587–2596. 2017. View Article : Google Scholar : PubMed/NCBI | |
Weick EM and Miska EA: piRNAs: From biogenesis to function. Development. 141:3458–3471. 2014. View Article : Google Scholar : PubMed/NCBI | |
Han BW and Zamore PD: piRNAs. Curr Biol. 24:R730–R733. 2014. View Article : Google Scholar : PubMed/NCBI | |
Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K and Hannon GJ: Developmentally regulated piRNA clusters implicate MILI in transposon control. Science. 316:744–747. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ross RJ, Weiner MM and Lin H: PIWI proteins and PIWI-interacting RNAs in the soma. Nature. 505:353–359. 2014. View Article : Google Scholar : PubMed/NCBI | |
Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, van den Elst H, Filippov DV, Blaser H, Raz E, Moens CB, et al: A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell. 129:69–82. 2007. View Article : Google Scholar : PubMed/NCBI | |
Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, Bestor T and Hannon GJ: A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 31:785–799. 2008. View Article : Google Scholar : PubMed/NCBI | |
Ghildiyal M and Zamore PD: Small silencing RNAs: an expanding universe. Nat Rev Genet. 10:94–108. 2009. View Article : Google Scholar : PubMed/NCBI | |
Peng JC and Lin H: Beyond transposons: The epigenetic and somatic functions of the Piwi-piRNA mechanism. Curr Opin Cell Biol. 25:190–194. 2013. View Article : Google Scholar : PubMed/NCBI | |
Feschotte C and Pritham EJ: DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet. 41:331–368. 2007. View Article : Google Scholar : PubMed/NCBI | |
Kubo S, Seleme MC, Soifer HS, Perez JL, Moran JV, Kazazian HH Jr and Kasahara N: L1 retrotransposition in nondividing and primary human somatic cells. Proc Natl Acad Sci USA. 103:8036–8041. 2006. View Article : Google Scholar : PubMed/NCBI | |
Pelisson A, Mejlumian L, Robert V, Terzian C and Bucheton A: Drosophila germline invasion by the endogenous retrovirus gypsy: Involvement of the viral env gene. Insect Biochem Mol Biol. 32:1249–1256. 2002. View Article : Google Scholar : PubMed/NCBI | |
Leblanc P, Desset S, Giorgi F, Taddei AR, Fausto AM, Mazzini M, Dastugue B and Vaury C: Life cycle of an endogenous retrovirus, ZAM, in Drosophila melanogaster. J Virol. 74:10658–10669. 2000. View Article : Google Scholar : PubMed/NCBI | |
Brouha B, Schustak J, Badge RM, Lutz-Prigge S, Farley AH, Moran JV and Kazazian HH Jr: Hot L1s account for the bulk of retrotransposition in the human population. Proc Natl Acad Sci USA. 100:5280–5285. 2003. View Article : Google Scholar : PubMed/NCBI | |
Alisch RS, Garcia-Perez JL, Muotri AR, Gage FH and Moran JV: Unconventional translation of mammalian LINE-1 retrotransposons. Genes Dev. 20:210–224. 2006. View Article : Google Scholar : PubMed/NCBI | |
Baer CF, Miyamoto MM and Denver DR: Mutation rate variation in multicellular eukaryotes: causes and consequences. Na Rev Genet. 8:619–631. 2007. View Article : Google Scholar | |
Belinco C, Diprima SN, Wolff RE, Thorp MW, Buschette JT and Simmons MJ: Cytotype regulation in Drosophila melanogaster: synergism between telomeric and non-telomeric P elements. Genet Res. 91:383–394. 2009. View Article : Google Scholar | |
Simmons MJ, Peterson MP, Thorp MW, Buschette JT, DiPrima SN, Harter CL and Skolnick MJ: piRNA-mediated transposon regulation and the germ-line mutation rate in Drosophila melanogaster males. Mutat Res. 773:16–21. 2015. View Article : Google Scholar : PubMed/NCBI | |
