Alteration of Epigenetic Regulation by Long Noncoding RNAs in Cancer
Abstract
:1. Introduction
2. Regulators of Histone Marks Deposition
2.1. Xist
2.2. HOTAIR
2.3. Other Polycomb Repressive Complexes Regulators
3. Regulators of DNA Methylation
3.1. H19
3.2. DACOR1 and ecCEBPA
3.3. TARID
4. Regulators of Chromosomal Architecture
4.1. CCAT1-L and LUNAR
4.2. LncTCF7 and SChLAP1
5. Conclusions
Acknowledgments
Conflicts of Interest
References
- Ransohoff, J.D.; Wei, Y.; Khavari, P.A. The functions and unique features of long intergenic noncoding RNA. Nat. Rev. Mol. Cell Boil. 2017. [Google Scholar] [CrossRef] [PubMed]
- Shen, H.; Laird, P.W. Interplay between the cancer genome and epigenome. Cell 2013, 153, 38–55. [Google Scholar] [CrossRef] [PubMed]
- Maurano, M.T.; Humbert, R.; Rynes, E.; Thurman, R.E.; Haugen, E.; Wang, H.; Reynolds, A.P.; Sandstrom, R.; Qu, H.; Brody, J.; et al. Systematic localization of common disease associated variation in regulatory DNA. Science 2012, 337, 1190–1195. [Google Scholar] [CrossRef] [PubMed]
- Melton, C.; Reuter, J.A.; Spacek, D.V.; Snyder, M. Recurrent somatic mutations in regulatory regions of human cancer genomes. Nat. Genet. 2015, 47, 710–716. [Google Scholar] [CrossRef] [PubMed]
- Roadmap Epigenomics Consortium; Kundaje, A.; Meuleman, W.; Ernst, J.; Bilenky, M.; Yen, A.; Heravi-Moussavi, A.; Kheradpour, P.; Zhang, Z.; Wang, J.; et al. Integrative analysis of 111 reference human epigenomes. Nature 2015, 518, 317–330. [Google Scholar] [CrossRef] [PubMed]
- Yan, X.; Hu, Z.; Feng, Y.; Hu, X.; Yuan, J.; Zhao, S.D.; Zhang, Y.; Yang, L.; Shan, W.; He, Q.; et al. Comprehensive genomic characterization of long noncoding RNAs across human cancers. Cancer Cell 2015, 28, 529–540. [Google Scholar] [CrossRef] [PubMed]
- Schmitt, A.M.; Chang, H.Y. Long Noncoding RNAs in Cancer Pathways. Cancer Cell 2016, 29, 452–463. [Google Scholar] [CrossRef] [PubMed]
- Kotake, Y.; Nakagawa, T.; Kitagawa, K.; Suzuki, S.; Liu, N.; Kitagawa, M.; Xiong, Y. Long noncoding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4B) tumor suppressor gene. Oncogene 2011, 30, 1956–1962. [Google Scholar] [CrossRef] [PubMed]
- Yap, K.L.; Li, S.; Muñoz-Cabello, A.M.; Raguz, S.; Zeng, L.; Mujtaba, S.; Gil, J.; Walsh, M.J.; Zhou, M.M. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol. Cell 2010, 38, 662–674. [Google Scholar] [CrossRef] [PubMed]
- Chen, D.; Zhang, Z.; Mao, C.; Zhou, Y.; Yu, L.; Yin, Y.; Wu, S.; Mou, X.; Zhu, Y. ANRIL inhibits p15(INK4b) through the TGFβ1 signaling pathway in human esophageal squamous cell carcinoma. Cell Immunol. 2014, 289, 91–96. [Google Scholar] [CrossRef] [PubMed]
- Cunnington, M.S.; Santibanez Koref, M.; Mayosi, B.M.; Burn, J.; Keavney, B. Chromosome 9p21 SNPs Associated with Multiple Disease Phenotypes Correlate with ANRIL Expression. PLoS Genet. 2010, 6, e1000899. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yu, W.; Gius, D.; Onyango, P.; Muldoon-Jacobs, K.; Karp, J.; Feinberg, A.P.; Cui, H. Epigenetic silencing of tumor suppressor gene p15 by its antisense RNA. Nature 2008, 451, 202–206. [Google Scholar] [CrossRef] [PubMed]
- Chung, S.; Nakagawa, H.; Uemura, M.; Piao, L.; Ashikawa, K.; Hosono, N.; Takata, R.; Akamatsu, S.; Kawaguchi, T.; Morizono, T.; et al. Association of a novel long noncoding RNA in 8q24 with prostate cancer susceptibility. Cancer Sci. 2011, 102, 245–252. [Google Scholar] [CrossRef] [PubMed]
- Alaiyan, B.; Ilyayev, N.; Stojadinovic, A.; Izadjoo, M.; Roistacher, M.; Pavlov, V.; Tzivin, V.; Halle, D.; Pan, H.; Trink, B.; et al. Differential expression of colon cancer associated transcript1 (CCAT1) along the colonic adenoma-carcinoma sequence. BMC Cancer 2013, 13, 196. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Merry, C.R.; Forrest, M.E.; Sabers, J.N.; Beard, L.; Gao, X.H.; Hatzoglou, M.; Jackson, M.W.; Wang, Z.; Markowitz, S.D.; Khalil, A.M. DNMT1-associated long noncoding RNAs regulate global gene expression and DNA methylation in colon cancer. Hum. Mol. Genet. 2015, 24, 6240–6253. [Google Scholar] [CrossRef] [PubMed]
- Di Ruscio, A.; Ebralidze, A.K.; Benoukraf, T.; Amabile, G.; Goff, L.A.; Terragni, J.; Figueroa, M.E.; De Figueiredo Pontes, L.L.; Alberich-Jorda, M.; Zhang, P.; et al. DNMT1-interacting RNAs block gene-specific DNA methylation. Nature 2013, 503, 371. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nasrollahzadeh-Khakiani, M.; Emadi-Baygi, M.; Nikpour, P. Augmented expression levels of lncRNAs ecCEBPA and UCA1 in gastric cancer tissues and their clinical significance. Iran. J. Basic Med. Sci. 2017, 20, 1149–1158. [Google Scholar] [PubMed]
