Long non-coding RNAs: The key players in glioma pathogenesis

Cancers

Volumn 7, Issue 3, 2015, Pages 1406-1424

  Mei Yee Kiang, Karrie ^a   Zhang, Xiao Qin ^a   Leung, Gilberto Ka Kit ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Biomarker; CRNDE; Glioblastoma stem cell; Glioma; Gliomagenesis; H19; HOTAIR; lncRNA; MEG3

Indexed keywords

COLORECTAL NEOPLASIA DIFFERENTIALLY EXPRESSED RNA; HOX TRANSCRIPT ANTISENSE INTERGENIC RNA; LONG UNTRANSLATED RNA; MATERNALLY EXPRESSED GENE 3 RNA; RNA H19; TUMOR MARKER; UNCLASSIFIED DRUG;

CANCER GROWTH; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER SURVIVAL; CARCINOGENESIS; CORRELATIONAL STUDY; DISEASE CLASSIFICATION; GENE REGULATORY NETWORK; GLIOMA; GLIOMA STEM CELL; HUMAN; MECHANOTRANSDUCTION; MOLECULARLY TARGETED THERAPY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; TUMOR PROMOTION;

EID: 84938489819     PISSN: None     EISSN: 20726694     Source Type: Journal    
DOI: 10.3390/cancers7030843     Document Type: Review

References (134)

1. The ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489, 57–74.
2. Derrien, T.; Johnson, R.; Bussotti, G.; Tanzer, A.; Djebali, S.; Tilgner, H.; Guernec, G.; Martin, D.; Merkel, A.; Knowles, D.G. The gencode v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression. Genome Res. 2012, 22, 1775–1789. [CrossRef] [PubMed]
3. Lipshitz, H.; Peattie, D.; Hogness, D. Novel transcripts from the ultrabithorax domain of the bithorax complex. Genes Dev. 1987, 1, 307–322. [CrossRef] [PubMed]
4. Sanchez-Elsner, T.; Gou, D.; Kremmer, E.; Sauer, F. Noncoding RNAs of trithorax response elements recruit Drosophila Ash1 to ultrabithorax. Science 2006, 311, 1118–1123. [CrossRef] [PubMed]
5. Sanchez-Herrero, E.; Akam, M. Spatially ordered transcription of regulatory DNA in the bithorax complex of Drosophila. Development 1989, 107, 321–329. [PubMed]
6. Kern, A.D.; Barbash, D.A.; Mell, J.C.; Hupalo, D.; Jensen, A. Highly constrained intergenic Drosophila ultraconserved elements are candidate ncrnas. Genome Biol. Evolut. 2015, 7, 689–698. [CrossRef] [PubMed]
7. Calin, G.A.; Liu, C.-G.; Ferracin, M.; Hyslop, T.; Spizzo, R.; Sevignani, C.; Fabbri, M.; Cimmino, A.; Lee, E.J.; Wojcik, S.E. Ultraconserved regions encoding ncrnas are altered in human leukemias and carcinomas. Cancer Cell 2007, 12, 215–229. [CrossRef] [PubMed]
8. Lipovich, L.; Johnson, R.; Lin, C.-Y. MacroRNA underdogs in a microRNA world: Evolutionary, regulatory, and biomedical significance of mammalian long non-protein-coding RNA. Biochim. Biophys. Acta 2010, 1799, 597–615. [CrossRef] [PubMed]
9. Mercer, T.R.; Dinger, M.E.; Mattick, J.S. Long non-coding RNAs: Insights into functions. Nat. Rev. Genet. 2009, 10, 155–159. [CrossRef] [PubMed]
10. Amaral, P.P.; Dinger, M.E.; Mercer, T.R.; Mattick, J.S. The eukaryotic genome as an RNA machine. Science 2008, 319, 1787–1789. [CrossRef] [PubMed]