Pezic D, Manakov SA, Sachidanandam R and Aravin AA: piRNA pathway targets active LINE1 elements to establish the repressive H3K9me3 mark in germ cells. Genes Dev. 28:1410–1428. 2014. View Article : Google Scholar : PubMed/NCBI | |
Czech B, Preall JB, McGinn J and Hannon GJ: A transcriptome-wide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway. Mol Cell. 50:749–761. 2013. View Article : Google Scholar : PubMed/NCBI | |
Handler D, Meixner K, Pizka M, Lauss K, Schmied C, Gruber FS and Brennecke J: The genetic makeup of the Drosophila piRNA pathway. Mol Cell. 50:762–777. 2013. View Article : Google Scholar : PubMed/NCBI | |
Muerdter F, Guzzardo PM, Gillis J, Luo Y, Yu Y, Chen C, Fekete R and Hannon GJ: A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol Cell. 50:736–748. 2013. View Article : Google Scholar : PubMed/NCBI | |
Sarot E, Payen-Groschene G, Bucheton A and Pelisson A: Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene. Genetics. 166:1313–1321. 2004. View Article : Google Scholar : PubMed/NCBI | |
Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, Perkins EM, Hur JK, Aravin AA and Tóth KF: Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev. 27:390–399. 2013. View Article : Google Scholar : PubMed/NCBI | |
Sienski G, Batki J, Senti KA, Dönertas D, Tirian L, Meixner K and Brennecke J: Silencio/CG9754 connects the Piwi-piRNA complex to the cellular heterochromatin machinery. Genes Dev. 29:2258–2271. 2015. View Article : Google Scholar : PubMed/NCBI | |
Sienski G, Donertas D and Brennecke J: Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell. 151:964–980. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H and Siomi MC: A slicer-mediated mechanism for repeat-associated siRNA 5′end formation in Drosophila. Science. 315:1587–1590. 2007. View Article : Google Scholar : PubMed/NCBI | |
Niki Y, Yamaguchi T and Mahowald AP: Establishment of stable cell lines of Drosophila germ-line stem cells. Proc Natl Acad Sci USA. 103:16325–16330. 2006. View Article : Google Scholar : PubMed/NCBI | |
Saito K, Ishizu H, Komai M, Kotani H, Kawamura Y, Nishida KM, Siomi H and Siomi MC: Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev. 24:2493–2498. 2010. View Article : Google Scholar : PubMed/NCBI | |
Ayyanathan K, Lechner MS, Bell P, Maul GG, Schultz DC, Yamada Y, Tanaka K, Torigoe K and Rauscher FJ III: Regulated recruitment of HP1 to a euchromatic gene induces mitotically heritable, epigenetic gene silencing: A mammalian cell culture model of gene variegation. Genes Dev. 17:1855–1869. 2003. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Danzer JR, Alvarez P, Belmont AS and Wallrath LL: Effects of tethering HP1 to euchromatic regions of the Drosophila genome. Development. 130:1817–1824. 2003. View Article : Google Scholar : PubMed/NCBI | |
Rangan P, Malone CD, Navarro C, Newbold SP, Hayes PS, Sachidanandam R, Hannon GJ and Lehmann R: piRNA production requires heterochromatin formation in Drosophila. Curr Biol. 21:1373–1379. 2011. View Article : Google Scholar : PubMed/NCBI | |
Yang Z, Chen KM, Pandey RR, Homolka D, Reuter M, Janeiro BK, Sachidanandam R, Fauvarque MO, McCarthy AA and Pillai RS: PIWI slicing and EXD1 drive biogenesis of nuclear piRNAs from cytosolic targets of the mouse piRNA pathway. Mol Cell. 61:138–152. 2016. View Article : Google Scholar : PubMed/NCBI | |
He W, Wang Z, Wang Q, Fan Q, Shou C, Wang J, Giercksky KE, Nesland JM and Suo Z: Expression of HIWI in human esophageal squamous cell carcinoma is significantly associated with poorer prognosis. BMC Cancer. 9:4262009. View Article : Google Scholar : PubMed/NCBI | |