- Hu, X.; Feng, Y.; Zhang, D.; Zhao, S.D.; Hu, Z.; Greshock, J.; Zhang, Y.; Yang, L.; Zhong, X.; Wang, L.P.; et al. A functional genomic approach identifies FAL1 as an oncogenic long noncoding RNA that associates with BMI1 and represses p21 expression in cancer. Cancer Cell 2014, 26, 344–357. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.; Yang, L.; Zhong, T.; Mueller, M.; Men, Y.; Zhang, N.; Xie, J.; Giang, K.; Chung, H.; Sun, X.; et al. H19 lncRNA alters DNA methylation genome wide by regulating S-adenosylhomocysteine hydrolase. Nat. Commun. 2015, 6, 10221. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Engel, N.; Thorvaldsen, J.L.; Bartolomei, M.S. CTCF binding sites promote transcription initiation and prevent DNA methylation on the maternal allele at the imprinted H19/Igf2 locus. Hum. Mol. Genet. 2006, 15, 2945–2954. [Google Scholar] [CrossRef] [PubMed]
- Guo, G.; Kang, Q.; Chen, Q.; Chen, Z.; Wang, J.; Tan, L.; Chen, J.L. High expression of long noncoding RNA H19 is required for efficient tumorigenesis induced by Bcr–Abl oncogene. FEBS Lett. 2014, 588, 1780–1786. [Google Scholar] [CrossRef] [PubMed]
- Dugimont, T.; Montpellier, C.; Adriaenssens, E.; Lottin, S.; Dumont, L.; Iotsova, V.; Lagrou, C.; Stéhelin, D.; Coll, J.; Curgy, J.J. The H19 TATA–less promoter is efficiently repressed by wild–type tumor suppressor gene product p53. Oncogene 1998, 16, 2395–2401. [Google Scholar] [CrossRef] [PubMed]
- Barsyte-Lovejoy, D.; Lau, S.K.; Boutros, P.C.; Khosravi, F.; Jurisica, I.; Andrulis, I.L.; Tsao, M.S.; Penn, L.Z. The c-Myc oncogene directly induces the H19 noncoding RNA by allele-specific binding to potentiate tumorigenesis. Cancer Res. 2006, 66, 5330–5337. [Google Scholar] [CrossRef] [PubMed]
- Park, I.Y.; Sohn, B.H.; Choo, J.H.; Joe, C.O.; Seong, J.K.; Lee, Y.I.; Chung, J.H. Deregulation of DNA methyltransferases and loss of parental methylation at the insulin-like growth factor II (Igf2)/H19 loci in p53 knockout mice prior to tumor development. J. Cell. Biochem. 2005, 94, 585–596. [Google Scholar] [CrossRef] [PubMed]
- Matouk, I.J.; Mezan, S.; Mizrahi, A.; Ohana, P.; Abu-Lail, R.; Galun, E.; Hochberg, A. The oncofetal H19 RNA connection: Hypoxia, p53 and cancer. Biochim. Biophys. Acta 2010, 1803, 443–451. [Google Scholar] [CrossRef] [PubMed]
- Rinn, J.L.; Kertesz, M.; Wang, J.K.; Squazzo, S.L.; Xu, X.; Brugmann, S.A.; Goodnough, L.H.; Helms, J.A.; Farnham, P.J.; Segal, E.; et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007, 129, 1311–1323. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Zhang, P.; Wang, L.; Piao, H.L.; Ma, L. Long noncoding RNA HOTAIR in carcinogenesis and metastasis. Acta Biochim. Biophys. Sin. 2014, 46, 1–5. [Google Scholar] [CrossRef] [PubMed]
- Li, G.; Zhang, H.; Wan, X.; Yang, X.; Zhu, C.; Wang, A.; He, L.; Miao, R.; Chen, S.; Zhao, H. Long noncoding RNA plays a key role in metastasis and prognosis of hepatocellular carcinoma. BioMed Res. Int. 2014, 780521. [Google Scholar] [CrossRef] [PubMed]
- Gupta, R.A.; Shah, N.; Wang, K.C.; Kim, J.; Horlings, H.M.; Wong, D.J.; Tsai, M.C.; Hung, T.; Argani, P.; Rinn, J.L.; et al. Long noncoding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010, 464, 1071–1076. [Google Scholar] [CrossRef] [PubMed]
- Kogo, R.; Shimamura, T.; Mimori, K.; Kawahara, K.; Imoto, S.; Sudo, T.; Tanaka, F.; Shibata, K.; Suzuki, A.; Komune, S.; et al. Long noncoding RNA HOTAIR regulates polycomb-dependent chromatin modification and is associated with poor prognosis in colorectal cancers. Cancer Res. 2011, 71, 6320–6326. [Google Scholar] [CrossRef] [PubMed]
- Tsai, M.C.; Manor, O.; Wan, Y.; Mosammaparast, N.; Wang, J.K.; Lan, F.; Shi, Y.; Segal, E.; Chang, H.Y. Long noncoding RNA as modular scaffold of histone modification complexes. Science 2010, 329, 689–693. [Google Scholar] [CrossRef] [PubMed]
- Portoso, M.; Ragazzini, R.; Brenčič, Ž.; Moiani, A.; Michaud, A.; Vassilev, I.; Wassef, M.; Servant, N.; Sargueil, B.; Margueron, R. PRC2 is dispensable for HOTAIR-mediated transcriptional repression. EMBO J. 2017, 36, 981–994. [Google Scholar] [CrossRef] [PubMed]
