Tissue and cancer-specific expression of DIEXF is epigenetically mediated by an Alu repeat

References

• International Human Genome Sequencing Consortium. Initial sequencing and analysis of the human genome. Nature. 2001:409(6822):860–921.
   PubMed Web of Science ®Google Scholar
• Wicker T, Sabot F, Hua-Van A, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8(12):973–982.
   PubMed Web of Science ®Google Scholar
• Elbarbary RA, Lucas BA, Maquat LE. Retrotransposons as regulators of gene expression. Science. 2016;351(6274):aac7247.
   PubMed Web of Science ®Google Scholar
• Goke J, Ng HH. CTRL+INSERT: retrotransposons and their contribution to regulation and innovation of the transcriptome. EMBO Rep. 2016;17(8):1131–1144.
   PubMed Web of Science ®Google Scholar
• Chen LL, Yang L. ALUternative regulation for gene expression. Trends Cell Biol. 2017;27(7):480–490.
   PubMed Web of Science ®Google Scholar
• Tomilin NV. Regulation of mammalian gene expression by retroelements and non-coding tandem repeats. Bioessays. 2008;30(4):338–348.
   PubMed Web of Science ®Google Scholar
• Deininger P. Alu elements: know the SINEs. Genome Biol. 2011;12(12):236.
   PubMed Web of Science ®Google Scholar
• Polak P, Domany E. Alu elements contain many binding sites for transcription factors and may play a role in regulation of developmental processes. BMC Genomics. 2006;7:133.
   PubMed Web of Science ®Google Scholar
• Su M, Han D, Boyd-Kirkup J, et al. Evolution of Alu elements toward enhancers. Cell Rep. 2014;7(2):376–385.
   PubMed Web of Science ®Google Scholar
• Tanaka Y, Yamashita R, Suzuki Y, et al. Effects of Alu elements on global nucleosome positioning in the human genome. BMC Genomics. 2010;11:309.
   PubMed Web of Science ®Google Scholar
• Collings CK, Anderson JN. Links between DNA methylation and nucleosome occupancy in the human genome. Epigenetics Chromatin. 2017;10:18.
   PubMed Web of Science ®Google Scholar
• Jorda M, Diez-Villanueva A, Mallona I, et al. The epigenetic landscape of Alu repeats delineates the structural and functional genomic architecture of colon cancer cells. Genome Res. 2017;27(1):118–132.
   PubMed Web of Science ®Google Scholar
• Lister R, Pelizzola M, Dowen RH, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 2009;462(7271):315–322.
   PubMed Web of Science ®Google Scholar
• Xie H, Wang M, Bonaldo Mde F, et al. High-throughput sequence-based epigenomic analysis of Alu repeats in human cerebellum. Nucleic Acids Res. 2009;37(13):4331–4340.
   PubMed Web of Science ®Google Scholar
• Kondo Y, Issa JP. Enrichment for histone H3 lysine 9 methylation at Alu repeats in human cells. J Biol Chem. 2003;278(30):27658–27662.
   PubMed Web of Science ®Google Scholar
• Feinberg AP, Tycko B. The history of cancer epigenetics. Nat Rev Cancer. 2004;4(2):143–153.
   PubMed Web of Science ®Google Scholar
• Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol. 2010;28(10):1057–1068.
   PubMed Web of Science ®Google Scholar
• Ehrlich M. DNA hypomethylation in cancer cells. Epigenomics. 2009;1(2):239–259.
   PubMed Web of Science ®Google Scholar
• Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet. 2007;8(4):286–298.
   PubMed Web of Science ®Google Scholar
• Gaudet F, Graeme JG, Eden A, et al. Induction of tumors in mice by genomic hypomethylation. Science. 2003;300(5618):489–492.
   PubMed Web of Science ®Google Scholar
• Eden A, Gaudet F, Waghmare A, et al. Chromosomal instability and tumors promoted by DNA hypomethylation. Science. 2003;300(5618):455.
   PubMed Web of Science ®Google Scholar
• Karpf AR, Matsui S. Genetic disruption of cytosine DNA methyltransferase enzymes induces chromosomal instability in human cancer cells. Cancer Res. 2005;65(19):8635–8639.
   PubMed Web of Science ®Google Scholar
• Daskalos A, Nikolaidis G, Xinarianos G, et al. Hypomethylation of retrotransposable elements correlates with genomic instability in non-small cell lung cancer. Int J Cancer. 2009;124(1):81–87.