11. Dinger, M.E.; Amaral, P.P.; Mercer, T.R.; Mattick, J.S. Pervasive transcription of the eukaryotic genome: Functional indices and conceptual implications. Brief. Funct. Genomics Proteomec. 2009, 8, 407–423. [CrossRef] [PubMed]
12. Sana, J.; Faltejskova, P.; Svoboda, M.; Slaby, O. Novel classes of non-coding RNAs and cancer. J. Transl. Med. 2012, 10, [CrossRef] [PubMed]
13. Birney, E.; Stamatoyannopoulos, J.A.; Dutta, A.; Guigó, R.; Gingeras, T.R.; Margulies, E.H.; Weng, Z.; Snyder, M.; Dermitzakis, E.T.; Thurman, R.E. Identification and analysis of functional elements in 1% of the human genome by the encode pilot project. Nature 2007, 447, 799–816. [CrossRef] [PubMed]
14. Carninci, P.; Kasukawa, T.; Katayama, S.; Gough, J.; Frith, M.; Maeda, N.; Oyama, R.; Ravasi, T.; Lenhard, B.; Wells, C. The transcriptional landscape of the mammalian genome. Science 2005, 309, 1559–1563. [PubMed]
15. Furuno, M.; Pang, K.C.; Ninomiya, N.; Fukuda, S.; Frith, M.C.; Bult, C.; Kai, C.; Kawai, J.; Carninci, P.; Hayashizaki, Y. Clusters of internally primed transcripts reveal novel long noncoding RNAs. PLoS Genet. 2006, 2, e37. [CrossRef] [PubMed]
16. Tate, M.C.; Aghi, M.K. Biology of angiogenesis and invasion in glioma. Neurotherapeutics 2009, 6, 447–457. [CrossRef] [PubMed]
17. Johnson, D.R.; O’Neill, B.P. Glioblastoma survival in the united states before and during the temozolomide era. J. Neuro-Oncol. 2012, 107, 359–364. [CrossRef] [PubMed]
18. Crespo, I.; Vital, A.L.; Gonzalez-Tablas, M.; del Carmen Patino, M.; Otero, A.; Lopes, M.C.; de Oliveira, C.; Domingues, P.; Orfao, A.; Tabernero, M.D. Molecular and genomic alterations in glioblastoma multiforme. Am. J. Pathol. 2015, 185, 1820–1833. [CrossRef] [PubMed]
19. Chan, D.; Kam, M.; Ma, B.; Ng, S.; Pang, J.; Lau, C.; Siu, D.; Ng, B.; Zhu, X.; Chen, G. Association of molecular marker o (6) methylguanine DNA methyltransferase and concomitant chemoradiotherapy with survival in southern chinese glioblastoma patients. Hong Kong Med. J. 2011, 17, 184–188. [PubMed]
20. Kaina, B.; Christmann, M. DNA repair in resistance to alkylating anticancer drugs. Int. J. Clin. Pharmacol. Ther. 2002, 40, 354–367. [CrossRef] [PubMed]
21. D’Incalci, M.; Citti, L.; Taverna, P.; Catapano, C.V. Importance of the DNA repair enzyme o 6-alkyl guanine alkyltransferase (at) in cancer chemotherapy. Cancer Treat. Rev. 1988, 15, 279–292. [CrossRef] [PubMed]
22. Stupp, R.; Mason, W.P.; van Den Bent, M.J.; Weller, M.; Fisher, B.; Taphoorn, M.J.; Belanger, K.; Brandes, A.A.; Marosi, C.; Bogdahn, U. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352, 987–996. [CrossRef] [PubMed]
23. Stupp, R.; Hegi, M.E.; Mason, W.P.; van den Bent, M.J.; Taphoorn, M.J.; Janzer, R.C.; Ludwin, S.K.; Allgeier, A.; Fisher, B.; Belanger, K. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the eortc-ncic trial. Lancet Oncol. 2009, 10, 459–466. [CrossRef]