- Sun, M.; Nie, F.; Wang, Y.; Zhang, Z.; Hou, J.; He, D.; Xie, M.; Xu, L.; De, W.; Wang, Z.; et al. LncRNA HOXA11-AS Promotes Proliferation and Invasion of Gastric Cancer by Scaffolding the Chromatin Modification Factors PRC2, LSD1, and DNMT1. Cancer Res. 2016, 76, 6299–6310. [Google Scholar] [CrossRef] [PubMed]
- Li, T.; Xu, C.; Cai, B.; Zhang, M.; Gao, F.; Gan, J. Expression and clinicopathological significance of the lncRNA HOXA11-AS in colorectal cancer. Oncol. Lett. 2016, 12, 4155–4160. [Google Scholar] [CrossRef] [PubMed]
- Leveille, N.; Melo, C.A.; Rooijers, K.; Diaz-Lagares, A.; Melo, S.A.; Korkmaz, G.; Lopes, R.; Akbari Moqadam, F.; Maia, A.R.; Wijchers, P.J.; et al. Genome-wide profiling of p53-regulated enhancer RNAs uncovers a subset of enhancers controlled by a lncRNA. Nat. Commun. 2015, 6, 6520. [Google Scholar] [CrossRef] [PubMed]
- Marin-Bejar, O.; Marchese, F.P.; Athie, A.; Sanchez, Y.; Gonzalez, J.; Segura, V.; Huang, L.; Moreno, I.; Navarro, A.; Monzo, M.; et al. Pint lincRNA connects the p53 pathway with epigenetic silencing by the Polycomb repressive complex 2. Genome Biol. 2013, 14, R104. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marin-Bejar, O.; Mas, A.M.; González, J.; Martinez, D.; Athie, A.; Morales, X.; Galduroz, M.; Raimondi, I.; Grossi, E.; Guo, S.; et al. The human lncRNA LINC-PINT inhibits tumor cell invasion through a highly conserved sequence element. Genome Biol. 2017, 18, 202. [Google Scholar] [CrossRef] [PubMed]
- Hollingshead, M.G.; Stockwin, L.H.; Alcoser, S.Y.; Newton, D.L.; Orsburn, B.C.; Bonomi, C.A.; Borgel, S.D.; Divelbiss, R.; Dougherty, K.M.; Hager, E.J.; et al. Gene expression profiling of 49 human tumor xenografts from in vitro culture through multiple in vivo passages–strategies for data mining in support of therapeutic studies. BMC Genom. 2014, 15, 393. [Google Scholar] [CrossRef] [PubMed]
- Tang, Y.; Wang, J.; Lian, Y.; Fan, C.; Zhang, P.; Wu, Y.; Li, X.; Xiong, F.; Li, X.; Li, G.; et al. Linking long noncoding RNAs and SWI/SNF complexes to chromatin remodeling in cancer. Mol. Cancer 2017, 16, 42. [Google Scholar] [CrossRef] [PubMed]
- Weng, A.P.; Ferrando, A.A.; Lee, W.; Morris, J.P., IV; Silverman, L.B.; Sanchez-Irizarry, C.; Blacklow, S.C.; Look, A.T.; Aster, J.C. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 2004, 306, 269–271. [Google Scholar] [CrossRef] [PubMed]
- Trimarchi, T.; Bilal, E.; Ntziachristos, P.; Fabbri, G.; Dalla-Favera, R.; Tsirigos, A.; Aifantis, I. Genome-wide mapping and characterization of Notch-regulated long noncoding RNAs in acute leukemia. Cell 2014, 158, 593–606. [Google Scholar] [CrossRef] [PubMed]
- Montes, M.; Nielsen, M.M.; Maglieri, G.; Jacobsen, A.; Højfeldt, J.; Agrawal-Singh, S.; Hansen, K.; Helin, K.; van de Werken, H.J.; Pedersen, J.S.; et al. The lncRNA MIR31HG regulates p16(INK4A) expression to modulate senescence. Nat. Commun. 2015, 6, 6967. [Google Scholar] [CrossRef] [PubMed]
- Pandey, G.K.; Mitra, S.; Subhash, S.; Hertwig, F.; Kanduri, M.; Mishra, K.; Fransson, S.; Ganeshram, A.; Mondal, T.; Bandaru, S.; et al. The risk-associated long noncoding RNA NBAT-1 controls neuroblastoma progression by regulating cell proliferation and neuronal differentiation. Cancer Cell 2014, 26, 722–737. [Google Scholar] [CrossRef] [PubMed]
- Hu, P.; Chu, J.; Wu, Y.; Sun, L.; Lv, X.; Zhu, Y.; Li, J.; Guo, Q.; Gong, C.; Liu, B.; et al. NBAT1 suppresses breast cancer metastasis by regulating DKK1 via PRC2. Oncotarget 2015, 6, 32410–32425. [Google Scholar] [CrossRef] [PubMed]
- Myant, K.B.; Cammareri, P.; McGhee, E.J.; Ridgway, R.A.; Huels, D.J.; Cordero, J.B.; Schwitalla, S.; Kalna, G.; Ogg, E.L.; Athineos, D.; et al. ROS production and NF-kB activation triggered by RAC1 facilitate WNT driven intestinal stem cell proliferation and colorectal cancer initiation. Cell Stem Cell 2013, 12, 761–773. [Google Scholar] [CrossRef] [PubMed]
- Quaggin, S.E.; Schwartz, L.; Cui, S.; Igarashi, P.; Deimling, J.; Post, M.; Rossant, J. The basic-helix-loop-helix protein pod1 is critically important for kidney and lung organogenesis. Development 1999, 126, 5771–5783. [Google Scholar] [PubMed]
- Arab, K.; Smith, L.T.; Gast, A.; Weichenhan, D.; Huang, J.P.; Claus, R.; Hielscher, T.; Espinosa, A.V.; Ringel, M.D.; Morrison, C.D.; et al. Epigenetic deregulation of TCF21 inhibits metastasis suppressor KISS1 in metastatic melanoma. Carcinogenesis 2011, 32, 1467–1473. [Google Scholar] [CrossRef] [PubMed]