He G, Chen L, Ye Y, Xiao Y, Hua K, Jarjoura D, Nakano T, Barsky SH, Shen R and Gao JX: Piwil2 expressed in various stages of cervical neoplasia is a potential complementary marker for p16INK4a. Am J Transl Res. 2:156–169. 2010.PubMed/NCBI | |
Rajasethupathy P, Antonov I, Sheridan R, Frey S, Sander C, Tuschl T and Kandel ER: A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell. 149:693–707. 2012. View Article : Google Scholar : PubMed/NCBI | |
Cui L, Lou Y, Zhang X, Zhou H, Deng H, Song H, Yu X, Xiao B, Wang W and Guo J: Detection of circulating tumor cells in peripheral blood from patients with gastric cancer using piRNAs as markers. Clin Biochem. 44:1050–1057. 2011. View Article : Google Scholar : PubMed/NCBI | |
Cheng J, Deng H, Xiao B, Zhou H, Zhou F, Shen Z and Guo J: piR-823, a novel non-coding small RNA, demonstrates in vitro and in vivo tumor suppressive activity in human gastric cancer cells. Cancer Lett. 315:12–17. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gupta K, Miller JD, Li JZ, Russell MW and Charbonneau C: Epidemiologic and socioeconomic burden of metastatic renal cell carcinoma (mRCC): A literature review. Cancer Treat Rev. 34:193–205. 2008. View Article : Google Scholar : PubMed/NCBI | |
Siomi MC, Sato K, Pezic D and Aravin AA: PIWI-interacting small RNAs: The vanguard of genome defence. Nat Rev Mol Cell Biol. 12:246–258. 2011. View Article : Google Scholar : PubMed/NCBI | |
Li D, Luo Y, Gao Y and Yang Y, Wang Y, Xu Y, Tan S, Zhang Y, Duan J and Yang Y: piR-651 promotes tumor formation in non-small cell lung carcinoma through the upregulation of cyclin D1 and CDK4. Int J Mol Med. 38:927–936. 2016. View Article : Google Scholar : PubMed/NCBI | |
Weng W, Liu N, Toiyama Y, Kusunoki M, Nagasaka T, Fujiwara T, Wei Q, Qin H, Lin H, Ma Y and Goel A: Novel evidence for a PIWI-interacting RNA (piRNA) as an oncogenic mediator of disease progression, and a potential prognostic biomarker in colorectal cancer. Mol Cancer. 17:162018. View Article : Google Scholar : PubMed/NCBI | |
Wu X, Weng L, Li X, Guo C, Pal SK, Jin JM, Li Y, Nelson RA, Mu B, Onami SH, et al: Identification of a 4-microRNA signature for clear cell renal cell carcinoma metastasis and prognosis. PLoS One. 7:e356612012. View Article : Google Scholar : PubMed/NCBI | |
Zeng Y, Qu LK, Meng L, Liu CY, Dong B, Xing XF, Wu J and Shou CC: HIWI expression profile in cancer cells and its prognostic value for patients with colorectal cancer. Chin Med J. 124:2144–2149. 2011.PubMed/NCBI | |
Liu JJ, Shen R, Chen L, Ye Y, He G, Hua K, Jarjoura D, Nakano T, Ramesh GK, Shapiro CL, et al: Piwil2 is expressed in various stages of breast cancers and has the potential to be used as a novel biomarker. Int J Clin Exp Pathol. 3:328–337. 2010.PubMed/NCBI | |
Grochola LF, Greither T, Taubert H, Möller P, Knippschild U, Udelnow A, Henne-Bruns D and Würl P: The stem cell-associated Hiwi gene in human adenocarcinoma of the pancreas: expression and risk of tumour-related death. Br J Cancer. 99:1083–1088. 2008. View Article : Google Scholar : PubMed/NCBI | |
Mei Y, Clark D and Mao L: Novel dimensions of piRNAs in cancer. Cancer Lett. 336:46–52. 2013. View Article : Google Scholar : PubMed/NCBI | |
Tan Y, Liu L, Liao M, Zhang C, Hu S, Zou M, Gu M and Li X: Emerging roles for PIWI proteins in cancer. Acta Biochim Biophys Sin. 47:315–324. 2015. View Article : Google Scholar : PubMed/NCBI | |
Litwin M, Szczepanska-Buda A, Piotrowska A, Dziegiel P and Witkiewicz W: The meaning of PIWI proteins in cancer development. Oncol Lett. 13:3354–3362. 2017. View Article : Google Scholar : PubMed/NCBI | |