24. Nagasubramanian, R.; Dolan, M.E. Temozolomide: Realizing the promise and potential. Curr. Opin. Oncol. 2003, 15, 412–418. [CrossRef] [PubMed]
25. Stark-Vance, V. Bevacizumab and cpt-11 in the Treatment of Relapsed Malignant Glioma. In Neuro-Oncology; Duke Univ Press: Durham, NC, USA, 2005; p. 369
26. Khasraw, M.; Ameratunga, M.; Grommes, C. Bevacizumab for the treatment of high-grade glioma: An update after phase III trials. Expert Opin. Biol. Ther. 2014, 14, 729–740. [CrossRef] [PubMed]
27. Hüttenhofer, A.; Vogel, J. Experimental approaches to identify non-coding RNAs. Nucl. Acids Res. 2006, 34, 635–646. [CrossRef] [PubMed]
28. Zhang, X.; Sun, S.; Pu, J.K.S.; Tsang, A.C.O.; Lee, D.; Man, V.O.Y.; Lui, W.M.; Wong, S.T.S.; Leung, G.K.K. Long non-coding RNA expression profiles predict clinical phenotypes in glioma. Neurobiol. Dis. 2012, 48, 1–8. [CrossRef] [PubMed]
29. Zhang, X.-Q.; Sun, S.; Lam, K.-F.; Kiang, K.M.-Y.; Pu, J.K.-S.; Ho, A.S.-W.; Lui, W.-M.; Fung, C.-F.; Wong, T.-S.; Leung, G.K.-K. A long non-coding RNA signature in glioblastoma multiforme predicts survival. Neurobiol. Dis. 2013, 58, 123–131. [CrossRef] [PubMed]
30. Geisler, S.; Coller, J. RNA in unexpected places: Long non-coding RNA functions in diverse cellular contexts. Nat. Rev. Mol. Cell Biol. 2013, 14, 699–712. [CrossRef] [PubMed]
31. Wilusz, J.E.; Sunwoo, H.; Spector, D.L. Long noncoding RNAs: Functional surprises from the RNA world. Genes Dev. 2009, 23, 1494–1504. [CrossRef] [PubMed]
32. Nagano, T.; Fraser, P. No-nonsense functions for long noncoding RNAs. Cell 2011, 145, 178–181. [CrossRef] [PubMed]
33. Zhang, X.-Q.; Leung, G.K.-K. Long non-coding RNAs in glioma: Functional roles and clinical perspectives. Neurochem. Int. 2014, 77, 78–85. [CrossRef] [PubMed]
34. Mercer, T.R.; Mattick, J.S. Structure and function of long noncoding RNAs in epigenetic regulation. Nat. Struct. Mol. Biol. 2013, 20, 300–307. [CrossRef] [PubMed]
35. Mattick, J.S.; Gagen, M.J. The evolution of controlled multitasked gene networks: The role of introns and other noncoding RNAs in the development of complex organisms. Mol. Biol. Evol. 2001, 18, 1611–1630. [CrossRef] [PubMed]
36. Khalil, A.M.; Guttman, M.; Huarte, M.; Garber, M.; Raj, A.; Morales, D.R.; Thomas, K.; Presser, A.; Bernstein, B.E.; van Oudenaarden, A. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl. Acad. Sci. USA 2009, 106, 11667–11672. [CrossRef] [PubMed]
37. Amaral, P.P.; Clark, M.B.; Gascoigne, D.K.; Dinger, M.E.; Mattick, J.S. Lncrnadb: A reference database for long noncoding RNAs. Nucl. Acids Res. 2011, 39, D146–D151. [CrossRef] [PubMed]
38. Yang, J.-H.; Li, J.-H.; Jiang, S.; Zhou, H.; Qu, L.-H. Chipbase: A database for decoding the transcriptional regulation of long non-coding RNA and microRNA genes from chip-seq data. Nucl. Acids Res. 2013, 41, D177–D187. [CrossRef] [PubMed]