- Smith, L.T.; Lin, M.; Brena, R.M.; Lang, J.C.; Schuller, D.E.; Otterson, G.A.; Morrison, C.D.; Smiraglia, D.J.; Plass, C. Epigenetic regulation of the tumor suppressor gene TCF21 on 6q23-q24 in lung and head and neck cancer. Proc. Natl. Acad. Sci. USA 2006, 103, 982–987. [Google Scholar] [CrossRef] [PubMed]
- Yildirim, E.; Kirby, J.E.; Brown, D.E.; Mercier, F.E.; Sadreyev, R.I.; Scadden, D.T.; Lee, J.T. Xist RNA is a potent suppressor of hematologic cancer in mice. Cell 2013, 152, 727–742. [Google Scholar] [CrossRef] [PubMed]
- Davidovich, C.; Zheng, L.; Goodrich, K.J.; Cech, T.R. Promiscuous RNA binding by Polycomb repressive complex 2. Nat. Struct. Mol. Biol. 2013, 20, 1250–1257. [Google Scholar] [CrossRef] [PubMed]
- Kaneko, S.; Son, J.; Shen, S.S.; Reinberg, D.; Bonasio, R. PRC2 binds active promoters and contacts nascent RNAs in embryonic stem cells. Nat. Struct. Mol. Biol. 2013, 20, 1258–1264. [Google Scholar] [CrossRef] [PubMed]
- Lee, J.T.; Bartolomei, M.S. X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell 2013, 152, 1308–1323. [Google Scholar] [CrossRef] [PubMed]
- Wutz, A.; Rasmussen, T.P.; Jaenisch, R. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat. Genet. 2002, 30, 167–174. [Google Scholar] [CrossRef] [PubMed]
- Beletskii, A.; Hong, Y.K.; Pehrson, J.; Egholm, M.; Strauss, W.M. PNA interference mapping demonstrates functional domains in the noncoding RNA Xist. Proc. Natl Acad. Sci. USA 2001, 98, 9215–9220. [Google Scholar] [CrossRef] [PubMed]
- Zhao, J.; Sun, B.K.; Erwin, J.A.; Song, J.J.; Lee, J.T. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 2008, 322, 750–756. [Google Scholar] [CrossRef] [PubMed]
- Kalantry, S.; Magnuson, T. The Polycomb group protein EED is dispensable for the initiation of random X-chromosome inactivation. PLoS Genet. 2006, 2, e66. [Google Scholar] [CrossRef] [PubMed]
- Kalantry, S.; Mills, K.C.; Yee, D.; Otte, A.P.; Panning, B.; Magnuson, T. The Polycomb group protein Eed protects the inactive X-chromosome from differentiation-induced reactivation. Nat. Cell Biol. 2006, 8, 195–202. [Google Scholar] [CrossRef] [PubMed]
- Chu, C.; Zhang, Q.C.; da Rocha, S.T.; Flynn, R.A.; Bharadwaj, M.; Calabrese, J.M.; Magnuson, T.; Heard, E.; Chang, H.Y. Systematic discovery of Xist RNA binding proteins. Cell 2015, 161, 404–416. [Google Scholar] [CrossRef] [PubMed]
- McHugh, C.A.; Chen, C.K.; Chow, A.; Surka, C.F.; Tran, C.; McDonel, P.; Pandya-Jones, A.; Blanco, M.; Burghard, C.; Moradian, A.; et al. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 2015, 521, 232–236. [Google Scholar] [CrossRef] [PubMed]
- Spatz, A.; Borg, C.; Feunteun, J. X-chromosome genetics and human cancer. Nat. Rev. Cancer 2004, 4, 617–629. [Google Scholar] [CrossRef] [PubMed]
- Thull, D.L.; Vogel, V.G. Recognition and management of hereditary breast cancer syndromes. Oncologist 2004, 9, 13–24. [Google Scholar] [CrossRef] [PubMed]
- Moynahan, M.E.; Chiu, J.W.; Koller, B.H.; Jasin, M. Brca1 controls homology-directed DNA repair. Mol. Cell 1999, 4, 511–518. [Google Scholar] [CrossRef]
- Farmer, H.; McCabe, N.; Lord, C.J.; Tutt, A.N.; Johnson, D.A.; Richardson, T.B.; Santarosa, M.; Dillon, K.J.; Hickson, I.; Knights, C.; et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434, 917–921. [Google Scholar] [CrossRef] [PubMed]
- Ganesan, S.; Silver, D.P.; Greenberg, R.A.; Avni, D.; Drapkin, R.; Miron, A.; Mok, S.C.; Randrianarison, V.; Brodie, S.; Salstrom, J.; et al. BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell 2002, 111, 393–405. [Google Scholar] [CrossRef]
- Jazaeri, A.A.; Yee, C.J.; Sotiriou, C.; Brantley, K.R.; Boyd, J.; Liu, E.T. Gene expression profiles of BRCA1-linked, BRCA2-linked, and sporadic ovarian cancers. J. Natl. Cancer Inst. 2002, 94, 990–1000. [Google Scholar] [CrossRef] [PubMed]
- Skalska, L.; Beltran-Nebot, M.; Ule, J.; Jenner, R.G. Regulatory feedback from nascent RNA to chromatin and transcription. Nat. Rev. Mol. Cell Biol. 2017, 18, 331–337. [Google Scholar] [CrossRef] [PubMed]
- Kim, W.Y.; Sharpless, N.E. The regulation of INK4/ARF in cancer and aging. Cell 2006, 127, 265–275. [Google Scholar] [CrossRef] [PubMed]