   PubMed Web of Science ®Google Scholar
• Rodriguez J, Frigola J, Vendrell E, et al. Chromosomal instability correlates with genome-wide DNA demethylation in human primary colorectal cancers. Cancer Res. 2006;66(17):8462–9468.
   PubMed Web of Science ®Google Scholar
• Rodriguez J, Vives L, Jorda M, et al. Genome-wide tracking of unmethylated DNA Alu repeats in normal and cancer cells. Nucleic Acids Res. 2008;36(3):770–784.
   PubMed Web of Science ®Google Scholar
• Charette JM, Baserga SJ. The DEAD-box RNA helicase-like Utp25 is an SSU processome component. RNA. 2010;16(11):2156–2169.
   PubMed Web of Science ®Google Scholar
• Goldfeder MB, Oliveira CC. Utp25p, a nucleolar Saccharomyces cerevisiae protein, interacts with U3 snoRNP subunits and affects processing of the 35S pre-rRNA. Febs J. 2010;277(13):2838–2852.
   PubMed Web of Science ®Google Scholar
• Chen J, Ruan H, Ng SM, et al. Loss of function of def selectively up-regulates Delta113p53 expression to arrest expansion growth of digestive organs in zebrafish. Genes Dev. 2005;19(23):2900–2911.
   PubMed Web of Science ®Google Scholar
• Aryal NK, Wasylishen AR, Pant V, et al. Loss of digestive organ expansion factor (Diexf) reveals an essential role during murine embryonic development that is independent of p53. Oncotarget. 2017;8(61):103996–104006.
   PubMedGoogle Scholar
• Tao T, Shi H, Guan Y, et al. Def defines a conserved nucleolar pathway that leads p53 to proteasome-independent degradation. Cell Res. 2013;23(5):620–634.
   PubMed Web of Science ®Google Scholar
• Guan Y, Huang D, Chen F, et al. Phosphorylation of def regulates nucleolar p53 turnover and cell cycle progression through def recruitment of calpain3. PLoS Biol. 2016;14(9):e1002555.
   PubMed Web of Science ®Google Scholar
• Zhu Z, Chen J, Xiong JW, et al. Haploinsufficiency of def activates p53-dependent TGFbeta signalling and causes scar formation after partial hepatectomy. PLoS One. 2014;9(5):e96576.
   PubMed Web of Science ®Google Scholar
• Tao T, Sondalle SB, Shi H, et al. The pre-rRNA processing factor DEF is rate limiting for the pathogenesis of MYCN-driven neuroblastoma. Oncogene. 2017;36(27):3852–3867.
   PubMed Web of Science ®Google Scholar
• Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet. 2003;33(Suppl):245–254.
   PubMed Web of Science ®Google Scholar
• Tuesta LM, Zhang Y. Mechanisms of epigenetic memory and addiction. Embo J. 2014;33(10):1091–1103.
   PubMed Web of Science ®Google Scholar
• Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012;13(7):484–492.
   PubMed Web of Science ®Google Scholar
• Ndlovu MN, Denis H, Fuks F. Exposing the DNA methylome iceberg. Trends Biochem Sci. 2011;36(7):381–387.
   PubMed Web of Science ®Google Scholar
• Yang AS, Estecio MR, Doshi K, et al. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res. 2004;32(3):e38.
   PubMed Web of Science ®Google Scholar
• Weisenberger DJ, Campan M, Long TI, et al. Analysis of repetitive element DNA methylation by MethyLight. Nucleic Acids Res. 2005;33(21):6823–6836.
   PubMed Web of Science ®Google Scholar
• Wu HC, Delgado-Cruzata L, Flom JD, et al. Global methylation profiles in DNA from different blood cell types. Epigenetics. 2011;6(1):76–85.
   PubMed Web of Science ®Google Scholar
• Yoshida T, Yamashita S, Takamura-Enya T, et al. Alu and Satalpha hypomethylation in Helicobacter pylori-infected gastric mucosae. Int J Cancer. 2011;128(1):33–39.
   PubMed Web of Science ®Google Scholar
• Choi IS, Estecio MR, Nagano Y, et al. Hypomethylation of LINE-1 and Alu in well-differentiated neuroendocrine tumors (pancreatic endocrine tumors and carcinoid tumors). Mod Pathol. 2007;20(7):802–810.