Tamura S, Isobe T, Ariyama H, Nakano M, Kikushige Y, Takaishi S, Kusaba H, Takenaka K, Ueki T, Nakamura M, et al: Ecadherin regulates proliferation of colorectal cancer stem cells through NANOG. Oncol Rep. 40:693–703. 2018.PubMed/NCBI | |
Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L and Hannon GJ: Argonaute2 is the catalytic engine of mammalian RNAi. Science. 305:1437–1441. 2004. View Article : Google Scholar : PubMed/NCBI | |
Yin H and Lin H: An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature. 450:304–308. 2007. View Article : Google Scholar : PubMed/NCBI | |
Chen Y, Hu W, Lu Y, Jiang S, Li C, Chen J, Tao D, Liu Y, Yang Y and Ma Y: A TALEN-based specific transcript knock-down of PIWIL2 suppresses cell growth in HepG2 tumor cell. Cell Pprolif. 47:448–456. 2014. View Article : Google Scholar | |
Lee JH, Jung C, Javadian-Elyaderani P, Schweyer S, Schütte D, Shoukier M, Karimi-Busheri F, Weinfeld M, Rasouli-Nia A, Hengstler JG, et al: Pathways of proliferation and antiapoptosis driven in breast cancer stem cells by stem cell protein piwil2. Cancer Res. 70:4569–4579. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zhang H, Ren Y, Xu H, Pang D, Duan C and Liu C: The expression of stem cell protein Piwil2 and piR-932 in breast cancer. Surg Oncol. 22:217–223. 2013. View Article : Google Scholar : PubMed/NCBI | |
Lee E, Iskow R, Yang L, Gokcumen O, Haseley P, Luquette LJ III, Lohr JG, Harris CC, Ding L, Wilson RK, et al: Landscape of somatic retrotransposition in human cancers. Science. 337:967–971. 2012. View Article : Google Scholar : PubMed/NCBI | |
Andreotti G, Karami S, Pfeiffer RM, Hurwitz L, Liao LM, Weinstein SJ, Albanes D, Virtamo J, Silverman DT, Rothman N and Moore LE: LINE1 methylation levels associated with increased bladder cancer risk in pre-diagnostic blood DNA among US (PLCO) and European (ATBC) cohort study participants. Epigenetics. 9:404–415. 2014. View Article : Google Scholar : PubMed/NCBI | |
Daskalos A, Nikolaidis G, Xinarianos G, Savvari P, Cassidy A, Zakopoulou R, Kotsinas A, Gorgoulis V, Field JK and Liloglou T: Hypomethylation of retrotransposable elements correlates with genomic instability in non-small cell lung cancer. Int J Cancer. 124:81–87. 2009. View Article : Google Scholar : PubMed/NCBI | |
Wang X, Jiang C, Fu B, Zhu R, Diao F, Xu N, Chen Z, Tao W and Li CJ: MILI, a PIWI family protein, inhibits melanoma cell migration through methylation of LINE1. Biochem Biophys Res Commun. 457:514–519. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ye Y, Yin DT, Chen L, Zhou Q, Shen R, He G, Yan Q, Tong Z, Issekutz AC, Shapiro CL, et al: Identification of Piwil2-like (PL2L) proteins that promote tumorigenesis. PLoS One. 5:e134062010. View Article : Google Scholar : PubMed/NCBI | |
Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, Asada N, Kojima K, Yamaguchi Y, Ijiri TW, et al: DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 22:908–917. 2008. View Article : Google Scholar : PubMed/NCBI | |
Lu Y, Li C, Zhang K, Sun H, Tao D, Liu Y, Zhang S and Ma Y: Identification of piRNAs in Hela cells by massive parallel sequencing. BMB Rep. 43:635–641. 2010. View Article : Google Scholar : PubMed/NCBI | |
Virani S, Colacino JA, Kim JH and Rozek LS: Cancer epigenetics: A brief review. ILAR J. 53:359–369. 2012. View Article : Google Scholar : PubMed/NCBI | |
Chik F, Szyf M and Rabbani SA: Role of epigenetics in cancer initiation and progression. Adv Exp Med Biol. 720:91–104. 2011. View Article : Google Scholar : PubMed/NCBI | |