- Beroukhim, R.; Mermel, C.H.; Porter, D.; Wei, G.; Raychaudhuri, S.; Donovan, J.; Barretina, J.; Boehm, J.S.; Dobson, J.; Urashima, M.; et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010, 463, 899–905. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bignell, G.R.; Greenman, C.D.; Davies, H.; Butler, A.P.; Edkins, S.; Andrews, J.M.; Buck, G.; Chen, L.; Beare, D.; Latimer, C.; et al. Signatures of mutation and selection in the cancer genome. Nature 2010, 463, 893–898. [Google Scholar] [CrossRef] [PubMed]
- Freedberg, D.E.; Rigas, S.H.; Russak, J.; Gai, W.; Kaplow, M.; Osman, I.; Turner, F.; Randerson-Moor, J.A.; Houghton, A.; Busam, K.; et al. Frequent p16-independent inactivation of p14ARF in human melanoma. J. Natl. Cancer Inst. 2008, 100, 784–795. [Google Scholar] [CrossRef] [PubMed]
- Ding, J.; Li, J.; Wang, H.; Tian, Y.; Xie, M.; He, X.; Ji, H.; Ma, Z.; Hui, B.; Wang, K.; et al. Long noncoding RNA CRNDE promotes colorectal cancer cell proliferation viaepigenetically silencing DUSP5/CDKN1A expression. Cell Death Dis. 2017, 8, e2997. [Google Scholar] [CrossRef] [PubMed]
- Xie, W.; Schultz, M.D.; Lister, R.; Hou, Z.; Rajagopal, N.; Ray, P.; Whitaker, J.W.; Tian, S.; Hawkins, R.D.; Leung, D.; et al. Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 2013, 153, 1134–1148. [Google Scholar] [CrossRef] [PubMed]
- Meissner, A.; Mikkelsen, T.S.; Gu, H.; Wernig, M.; Hanna, J.; Sivachenko, A.; Zhang, X.; Bernstein, B.E.; Nusbaum, C.; Jaffe, D.B.; et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 2008, 454, 766–770. [Google Scholar] [CrossRef] [PubMed]
- Klose, R.J.; Bird, A.P. Genomic DNA methylation: The mark and its mediators. Trends Biochem. Sci. 2006, 31, 89–97. [Google Scholar] [CrossRef] [PubMed]
- Ziller, M.J.; Gu, H.; Müller, F.; Donaghey, J.; Tsai, L.T.; Kohlbacher, O.; De Jager, P.L.; Rosen, E.D.; Bennett, D.A.; Bernstein, B.E.; et al. Charting a dynamic DNA methylation landscape of the human genome. Nature 2013, 500, 477–481. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boultwood, J.; Wainscoat, J.S. Gene silencing by DNA methylation in haematological malignancies. Br. J. Haematol. 2007, 138, 3–11. [Google Scholar] [CrossRef] [PubMed]
- Iacobuzio-Donahue, C.A. Epigenetic changes in cancer. Annu. Rev. Pathol. Mech. Dis. 2009, 4, 229–249. [Google Scholar] [CrossRef] [PubMed]
- Irizarry, R.A.; Ladd-Acosta, C.; Wen, B.; Wu, Z.; Montano, C.; Onyango, P.; Cui, H.; Gabo, K.; Rongione, M.; Webster, M.; et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat. Genet. 2009, 41, 178–186. [Google Scholar] [CrossRef] [PubMed]
- Sasaki, H.; Ishihara, K.; Kato, R. Mechanisms of Igf2/H19 imprinting: DNA methylation, chromatin and long-distance gene regulation. J. Biochem. 2000, 127, 711–715. [Google Scholar] [CrossRef] [PubMed]
- Yoshimizu, T.; Miroglio, A.; Ripoche, M.A.; Gabory, A.; Vernucci, M.; Riccio, A.; Colnot, S.; Godard, C.; Terris, B.; Jammes, H.; et al. The H19 locus acts in vivo as a tumor suppressor. Proc. Natl. Acad. Sci. USA 2008, 105, 12417–12422. [Google Scholar] [CrossRef] [PubMed]
- Lottin, S.; Adriaenssens, E.; Dupressoir, T.; Berteaux, N.; Montpellier, C.; Coll, J.; Dugimont, T.; Curgy, J.J. Overexpression of an ectopic H19 gene enhances the tumorigenic properties of breast cancer cells. Carcinogenesis 2002, 23, 1885–1895. [Google Scholar] [CrossRef] [PubMed]
- Berteaux, N.; Lottin, S.; Monte, D.; Pinte, S.; Quatannens, B.; Coll, J.; Hondermarck, H.; Curgy, J.J.; Dugimont, T.; Adriaenssens, E. H19 mRNA-like noncoding RNA promotes breast cancer cell proliferation through positive control by E2F1. J. Biol. Chem. 2005, 280, 29625–29636. [Google Scholar] [CrossRef] [PubMed]
- Berteaux, N.; Lottin, S.; Adriaenssens, E.; Van Coppenolle, F.; Leroy, X.; Coll, J.; Dugimont, T.; Curgy, J.J. Hormonal regulation of H19 gene expression in prostate epithelial cells. J. Endocrinol. 2004, 183, 69–78. [Google Scholar] [CrossRef] [PubMed]
- Hata, A.; Lagna, G.; Massague, J.; Hemmati-Brivanlou, A. Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev. 1998, 12, 186–197. [Google Scholar] [CrossRef] [PubMed]
- Kodach, L.L.; Wiercinska, E.; de Miranda, N.F.; Bleuming, S.A.; Musler, A.R.; Peppelenbosch, M.P.; Dekker, E.; van den Brink, G.R.; van Noesel, C.J.; Morreau, H.; et al. The bone morphogenetic protein pathway is inactivated in the majority of sporadic colorectal cancers. Gastroenterology 2008, 134, 1332–1341. [Google Scholar] [CrossRef] [PubMed]