   PubMed Web of Science ®Google Scholar
• Jintaridth P, Mutirangura A. Distinctive patterns of age-dependent hypomethylation in interspersed repetitive sequences. Physiol Genomics. 2010;41(2):194–200.
   PubMed Web of Science ®Google Scholar
• Klein Hesselink EN, Zafon C, Villalmanzo N, et al. Increased global DNA hypomethylation in distant metastatic and dedifferentiated thyroid cancer. J Clin Endocrinol Metab. 2018;103(2):397–406.
   PubMed Web of Science ®Google Scholar
• Buj R, Mallona I, Diez-Villanueva A, et al. Quantification of unmethylated Alu (QUAlu): a tool to assess global hypomethylation in routine clinical samples. Oncotarget. 2016;7(9):10536–10546.
   PubMedGoogle Scholar
• Xiang S, Liu Z, Zhang B, et al. Methylation status of individual CpG sites within Alu elements in the human genome and Alu hypomethylation in gastric carcinomas. BMC Cancer. 2010;10:44.
   PubMed Web of Science ®Google Scholar
• Gilson E, Horard B. Comprehensive DNA methylation profiling of human repetitive DNA elements using an MeDIP-on-RepArray assay. Methods Mol Biol. 2012;859:267–291.
   PubMedGoogle Scholar
• Xie H, Wang M, Bonaldo MD, et al. Epigenomic analysis of Alu repeats in human ependymomas. Proc Natl Acad Sci U S A. 2010;107(15):6952–6957.
   PubMed Web of Science ®Google Scholar
• Hellmann-Blumberg U, Hintz MF, Gatewood JM, et al. Developmental differences in methylation of human Alu repeats. Mol Cell Biol. 1993;13(8):4523–4530.
   PubMed Web of Science ®Google Scholar
• Rodriguez J, Vives L, Jordà M, et al. Genome-wide tracking of unmethylated DNA Alu repeats in normal and cancer cells. Nucleic Acids Res. 2007;36(3):770–784.
   PubMed Web of Science ®Google Scholar
• Brohede J, Rand KN. Evolutionary evidence suggests that CpG island-associated Alus are frequently unmethylated in human germline. Hum Genet. 2006;119(4):457–458.
   PubMed Web of Science ®Google Scholar
• Rand KN, Molloy PL. Sensitive measurement of unmethylated repeat DNA sequences by end-specific PCR. Biotechniques. 2010;49(4):xiii–xvii.
   PubMed Web of Science ®Google Scholar
• Luo Y, Lu X, Xie H. Dynamic Alu methylation during normal development, aging, and tumorigenesis. Biomed Res Int. 2014;2014:784706.
   PubMed Web of Science ®Google Scholar
• Mollet IG, Ben-Dov C, Felicio-Silva D, et al. Unconstrained mining of transcript data reveals increased alternative splicing complexity in the human transcriptome. Nucleic Acids Res. 2010;38(14):4740–4754.
   PubMed Web of Science ®Google Scholar
• Bakshi A, Herke S, Batzer MA, et al. DNA methylation variation of human-specific Alu repeats. Epigenetics. 2016;11(2):163–173.
   PubMed Web of Science ®Google Scholar
• Brosius J. RNAs from all categories generate retrosequences that may be exapted as novel genes or regulatory elements. Gene. 1999;238(1):115–134.
   PubMed Web of Science ®Google Scholar
• Bouttier M, Laperriere D, Memari B, et al. Alu repeats as transcriptional regulatory platforms in macrophage responses toM. tuberculosis infection. Nucleic Acids Res. 2016;44(22):10571–10587.
   PubMed Web of Science ®Google Scholar
• Lunyak VV, Prefontaine GG, Nunez E, et al. Developmentally regulated activation of a SINE B2 repeat as a domain boundary in organogenesis. Science. 2007;317(5835):248–251.
   PubMed Web of Science ®Google Scholar
• Wang X, Fan J, Liu D, et al. Spreading of Alu methylation to the promoter of the MLH1 gene in gastrointestinal cancer. PLoS One. 2011;6(10):e25913.
   PubMed Web of Science ®Google Scholar
• Rollins RA, Haghighi F, Edwards JR, et al. Large-scale structure of genomic methylation patterns. Genome Res. 2006;16(2):157–163.