Cavalli LR, Urban CA, Dai D, de Assis S, Tavares DC, Rone JD, Bleggi-Torres LF, Lima RS, Cavalli IJ, Issa JP, et al: Genetic and epigenetic alterations in sentinel lymph nodes metastatic lesions compared to their corresponding primary breast tumors. Cancer Genet Cytogenet. 146:33–40. 2003. View Article : Google Scholar : PubMed/NCBI | |
Hanahan D and Weinberg RA: Hallmarks of cancer: The next generation. Cell. 144:646–674. 2011. View Article : Google Scholar : PubMed/NCBI | |
Calin GA and Croce CM: MicroRNA signatures in human cancers. Nat Rev Cancer. 6:857–866. 2006. View Article : Google Scholar : PubMed/NCBI | |
Esteller M: Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet. 8:286–298. 2007. View Article : Google Scholar : PubMed/NCBI | |
Hinoue T, Weisenberger DJ, Lange CP, Shen H, Byun HM, Van Den Berg D, Malik S, Pan F, Noushmehr H, van Dijk CM, et al: Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res. 22:271–282. 2012. View Article : Google Scholar : PubMed/NCBI | |
Azad N, Zahnow CA, Rudin CM and Baylin SB: The future of epigenetic therapy in solid tumours-lessons from the past. Nat Rev Clin Oncol. 10:256–266. 2013. View Article : Google Scholar : PubMed/NCBI | |
Jones PA and Taylor SM: Cellular differentiation, cytidine analogs and DNA methylation. Cell. 20:85–93. 1980. View Article : Google Scholar : PubMed/NCBI | |
Merry CR, Forrest ME, Sabers JN, Beard L, Gao XH, Hatzoglou M, Jackson MW, Wang Z, Markowitz SD and Khalil AM: DNMT1-associated long non-coding RNAs regulate global gene expression and DNA methylation in colon cancer. Hum Mol Genet. 24:6240–6253. 2015. View Article : Google Scholar : PubMed/NCBI | |
Liu T, Wu X, Chen T, Luo Z and Hu X: Downregulation of DNMT3A by miR-708-5p inhibits lung cancer stem cell-like phenotypes through repressing Wnt/β-catenin signaling. Clin Cancer Res. 24:1748–1760. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wang LH, Huang J, Wu CR, Huang LY, Cui J, Xing ZZ and Zhao CY: Downregulation of miR29b targets DNMT3b to suppress cellular apoptosis and enhance proliferation in pancreatic cancer. Mol Med Rep. 17:2113–2120. 2018.PubMed/NCBI | |
Yang L, Hou J, Cui XH, Suo LN and Lv YW: RG108 induces the apoptosis of endometrial cancer Ishikawa cell lines by inhibiting the expression of DNMT3B and demethylation of HMLH1. Eur Rev Med Pharmacol Sci. 21:5056–5064. 2017.PubMed/NCBI | |
Heo J, Lim J, Lee S, Jeong J, Kang H, Kim Y, Kang JW, Yu HY, Jeong EM, Kim K, et al: Sirt1 regulates DNA methylation and differentiation potential of embryonic stem cells by antagonizing Dnmt3l. Cell Rep. 18:1930–1945. 2017. View Article : Google Scholar : PubMed/NCBI | |
Guo Y, Wang M, Jia X, Zhu H, Zhi Y and Yuan L: Wnt signaling pathway upregulates DNMT1 to trigger NHERF1 promoter hypermethylation in colon cancer. Oncol Rep. 40:1165–1173. 2018.PubMed/NCBI | |
Zochbauer-Muller S, Gazdar AF and Minna JD: Molecular pathogenesis of lung cancer. Ann Rev Physiol. 64:681–708. 2002. View Article : Google Scholar | |
Nakajima NI, Niimi A, Isono M, Oike T, Sato H, Nakano T and Shibata A: Inhibition of the HDAC/Suv39/G9a pathway restores the expression of DNA damage-dependent major histocompatibility complex class I-related chain A and B in cancer cells. Oncol Rep. 38:693–702. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ferreira HJ, Heyn H, del Muro Garcia X, Vidal A, Larriba S, Muñoz C, Villanueva A and Esteller M: Epigenetic loss of the PIWI/piRNA machinery in human testicular tumorigenesis. Epigenetics. 9:113–118. 2014. View Article : Google Scholar : PubMed/NCBI | |