- Chaneton, B.; Hillmann, P.; Zheng, L.; Martin, A.C.; Maddocks, O.D.; Chokkathukalam, A.; Coyle, J.E.; Jankevics, A.; Holding, F.P.; Vousden, K.H.; et al. Serine is a natural ligand and allosteric activator of pyruvate kinase M2. Nature 2012, 491, 458–462. [Google Scholar] [CrossRef] [PubMed]
- Wong, N.; De Melo, J.; Tang, D. PKM2, a central point of regulation in cancer metabolism. Int. J. Cell Biol. 2013, 2013. [Google Scholar] [CrossRef] [PubMed]
- Frank-Kamenetskii, M.D.; Mirkin, S.M. Triplex DNA structures. Annu. Rev. Biochem. 1995, 64, 65–95. [Google Scholar] [CrossRef] [PubMed]
- Xue, M.; Li, X.; Wu, W.; Zhang, S.; Wu, S.; Li, Z.; Chen, W. Upregulation of long noncoding RNA urothelial carcinoma associated 1 by CCAAT/enhancer binding protein alpha contributes to bladder cancer cell growth and reduced apoptosis. Oncol. Rep. 2014, 31, 1993–2000. [Google Scholar] [CrossRef] [PubMed]
- Hughes, J.M.; Legnini, I.; Salvatori, B.; Masciarelli, S.; Marchioni, M.; Fazi, F.; Morlando, M.; Bozzoni, I.; Fatica, A. C/EBPα-p30 protein induces expression of the oncogenic long noncoding RNA UCA1 in acute myeloid leukemia. Oncotarget 2015, 6, 18534–18544. [Google Scholar] [CrossRef] [PubMed]
- Bergman, Y.; Cedar, H. DNA methylation dynamics in health and disease. Nat. Struct. Mol. Biol. 2013, 20, 274–281. [Google Scholar] [CrossRef] [PubMed]
- Tessema, M.; Willink, R.; Do, K.; Yu, Y.Y.; Yu, W.; Machida, E.O.; Brock, M.; Van Neste, L.; Stidley, C.A.; Baylin, S.B.; Belinsky, S.A. Promoter methylation of genes in and around the candidate lung cancer susceptibility locus 6q23–25. Cancer Res. 2008, 68, 1707–1714. [Google Scholar] [CrossRef] [PubMed]
- Barreto, G.; Schäfer, A.; Marhold, J.; Stach, D.; Swaminathan, S.K.; Handa, V.; Döderlein, G.; Maltry, N.; Wu, W.; Lyko, F.; et al. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 2007, 445, 671–675. [Google Scholar] [CrossRef] [PubMed]
- Cortellino, S.; Xu, J.; Sannai, M.; Moore, R.; Caretti, E.; Cigliano, A.; Le Coz, M.; Devarajan, K.; Wessels, A.; Soprano, D.; et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 2011, 146, 67–79. [Google Scholar] [CrossRef] [PubMed]
- Schmitz, K.M.; Schmitt, N.; Hoffmann-Rohrer, U.; Schäfer, A.; Grummt, I.; Mayer, C. TAF12 recruits Gadd45a and the nucleotide excision repair complex to the promoter of rRNA genes leading to active DNA demethylation. Mol. Cell 2009, 33, 344–353. [Google Scholar] [CrossRef] [PubMed]
- Ginno, P.A.; Lott, P.L.; Christensen, H.C.; Korf, I.; Chédin, F. R-loop formation is a distinctive characteristic of unmethylated human CpG island promoters. Mol. Cell 2012, 45, 814–825. [Google Scholar] [CrossRef] [PubMed]
- Lam, M.T.Y.; Li, W.; Rosenfeld, M.G.; Glass, C.K. Enhancer RNAs and regulated transcriptional programs. Trends Biochem. Sci. 2014, 39, 170–182. [Google Scholar] [CrossRef] [PubMed]
- Hah, N.; Danko, C.G.; Core, L.; Waterfall, J.J.; Siepel, A.; Lis, J.T.; Kraus, W.L. A rapid, extensive, and transient transcriptional response to estrogen signaling in breast cancer cells. Cell 2011, 145, 622–634. [Google Scholar] [CrossRef] [PubMed]
- Wang, D.; Garcia-Bassets, I.; Benner, C.; Li, W.; Su, X.; Zhou, Y.; Qiu, J.; Liu, W.; Kaikkonen, M.U.; Ohgi, K.A.; et al. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature 2011, 474, 390–394. [Google Scholar] [CrossRef] [PubMed]
- Ko, J.Y.; Oh, S.; Yoo, K.H. Functional Enhancers As Master Regulators of Tissue-Specific Gene Regulation and Cancer Development. Mol. Cells 2017, 40, 169–177. [Google Scholar] [PubMed]
- Shou, Y.; Martelli, M.L.; Gabrea, A.; Qi, Y.; Brents, L.A.; Roschke, A.; Dewald, G.; Kirsch, I.R.; Bergsagel, P.L.; Kuehl, W.M. Diverse karyotypic abnormalities of the c-myc locus associated with cmyc dysregulation and tumor progression in multiple myeloma. Proc. Natl. Acad. Sci. USA 2000, 97, 228–233. [Google Scholar] [CrossRef] [PubMed]
- Affer, M.; Chesi, M.; Chen, W.D.; Keats, J.J.; Demchenko, Y.N.; Tamizhmani, K.; Garbitt, V.M.; Riggs, D.L.; Brents, L.A.; Roschke, A.V.; et al. Promiscuous MYC locus rearrangements hijack enhancers but mostly super-enhancers to dysregulate MYC expression in multiple myeloma. Leukemia 2014, 28, 1725–1735. [Google Scholar] [CrossRef] [PubMed]
- Gudmundsson, J.; Sulem, P.; Manolescu, A.; Amundadottir, L.T.; Gudbjartsson, D.; Helgason, A.; Rafnar, T.; Bergthorsson, J.T.; Agnarsson, B.A.; Baker, A.; et al. Genome-wide association study identifies a second prostate cancer susceptibility variant at 8q24. Nat. Genet. 2007, 39, 631–637. [Google Scholar] [CrossRef] [PubMed]