39. Volders, P.-J.; Helsens, K.; Wang, X.; Menten, B.; Martens, L.; Gevaert, K.; Vandesompele, J.; Mestdagh, P. Lncipedia: A database for annotated human lncRNA transcript sequences and structures. Nucl. Acids Res. 2013, 41, D246–D251. [CrossRef] [PubMed]
40. Park, C.; Yu, N.; Choi, I.; Kim, W.; Lee, S. Lncrnator: A comprehensive resource for functional investigation of long noncoding RNAs. Bioinformatics 2014. [CrossRef] [PubMed]
41. Kaikkonen, M.U.; Lam, M.T.; Glass, C.K. Non-coding RNAs as regulators of gene expression and epigenetics. Cardiovasc. Res. 2011, 90, 430–440. [CrossRef] [PubMed]
42. Prasanth, K.V.; Spector, D.L. Eukaryotic regulatory RNAs: An answer to the “genome complexity” conundrum. Genes Dev. 2007, 21, 11–42. [CrossRef] [PubMed]
43. Shamovsky, I.; Nudler, E. Gene control by large noncoding RNAS. STKE 2006, [CrossRef] [PubMed]
44. 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. Functional demarcation of active and silent chromatin domains in human hox loci by noncoding RNAs. Cell 2007, 129, 1311–1323. [CrossRef] [PubMed]
45. 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. [CrossRef] [PubMed]
46. Jeon, Y.; Lee, J.T. Yy1 tethers xist RNA to the inactive x nucleation center. Cell 2011, 146, 119–133. [CrossRef] [PubMed]
47. Zhang, K.; Sun, X.; Zhou, X.; Han, L.; Chen, L.; Shi, Z.; Zhang, A.; Ye, M.; Wang, Q.; Liu, C. Long non-coding RNA hotair promotes glioblastoma cell cycle progression in an ezh2 dependent manner. Oncotarget 2015, 6, [PubMed]
48. Bian, E.B.; Li, J.; Xie, Y.S.; Zong, G.; Li, J.; Zhao, B. LncRNAs: New players in gliomas, with special emphasis on the interaction of lncRNAs with ezh2. J. Cell. Physiol. 2015, 230, 496–503. [CrossRef] [PubMed]
49. Cabili, M.N.; Trapnell, C.; Goff, L.; Koziol, M.; Tazon-Vega, B.; Regev, A.; Rinn, J.L. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 2011, 25, 1915–1927. [CrossRef] [PubMed]
50. Ruiz-Orera, J.; Messeguer, X.; Subirana, J.A.; Alba, M.M. Long non-coding RNAS as a source of new peptides. eLife 2014, 3, e03523. [CrossRef] [PubMed]
51. Van Heesch, S.; van Iterson, M.; Jacobi, J.; Boymans, S.; Essers, P.B.; de Bruijn, E.; Hao, W.; MacInnes, A.W.; Cuppen, E.; Simonis, M. Extensive localization of long noncoding RNAs to the cytosol and mono-and polyribosomal complexes. Genome Biol. 2014, [CrossRef] [PubMed]
52. Salmena, L.; Poliseno, L.; Tay, Y.; Kats, L.; Pandolfi, P.P. A ceRNA hypothesis: The rosetta stone of a hidden RNA language? Cell 2011, 146, 353–358. [CrossRef] [PubMed]
53. Poliseno, L.; Salmena, L.; Zhang, J.; Carver, B.; Haveman, W.J.; Pandolfi, P.P. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 2010, 465, 1033–1038. [CrossRef] [PubMed]
54. Franco-Zorrilla, J.M.; Valli, A.; Todesco, M.; Mateos, I.; Puga, M.I.; Rubio-Somoza, I.; Leyva, A.; Weigel, D.; García, J.A.; Paz-Ares, J. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 2007, 39, 1033–1037. [CrossRef] [PubMed]