Sciamanna I, Vitullo P, Curatolo A and Spadafora C: A reverse transcriptase-dependent mechanism is essential for murine preimplantation development. Genes. 2:360–373. 2011. View Article : Google Scholar : PubMed/NCBI | |
Akers SN, Moysich K, Zhang W, Lai Collamat G, Miller A, Lele S, Odunsi K and Karpf AR: LINE1 and Alu repetitive element DNA methylation in tumors and white blood cells from epithelial ovarian cancer patients. Gynecol Oncol. 132:462–467. 2014. View Article : Google Scholar : PubMed/NCBI | |
Slotkin RK and Martienssen R: Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 8:272–285. 2007. View Article : Google Scholar : PubMed/NCBI | |
Shilatifard A: Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem. 75:243–269. 2006. View Article : Google Scholar : PubMed/NCBI | |
Grewal SI and Jia S: Heterochromatin revisited. Nat Rev Genet. 8:35–46. 2007. View Article : Google Scholar : PubMed/NCBI | |
Heard E: Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome. Curr Opin Genet Dev. 15:482–489. 2005. View Article : Google Scholar : PubMed/NCBI | |
Corcoran AE: Immunoglobulin locus silencing and allelic exclusion. Semin Immunol. 17:141–154. 2005. View Article : Google Scholar : PubMed/NCBI | |
Skok JA, Gisler R, Novatchkova M, Farmer D, de Laat W and Busslinger M: Reversible contraction by looping of the Tcra and Tcrb loci in rearranging thymocytes. Nat Immunol. 8:378–387. 2007. View Article : Google Scholar : PubMed/NCBI | |
Klose RJ and Zhang Y: Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol. 8:307–318. 2007. View Article : Google Scholar : PubMed/NCBI | |
Feldman N, Gerson A, Fang J, Li E, Zhang Y, Shinkai Y, Cedar H and Bergman Y: G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nat Cell Biol. 8:188–194. 2006. View Article : Google Scholar : PubMed/NCBI | |
Lee E, Wang J, Jung Y, Cackowski FC and Taichman RS: Reduction of two histone marks, H3k9me3 and H3k27me3 by epidrug induces neuroendocrine differentiation in prostate cancer. J Cell Biochem. 119:3697–3705. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ooi L and Wood IC: Chromatin crosstalk in development and disease: lessons from REST. Nat Rev Genet. 8:544–554. 2007. View Article : Google Scholar : PubMed/NCBI | |
Shi Y: Histone lysine demethylases: emerging roles in development, physiology and disease. Nat Rev Genet. 8:829–833. 2007. View Article : Google Scholar : PubMed/NCBI | |
Yang M, Gocke CB, Luo X, Borek D, Tomchick DR, Machius M, Otwinowski Z and Yu H: Structural basis for CoREST-dependent demethylation of nucleosomes by the human LSD1 histone demethylase. Mol Cell. 23:377–387. 2006. View Article : Google Scholar : PubMed/NCBI | |
Grewal SI and Elgin SC: Transcription and RNA interference in the formation of heterochromatin. Nature. 447:399–406. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lee J, Ko J and Yi JY: Histone deacetylase inhibitor (HDACi) upregulates activin A and activates the Smad signaling pathway in melanomas. J Dermatol Sci. 90:13–20. 2017. View Article : Google Scholar : PubMed/NCBI | |
Terranova-Barberio M, Thomas S and Munster PN: Host histone acetylation unlocks HDAC inhibitor potential. Oncotarget. 8:106161–106162. 2017. View Article : Google Scholar : PubMed/NCBI | |
Liu C, Liu L, Chen X, Cheng J, Zhang H, Zhang C, Shan J, Shen J and Qian C: LSD1 stimulates cancer-associated fibroblasts to drive Notch3-dependent self-renewal of liver cancer stem-like cells. Cancer Res. 78:938–949. 2018. View Article : Google Scholar : PubMed/NCBI | |