- Ghoussaini, M.; Song, H.; Koessler, T.; Al Olama, A.A.; Kote-Jarai, Z.; Driver, K.E.; Pooley, K.A.; Ramus, S.J.; Kjaer, S.K.; Hogdall, E.; et al. Multiple loci with different cancer specificities within the 8q24 gene desert. J. Natl. Cancer Inst. 2008, 100, 962–966. [Google Scholar] [CrossRef] [PubMed]
- Easton, D.F.; Pooley, K.A.; Dunning, A.M.; Pharoah, P.D.; Thompson, D.; Ballinger, D.G.; Struewing, J.P.; Morrison, J.; Field, H.; Luben, R.; et al. Genome-wide association study identifies novel breast cancer susceptibility loci. Nature 2007, 447, 1087–1093. [Google Scholar] [CrossRef] [PubMed]
- Zanke, B.W.; Greenwood, C.M.; Rangrej, J.; Kustra, R.; Tenesa, A.; Farrington, S.M.; Prendergast, J.; Olschwang, S.; Chiang, T.; Crowdy, E.; et al. Genome-wide association scan identifies a colorectal cancer susceptibility locus on chromosome 8q24. Nat. Genet. 2007, 39, 989–994. [Google Scholar] [CrossRef] [PubMed]
- Ahmadiyeh, N.; Pomerantz, M.M.; Grisanzio, C.; Herman, P.; Jia, L.; Almendro, V.; He, H.H.; Brown, M.; Liu, X.S.; Davis, M.; et al. 8q24 prostate, breast, and colon cancer risk loci show tissue-specific long-range interaction with MYC. Proc. Natl. Acad. Sci. USA 2010, 107, 9742–9746. [Google Scholar] [CrossRef] [PubMed]
- Hung, C.L.; Wang, L.Y.; Yu, Y.L.; Chen, H.W.; Srivastava, S.; Petrovics, G.; Kung, H.J. A long noncoding RNA connects c-Myc to tumor metabolism. Proc. Natl. Acad. Sci. USA 2014, 111, 18697–18702. [Google Scholar] [CrossRef] [PubMed]
- Prensner, J.R.; Iyer, M.K.; Balbin, O.A.; Dhanasekaran, S.M.; Cao, Q.; Brenner, J.C.; Laxman, B.; Asangani, I.A.; Grasso, C.S.; Kominsky, H.D.; et al. Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression. Nat. Biotechnol. 2011, 29, 742–749. [Google Scholar] [CrossRef] [PubMed]
- Ling, H.; Spizzo, R.; Atlasi, Y.; Nicoloso, M.; Shimizu, M.; Redis, R.S.; Nishida, N.; Gafà, R.; Song, J.; Guo, Z.; et al. CCAT2, a novel noncoding RNA mapping to 8q24, underlies metastatic progression and chromosomal instability in colon cancer. Genome Res. 2013, 23, 1446–1461. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nissan, A.; Stojadinovic, A.; Mitrani-Rosenbaum, S.; Halle, D.; Grinbaum, R.; Roistacher, M.; Bochem, A.; Dayanc, B.E.; Ritter, G.; Gomceli, I.; et al. Colon cancer associated transcript-1: A novel RNA expressed in malignant and pre-malignant human tissues. Int. J. Cancer 2012, 130, 1598–1606. [Google Scholar] [CrossRef] [PubMed]
- Xiang, J.F.; Yin, Q.F.; Chen, T.; Zhang, Y.; Zhang, X.O.; Wu, Z.; Zhang, S.; Wang, H.B.; Ge, J.; Lu, X.; et al. Human colorectal cancer-specific CCAT1-L lncRNA regulates long-range chromatin interactions at the MYC locus. Cell Res. 2014, 24, 513–531. [Google Scholar] [CrossRef] [PubMed]
- Sanyal, A.; Lajoie, B.R.; Jain, G.; Dekker, J. The long-range interaction landscape of gene promoters. Nature 2012, 489, 109–113. [Google Scholar] [CrossRef] [PubMed]
- Phillips, J.E.; Corces, V.G. CTCF: Master weaver of the genome. Cell 2009, 137, 1194–1211. [Google Scholar] [CrossRef] [PubMed]
- Ferrando, A.A.; Neuberg, D.S.; Staunton, J.; Loh, M.L.; Huard, C.; Raimondi, S.C.; Behm, F.G.; Pui, C.H.; Downing, J.R.; Gilliland, D.G.; et al. Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 2002, 1, 75–87. [Google Scholar] [CrossRef]
- Medyouf, H.; Gusscott, S.; Wang, H.; Tseng, J.C.; Wai, C.; Nemirovsky, O.; Trumpp, A.; Pflumio, F.; Carboni, J.; Gottardis, M.; et al. High-level IGF1R expression is required for leukemia-initiating cell activity in T-ALL and is supported by Notch signaling. J. Exp. Med. 2011, 208, 1809–1822. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roberts, C.W.; Orkin, S.H. The SWI/SNF complex—Chromatin and cancer. Nat. Rev. Cancer 2004, 4, 133–142. [Google Scholar] [CrossRef] [PubMed]
- Tolstorukov, M.Y.; Sansam, C.G.; Lu, P.; Koellhoffer, E.C.; Helming, K.C.; Alver, B.H.; Tillman, E.J.; Evans, J.A.; Wilson, B.G.; Park, P.J.; et al. Swi/Snf chromatin remodeling/tumor suppressor complex establishes nucleosome occupancy at target promoters. Proc. Natl. Acad. Sci. USA 2013, 110, 10165–10170. [Google Scholar] [CrossRef] [PubMed]
- You, J.S.; De Carvalho, D.D.; Dai, C.; Liu, M.; Pandiyan, K.; Zhou, X.J.; Liang, G.; Jones, P.A. SNF5 is an essential executor of epigenetic regulation during differentiation. PLoS Genet. 2013, 9, e1003459. [Google Scholar] [CrossRef] [PubMed]