   PubMed Web of Science ®Google Scholar
• Barrera V, Peinado MA. Evaluation of single CpG sites as proxies of CpG island methylation states at the genome scale. Nucleic Acids Res. 2012;40(22):11490–11498.
   PubMed Web of Science ®Google Scholar
• Djebali S, Davis CA, Merkel A, et al. Landscape of transcription in human cells. Nature. 2012;489(7414):101–108.
   PubMed Web of Science ®Google Scholar
• De Klerk E,T, Hoen PA. Alternative mRNA transcription, processing, and translation: insights from RNA sequencing. Trends Genet. 2015;31(3):128–139.
   PubMed Web of Science ®Google Scholar
• Mayr C, Bartel DP. Widespread shortening of 3′UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell. 2009;138(4):673–684.
   PubMed Web of Science ®Google Scholar
• Frith MC, Mori R, Asai K. A mostly traditional approach improves alignment of bisulfite-converted DNA. Nucleic Acids Res. 2012;40(13):e100.
   PubMed Web of Science ®Google Scholar
• Carninci P, Sandelin A, Lenhard B, et al. Genome-wide analysis of mammalian promoter architecture and evolution. Nat Genet. 2006;38(6):626–635.
   PubMed Web of Science ®Google Scholar
• Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev. 2011;25(10):1010–1022.
   PubMed Web of Science ®Google Scholar
• Davuluri RV, Suzuki Y, Sugano S, et al. The functional consequences of alternative promoter use in mammalian genomes. Trends Genet. 2008;24(4):167–177.
   PubMed Web of Science ®Google Scholar
• Hatchwell E, Greally JM. The potential role of epigenomic dysregulation in complex human disease. Trends Genet. 2007;23(11):588–595.
   PubMed Web of Science ®Google Scholar
• Rach EA, Winter DR, Benjamin AM, et al. Transcription initiation patterns indicate divergent strategies for gene regulation at the chromatin level. PLoS Genet. 2011;7(1):e1001274.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Ma X, Zhang MQ. Bivalent-like chromatin markers are predictive for transcription start site distribution in human. PLoS ONE. 2012;7(6):e38112.
   PubMed Web of Science ®Google Scholar
• Molto E, Fernandez A, Montoliu L. Boundaries in vertebrate genomes: different solutions to adequately insulate gene expression domains. Brief Funct Genomic Proteomic. 2009;8(4):283–296.
   PubMedGoogle Scholar
• Rajendiran S, Gibbs LD, Van Treuren T, et al. MIEN1 is tightly regulated by SINE Alu methylation in its promoter. Oncotarget. 2016;7(40):65307–65319.
   PubMedGoogle Scholar
• Rhee I, Bachman KE, Park BH, et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature. 2002;416(6880):552–556.
   PubMed Web of Science ®Google Scholar
• Barrero MJ, Berdasco M, Paramonov I, et al. DNA hypermethylation in somatic cells correlates with higher reprogramming efficiency. Stem Cells. 2012;30(8):1696–1702.
   PubMed Web of Science ®Google Scholar
• Mallona I, Diez-Villanueva A, Peinado MA. Methylation plotter: a web tool for dynamic visualization of DNA methylation data. Source Code Biol Med. 2014;9(1):11.
   PubMedGoogle Scholar
• Ullu E, Tschudi C. Alu sequences are processed 7SL RNA genes. Nature. 1984;312(5990):171–172.
   PubMed Web of Science ®Google Scholar
• Ngoka LCM. Sample prep for proteomics of breast cancer: proteomics and gene ontology reveal dramatic differences in protein solubilization preferences of radioimmunoprecipitation assay and urea lysis buffers. Proteome Sci. 2008;6:30.
   Web of Science ®Google Scholar
• Pasquali L, Gaulton KJ, Rodriguez-Segui SA, et al. Pancreatic islet enhancer clusters enriched in type 2 diabetes risk-associated variants. Nat Genet. 2014;46(2):136–143.
   PubMed Web of Science ®Google Scholar
• Forn M, Muñoz M, Tauriello DV, et al. Long range epigenetic silencing is a trans-species mechanism that results in cancer specific deregulation by overriding the chromatin domains of normal cells. Mol Oncol. 2013;7(6):1129–1141.
   PubMed Web of Science ®Google Scholar
• Metsalu T, Vilo J. ClustVis: a web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Res. 2015;43(W1):W566–570.
   PubMed Web of Science ®Google Scholar