Fei W, Chen L, Chen J, Shi Q, Zhang L, Liu S, Li L, Zheng L and Hu X: RBP4 and THBS2 are serum biomarkers for diagnosis of colorectal cancer. Oncotarget. 8:92254–92264. 2017. View Article : Google Scholar : PubMed/NCBI | |
Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA and Shi Y: Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell. 119:941–953. 2004. View Article : Google Scholar : PubMed/NCBI | |
Smith CD, Shu S, Mungall CJ and Karpen GH: The Release 5.1 annotation of Drosophila melanogaster heterochromatin. Science. 316:1586–1591. 2007. View Article : Google Scholar : PubMed/NCBI | |
Smallwood A, Esteve PO, Pradhan S and Carey M: Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes Dev. 21:1169–1178. 2007. View Article : Google Scholar : PubMed/NCBI | |
Peters AH, O'Carroll D, Scherthan H, Mechtler K, Sauer S, Schöfer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, et al: Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell. 107:323–337. 2001. View Article : Google Scholar : PubMed/NCBI | |
Yoon KA, Hwangbo B, Kim IJ, Park S, Kim HS, Kee HJ, Lee JE, Jang YK, Park JG and Lee JS: Novel polymorphisms in the SUV39H2 histone methyltransferase and the risk of lung cancer. Carcinogenesis. 27:2217–2222. 2006. View Article : Google Scholar : PubMed/NCBI | |
Zhao Z, Hu Y, Shen X, Lao Y, Zhang L, Qiu X, Hu J, Gong P, Cui H, Lu S, et al: HBx represses RIZ1 expression by DNA methyltransferase 1 involvement in decreased miR-152 in hepatocellular carcinoma. Oncol Rep. 37:2811–2818. 2017. View Article : Google Scholar : PubMed/NCBI | |
Gibbons RJ: Histone modifying and chromatin remodelling enzymes in cancer and dysplastic syndromes. Hum Mol Genet. 14:R85–R92. 2005. View Article : Google Scholar : PubMed/NCBI | |
Lakshmikuttyamma A, Takahashi N, Pastural E, Torlakovic E, Amin HM, Garcia-Manero G, Voralia M, Czader M, DeCoteau JF and Geyer CR: RIZ1 is potential CML tumor suppressor that is down-regulated during disease progression. J Hematol Oncol. 2:282009. View Article : Google Scholar : PubMed/NCBI | |
Espino PS, Drobic B, Dunn KL and Davie JR: Histone modifications as a platform for cancer therapy. J Cell Biochem. 94:1088–1102. 2005. View Article : Google Scholar : PubMed/NCBI | |
Hamamoto R, Furukawa Y, Morita M, Iimura Y, Silva FP, Li M, Yagyu R and Nakamura Y: SMYD3 encodes a histone methyltransferase involved in the proliferation of cancer cells. Nat Cell Biol. 6:731–740. 2004. View Article : Google Scholar : PubMed/NCBI | |
Li W, Zhang X, Lu X, You L, Song Y, Luo Z, Zhang J, Nie J, Zheng W, Xu D, et al: 5-Hydroxymethylcytosine signatures in circulating cell-free DNA as diagnostic biomarkers for human cancers. Cell Res. 27:1243–1257. 2017. View Article : Google Scholar : PubMed/NCBI | |
Pulukuri SM, Estes N, Patel J and Rao JS: Demethylation-linked activation of urokinase plasminogen activator is involved in progression of prostate cancer. Cancer Res. 67:930–939. 2007. View Article : Google Scholar : PubMed/NCBI | |
Stepanova V, Dergilev KV, Holman KR, Parfyonova YV, Tsokolaeva ZI, Teter M, Atochina-Vasserman EN, Volgina A, Zaitsev SV, Lewis SP, et al: Urokinase-type plasminogen activator (uPA) is critical for progression of tuberous sclerosis complex 2 (TSC2)-deficient tumors. J Biol Chem. 292:20528–20543. 2017. View Article : Google Scholar : PubMed/NCBI | |
Foekens JA, Peters HA, Look MP, Portengen H, Schmitt M, Kramer MD, Brünner N, Jänicke F, Meijer-van Gelder ME, Henzen-Logmans SC, et al: The urokinase system of plasminogen activation and prognosis in 2780 breast cancer patients. Cancer Res. 60:636–643. 2000.PubMed/NCBI | |