55. Cazalla, D.; Yario, T.; Steitz, J.A. Down-regulation of a host microRNA by a herpesvirus saimiri noncoding RNA. Science 2010, 328, 1563–1566. [CrossRef] [PubMed]
56. Wang, J.; Liu, X.; Wu, H.; Ni, P.; Gu, Z.; Qiao, Y.; Chen, N.; Sun, F.; Fan, Q. Creb up-regulates long non-coding RNA, hulc expression through interaction with microRNA-372 in liver cancer. Nucl. Acids Res. 2010, 38, 5366–5383. [CrossRef] [PubMed]
57. Cesana, M.; Cacchiarelli, D.; Legnini, I.; Santini, T.; Sthandier, O.; Chinappi, M.; Tramontano, A.; Bozzoni, I. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 2011, 147, 358–369. [CrossRef] [PubMed]
58. Mercer, T.R.; Dinger, M.E.; Sunkin, S.M.; Mehler, M.F.; Mattick, J.S. Specific expression of long noncoding RNAs in the mouse brain. Proc. Natl. Acad. Sci. USA 2008, 105, 716–721. [CrossRef] [PubMed]
59. Ravasi, T.; Suzuki, H.; Pang, K.C.; Katayama, S.; Furuno, M.; Okunishi, R.; Fukuda, S.; Ru, K.; Frith, M.C.; Gongora, M.M. Experimental validation of the regulated expression of large numbers of non-coding RNAs from the mouse genome. Genome Res. 2006, 16, 11–19. [CrossRef] [PubMed]
60. Qureshi, I.A.; Mattick, J.S.; Mehler, M.F. Long non-coding RNAs in nervous system function and disease. Brain Res. 2010, 1338, 20–35. [CrossRef] [PubMed]
61. Mehler, M.F.; Mattick, J.S. Noncoding RNAs and RNA editing in brain development, functional diversification, and neurological disease. Physiol. Rev. 2007, 87, 799–823. [CrossRef] [PubMed]
62. Taft, R.J.; Pang, K.C.; Mercer, T.R.; Dinger, M.; Mattick, J.S. Non-coding RNAs: Regulators of disease. J. Pathol. 2010, 220, 126–139. [CrossRef] [PubMed]
63. Mehler, M.F.; Mattick, J.S. Non-coding RNAs in the nervous system. J. Physiol. 2006, 575, 333–341. [CrossRef] [PubMed]
64. Guttman, M.; Amit, I.; Garber, M.; French, C.; Lin, M.F.; Feldser, D.; Huarte, M.; Zuk, O.; Carey, B.W.; Cassady, J.P. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009, 458, 223–227. [CrossRef] [PubMed]
65. Mercer, T.R.; Qureshi, I.A.; Gokhan, S.; Dinger, M.E.; Li, G.; Mattick, J.S.; Mehler, M.F. Long noncoding RNAs in neuronal-glial fate specification and oligodendrocyte lineage maturation. BMC Neurosci. 2010, 11, [CrossRef] [PubMed]
66. Sauvageau, M.; Goff, L.A.; Lodato, S.; Bonev, B.; Groff, A.F.; Sanchez-Gomez, D.B.; Gerhardinger, C.; Hacisuleyman, E.; Li, E.; Spence, M. Multiple knockout mouse models reveal lincRNAs are required for life and brain development. eLife 2013, 2, e01749. [CrossRef] [PubMed]
67. Ripoche, M.-A.; Kress, C.; Poirier, F.; Dandolo, L. Deletion of the H19 transcription unit reveals the existence of a putative imprinting control element. Genes Dev. 1997, 11, 1596–1604. [CrossRef] [PubMed]
68. Gordon, F.E.; Nutt, C.L.; Cheunsuchon, P.; Nakayama, Y.; Provencher, K.A.; Rice, K.A.; Zhou, Y.; Zhang, X.; Klibanski, A. Increased expression of angiogenic genes in the brains of mouse meg3-null embryos. Endocrinology 2010, 151, 2443–2452. [CrossRef] [PubMed]