- Reisman, D.; Glaros, S.; Thompson, E.A. The SWI/SNF complex and cancer. Oncogene 2009, 28, 1653–1668. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; He, L.; Du, Y.; Zhu, P.; Huang, G.; Luo, J.; Yan, X.; Ye, B.; Li, C.; Xia, P.; et al. The long noncoding RNA lncTCF7 promotes self-renewal of human liver cancer stem cells through activation of Wnt signaling. Cell Stem Cell 2015, 16, 413–425. [Google Scholar] [CrossRef] [PubMed]
- Hoffmeyer, K.; Raggioli, A.; Rudloff, S.; Anton, R.; Hierholzer, A.; Del Valle, I.; Hein, K.; Vogt, R.; Kemler, R. Wnt/β-catenin signaling regulates telomerase in stem cells and cancer cells. Science 2012, 336, 1549–1554. [Google Scholar] [CrossRef] [PubMed]
- Prensner, J.R.; Iyer, M.K.; Sahu, A.; Asangani, I.A.; Cao, Q.; Patel, L.; Vergara, I.A.; Davicioni, E.; Erho, N.; Ghadessi, M.; et al. The long noncoding RNA SChLAP1 promotes aggressive prostate cancer and antagonizes the SWI/SNF complex. Nat. Genet. 2013, 45, 1392–1398. [Google Scholar] [CrossRef] [PubMed]
Name | Cancer | Mechanism | Ref. |
---|---|---|---|
ANRIL | High expression linked to poor outcome in prostate and gastric cancer. | Interacts with CBX7 and PRC2 to silence the INK4b/ARF/INK4a locus. | [8,9,10,11,12] |
CCAT1-L | Upregulated in human colorectal cancers | Regulates long-range chromatin interactions to activate the transcription of the MYC locus. | [13,14] |
DACOR1 | Downregulated in colon tumors. | Interacts with and inhibits the DNA methyltransferase DNMT1. | [15] |
ecCEBPA | Shows inverse correlation with CEBPA in leukaemia cell lines. | Interacts with DNMT1 and prevents CEBPA locus methylation. | [16,17] |
FAL1 | Frequently amplified in human cancers. | Interacts with PRC1 to silence the CKDN1A locus. | [18] |
H19 | Promotes oncogenesis in different cancer types. | Interacts with SAHH inhibiting the DNMT3B dependent DNA methylation at different genetic loci. | [19,20,21,22,23,24,25] |
HOTAIR | Overexpressed in liver, metastatic breast, lung and pancreatic tumors. | Interacts with PRC2 and LSD1 to silence genes. | [26,27,28,29,30,31,32] |
HOXA11-AS | Acts as oncogene or tumor suppressor depending on the cellular context. | Interacts with PRC2, LSD1 and DNMT1 to silence genes | [33,34] |
LED | Downregulated in p53 wild-type leukaemia. | Promotes CDKN1A transcription by acting as enhancer RNA. | [35] |
LINC-PINT | Downregulated in colorectal cancer | Interacts with PRC2 to silence genes. | [36,37,38] |
lncTCF7 | Highly expressed in hepatocellular carcinoma and it is a negative prognostic factor in glioma. | Recruits the SWI/SNF complex to activate the expression of the transcription factor TCF7. | [39] |
LUNAR1 | Upregulated in T-cell acute lymphoblastic leukemia. | Induces chromatin looping and recruits the Mediator complex to activate IGF1R transcription. | [40,41] |
MIR31HG | Deregulated in different human cancers. | Interacts with PRC2 to silence the INK4A locus. | [42] |
NBAT1 | Loss of NBAT1 is asssociated with poor clinical outcome in Neuroblastoma (NB) and breast cancer (BC). | In NB interacts with PRC2 to silence genes while in BC it interacts with PRC2 to repress its activity. | [43,44] |
SChLAP1 | Overexpressed in a subset of prostate cancers. It is critical for metastasis and predicts poor outcomes. | Inhibits the binding of the SWI/SNF chromatin remodelling to the genome. | [45] |
TARID | Deregulated in different human cancers. | Recruits the DNA demethylation regulator growth arrest and DNA damage inducible protein GADD45α to activate the transcription of the tumor suppressor gene TCF21. | [46,47,48] |
Xist | Abnormal expression associated with tumor initiation and progression. | Represses gene expression by multiple epigenetic mechanisms. | [49] |
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Morlando, M.; Fatica, A. Alteration of Epigenetic Regulation by Long Noncoding RNAs in Cancer. Int. J. Mol. Sci. 2018, 19, 570. https://doi.org/10.3390/ijms19020570
Morlando M, Fatica A. Alteration of Epigenetic Regulation by Long Noncoding RNAs in Cancer. International Journal of Molecular Sciences. 2018; 19(2):570. https://doi.org/10.3390/ijms19020570
Chicago/Turabian StyleMorlando, Mariangela, and Alessandro Fatica. 2018. "Alteration of Epigenetic Regulation by Long Noncoding RNAs in Cancer" International Journal of Molecular Sciences 19, no. 2: 570. https://doi.org/10.3390/ijms19020570