Miyake H, Hara I, Yamanaka K, Gohji K, Arakawa S and Kamidono S: Elevation of serum levels of urokinase-type plasminogen activator and its receptor is associated with disease progression and prognosis in patients with prostate cancer. Prostate. 39:123–129. 1999. View Article : Google Scholar : PubMed/NCBI | |
Zhang Z, Wang J, Wang X, Song W, Shi Y and Zhang L: MicroRNA-21 promotes proliferation, migration, and invasion of cervical cancer through targeting TIMP3. Arch Gynecol Obstet. 297:433–442. 2018. View Article : Google Scholar : PubMed/NCBI | |
Qi JH, Ebrahem Q, Moore N, Murphy G, Claesson-Welsh L, Bond M, Baker A and Anand-Apte B: A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat Med. 9:407–415. 2003. View Article : Google Scholar : PubMed/NCBI | |
Cui H, Hu Y, Guo D, Zhang A, Gu Y, Zhang S, Zhao C, Gong P, Shen X, Li Y, et al: DNA methyltransferase 3A isoform b contributes to repressing E-cadherin through cooperation of DNA methylation and H3K27/H3K9 methylation in EMT-related metastasis of gastric cancer. Oncogene. 37:4358–4371. 2018. View Article : Google Scholar : PubMed/NCBI | |
Filbin MG, Tirosh I, Hovestadt V, Shaw ML, Escalante LE, Mathewson ND, Neftel C, Frank N, Pelton K, Hebert CM, et al: Developmental and oncogenic programs in H3K27M gliomas dissected by single-cell RNA-seq. Science. 360:331–335. 2018. View Article : Google Scholar : PubMed/NCBI | |
Gregory PA, Bracken CP, Bert AG and Goodall GJ: MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle. 7:3112–3118. 2008. View Article : Google Scholar : PubMed/NCBI | |
Suarez Y and Sessa WC: MicroRNAs as novel regulators of angiogenesis. Circ Res. 104:442–454. 2009. View Article : Google Scholar : PubMed/NCBI | |
Liang Z, Wu H, Reddy S, Zhu A, Wang S, Blevins D, Yoon Y, Zhang Y and Shim H: Blockade of invasion and metastasis of breast cancer cells via targeting CXCR4 with an artificial microRNA. Biochem Biophys Res Commun. 363:542–546. 2007. View Article : Google Scholar : PubMed/NCBI | |
Henderson IR and Jacobsen SE: Epigenetic inheritance in plants. Nature. 447:418–424. 2007. View Article : Google Scholar : PubMed/NCBI | |
Wassenegger M, Heimes S, Riedel L and Sanger HL: RNA-directed de novo methylation of genomic sequences in plants. Cell. 76:567–576. 1994. View Article : Google Scholar : PubMed/NCBI | |
Seitz H, Youngson N, Lin SP, Dalbert S, Paulsen M, Bachellerie JP, Ferguson-Smith AC and Cavaillé J: Imprinted microRNA genes transcribed antisense to a reciprocally imprinted retrotransposon-like gene. Nat Genet. 34:261–262. 2003. View Article : Google Scholar : PubMed/NCBI | |
Lin SP, Coan P, da Rocha ST, Seitz H, Cavaille J, Teng PW, Takada S and Ferguson-Smith AC: Differential regulation of imprinting in the murine embryo and placenta by the Dlk1-Dio3 imprinting control region. Development. 134:417–426. 2007. View Article : Google Scholar : PubMed/NCBI | |
Sinkkonen L, Hugenschmidt T, Berninger P, Gaidatzis D, Mohn F, Artus-Revel CG, Zavolan M, Svoboda P and Filipowicz W: MicroRNAs control de novo DNA methylation through regulation of transcriptional repressors in mouse embryonic stem cells. Nat Struct Mol Biol. 15:259–267. 2008. View Article : Google Scholar : PubMed/NCBI | |
Benetti R, Gonzalo S, Jaco I, Muñoz P, Gonzalez S, Schoeftner S, Murchison E, Andl T, Chen T and Klatt P: A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nat Struct Mol Biol. 15:268–279. 2008. View Article : Google Scholar : PubMed/NCBI |