69. Zhang, B.; Arun, G.; Mao, Y.S.; Lazar, Z.; Hung, G.; Bhattacharjee, G.; Xiao, X.; Booth, C.J.; Wu, J.; Zhang, C. The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult. Cell Rep. 2012, 2, 111–123. [CrossRef] [PubMed]
70. Nakagawa, S.; Naganuma, T.; Shioi, G.; Hirose, T. Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice. J. Cell Biol. 2011, 193, 31–39. [CrossRef] [PubMed]
71. Amaral, P.P.; Neyt, C.; Wilkins, S.J.; Askarian-Amiri, M.E.; Sunkin, S.M.; Perkins, A.C.; Mattick, J.S. Complex architecture and regulated expression of the sox2ot locus during vertebrate development. RNA 2009, 15, 2013–2027. [CrossRef] [PubMed]
72. Tochitani, S.; Hayashizaki, Y. Nkx2. 2 antisense RNA overexpression enhanced oligodendrocytic differentiation. Biochem. Biophys. Res. Commun. 2008, 372, 691–696. [CrossRef] [PubMed]
73. Johnstone, K.A.; DuBose, A.J.; Futtner, C.R.; Elmore, M.D.; Brannan, C.I.; Resnick, J.L. A human imprinting centre demonstrates conserved acquisition but diverged maintenance of imprinting in a mouse model for angelman syndrome imprinting defects. Hum. Mol. Genet. 2006, 15, 393–404. [CrossRef] [PubMed]
74. Sutherland, H.F.; Wadey, R.; McKie, J.M.; Taylor, C.; Atif, U.; Johnstone, K.A.; Halford, S.; Kim, U.-J.; Goodship, J.; Baldini, A. Identification of a novel transcript disrupted by a balanced translocation associated with digeorge syndrome. Am. J. Hum. Genet. 1996, 59, [PubMed]
75. Willingham, A.; Orth, A.; Batalov, S.; Peters, E.; Wen, B.; Aza-Blanc, P.; Hogenesch, J.; Schultz, P. A strategy for probing the function of noncoding RNAs finds a repressor of nfat. Science 2005, 309, 1570–1573. [CrossRef] [PubMed]
76. Faghihi, M.A.; Modarresi, F.; Khalil, A.M.; Wood, D.E.; Sahagan, B.G.; Morgan, T.E.; Finch, C.E.; Laurent, G.S., III; Kenny, P.J.; Wahlestedt, C. Expression of a noncoding RNA is elevated in Alzheimer’s disease and drives rapid feed-forward regulation of -secretase. Nat. Med. 2008, 14, 723–730. [CrossRef] [PubMed]
77. Mus, E.; Hof, P.R.; Tiedge, H. Dendritic bc200 RNA in aging and in Alzheimer’s disease. Proc. Natl. Acad. Sci. USA 2007, 104, 10679–10684. [CrossRef] [PubMed]
78. Tsunoda, I.; Fujinami, R.S. Neuropathogenesis of theiler’s murine encephalomyelitis virus infection, an animal model for multiple sclerosis. J. Neuroimmune Pharmacol. 2010, 5, 355–369. [CrossRef] [PubMed]
79. Müller, S.; Zirkel, D.; Westphal, M.; Zumkeller, W. Genomic imprinting of IGF2 and H19 in human meningiomas. Eur. J. Cancer 2000, 36, 651–655. [CrossRef]
80. Chubb, J.; Bradshaw, N.; Soares, D.; Porteous, D.; Millar, J. The disc locus in psychiatric illness. Mol. Psychiatry 2008, 13, 36–64. [CrossRef] [PubMed]
81. Millar, J.K.; Wilson-Annan, J.C.; Anderson, S.; Christie, S.; Taylor, M.S.; Semple, C.A.; Devon, R.S.; St Clair, D.M.; Muir, W.J.; Blackwood, D.H. Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum. Mol. Genet. 2000, 9, 1415–1423. [CrossRef] [PubMed]
82. Williams, J.M.; Beck, T.F.; Pearson, D.M.; Proud, M.B.; Cheung, S.W.; Scott, D.A. A 1q42 deletion involving DISC1, DISC2, and TSNAX in an autism spectrum disorder. Am. J. Med. Genet. Part A 2009, 149, 1758–1762. [CrossRef] [PubMed]
83. Brunner, A.L.; Beck, A.H.; Edris, B.; Sweeney, R.T.; Zhu, S.X.; Li, R.; Montgomery, K.; Varma, S.; Gilks, T.; Guo, X. Transcriptional profiling of long non-coding RNAs and novel transcribed regions across a diverse panel of archived human cancers. Genome Biol. 2012, 13, R75. [CrossRef] [PubMed]
84. Gibb, E.A.; Vucic, E.A.; Enfield, K.S.; Stewart, G.L.; Lonergan, K.M.; Becker-Santos, D.D.; Kennett, J.Y.; MacAulay, C.E.; Lam, S.; Brown, C.J. Human cancer long non-coding RNA transcriptomes. PLoS ONE 2011, 6, e25915. [CrossRef] [PubMed]
85. Han, L.; Zhang, K.; Shi, Z.; Zhang, J.; Zhu, J.; Zhu, S.; Zhang, A.; Jia, Z.; Wang, G.; Yu, S. LncRNA profile of glioblastoma reveals the potential role of lncRNAs in contributing to glioblastoma pathogenesis. Int. J. Oncol. 2012, 40, 2004–2012. [PubMed]
86. Pastori, C.; Kapranov, P.; Penas, C.; Peschansky, V.; Volmar, C.-H.; Sarkaria, J.N.; Bregy, A.; Komotar, R.; Laurent, G.S.; Ayad, N.G. The bromodomain protein brd4 controls hotair, a long noncoding RNA essential for glioblastoma proliferation. Proc. Natl. Acad. Sci. USA 2015, 112, 8326–8331. [CrossRef] [PubMed]
87. Vital, A.L.; Tabernero, M.D.; Castrillo, A.; Rebelo, O.; Tão, H.; Gomes, F.; Nieto, A.B.; Oliveira, C.R.; Lopes, M.C.; Orfao, A. Gene expression profiles of human glioblastomas are associated with both tumor cytogenetics and histopathology. Neuro Oncol. 2010, 12, 991–1003. [CrossRef] [PubMed]
88. Guo, H.; Wu, L.; Yang, Q.; Ye, M.; Zhu, X. Functional linc-POU3F3 is overexpressed and contributes to tumorigenesis in glioma. Gene 2015, 554, 114–119. [CrossRef] [PubMed]
89. 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. [CrossRef] [PubMed]
90. Shi, Y.; Wang, Y.; Luan, W.; Wang, P.; Tao, T.; Zhang, J.; Qian, J.; Liu, N.; You, Y. Long non-coding RNA H19 promotes glioma cell invasion by deriving mir-675. PLoS ONE 2014, 9, e86295. [CrossRef] [PubMed]
91. Ma, K.-X.; Wang, H.-J.; Li, X.-R.; Li, T.; Su, G.; Yang, P.; Wu, J.-W. Long noncoding RNA Malat1 associates with the malignant status and poor prognosis in glioma. Tumor. Biol. 2015, 36, 3355–3359. [CrossRef] [PubMed]
92. Baritaki, S.; Chatzinikola, A.M.; Vakis, A.F.; Soulitzis, N.; Karabetsos, D.A.; Neonakis, I.; Bonavida, B.; Spandidos, D.A. YY1 over-expression in human brain gliomas and meningiomas correlates with TGF-1, IGF-1 and FGF-2 mRNA levels. Cancer Investig. 2009, 27, 184–192. [CrossRef] [PubMed]
93. Palmieri, D.; Chambers, A.F.; Felding-Habermann, B.; Huang, S.; Steeg, P.S. The biology of metastasis to a sanctuary site. Clin. Cancer Res. 2007, 13, 1656–1662. [CrossRef] [PubMed]
94. 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. Long non-coding RNA hotair reprograms chromatin state to promote cancer metastasis. Nature 2010, 464, 1071–1076. [CrossRef] [PubMed]
95. Li, R.; Qian, J.; Wang, Y.Y.; Zhang, J.X.; You, Y.P. Long noncoding RNA profiles reveal three molecular subtypes in glioma. CNS Neurosci. Ther. 2014, 20, 339–343. [CrossRef] [PubMed]
96. Zhang, J.-X.; Han, L.; Bao, Z.-S.; Wang, Y.-Y.; Chen, L.-Y.; Yan, W.; Yu, S.-Z.; Pu, P.-Y.; Liu, N.; You, Y.-P. Hotair, a cell cycle-associated long noncoding RNA and a strong predictor of survival, is preferentially expressed in classical and mesenchymal glioma. Neuro Oncol. 2013, 15, 1595–1603. [CrossRef] [PubMed]
97. Bao, S.; Wu, Q.; McLendon, R.E.; Hao, Y.; Shi, Q.; Hjelmeland, A.B.; Dewhirst, M.W.; Bigner, D.D.; Rich, J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444, 756–760. [CrossRef] [PubMed]
98. Galli, R.; Binda, E.; Orfanelli, U.; Cipelletti, B.; Gritti, A.; de Vitis, S.; Fiocco, R.; Foroni, C.; Dimeco, F.; Vescovi, A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004, 64, 7011–7021. [CrossRef] [PubMed]
99. Cheng, L.; Bao, S.; Rich, J.N. Potential therapeutic implications of cancer stem cells in glioblastoma. Biochem. Pharmacol. 2010, 80, 654–665. [CrossRef] [PubMed]
100. Zhang, X.; Kiang, K.M.-Y.; Zhang, G.P.-D.; Leung, G.K.K. Long non-coding RNAs dysregulation and function in glioblastoma stem cells. Non-Coding RNA 2015, 1, 69–86. [CrossRef]
101. Wang, P.; Ren, Z.; Sun, P. Overexpression of the long non-coding RNA meg3 impairs in vitro glioma cell proliferation. J. Cell. Biochem. 2012, 113, 1868–1874. [CrossRef] [PubMed]
102. Benetatos, L.; Vartholomatos, G.; Hatzimichael, E. Meg3 imprinted gene contribution in tumorigenesis. Int. J. Cancer 2011, 129, 773–779. [CrossRef] [PubMed]
103. Wang, Y.; Wang, Y.; Li, J.; Zhang, Y.; Yin, H.; Han, B. Crnde, a long-noncoding RNA, promotes glioma cell growth and invasion through mtor signaling. Cancer Lett. 2015. [CrossRef]
104. Trojan, L.; Kopinski, P.; Mazurek, A.; Chyczewski, L.; Ly, A.; Jarocki, P.; Niklinski, J.; Shevelev, A.; Trzos, R.; Pan, Y. Igf-I triple helix gene therapy of rat and human gliomas. Rocz. Akad. Med. w Bialymstoku (1995) 2002, 48, 18–27.
105. Yao, Y.; Ma, J.; Xue, Y.; Wang, P.; Li, Z.; Liu, J.; Chen, L.; Xi, Z.; Teng, H.; Wang, Z. Knockdown of long non-coding RNA XIST exerts tumor-suppressive functions in human glioblastoma stem cells by up-regulating miR-152. Cancer Lett. 2015, 359, 75–86. [CrossRef] [PubMed]
106. Ma, M.; Li, C.; Zhang, Y.; Weng, M.; Zhang, M.; Qin, Y.; Gong, W.; Quan, Z. Long non-coding RNA hotair, a c-Myc activated driver of malignancy, negatively regulates miRNA-130a in gallbladder cancer. Mol. Cancer 2014, 13, [CrossRef] [PubMed]
107. Katherine, K. Expression data from paediatric ependymoma short-term cell cultures. Unpublished study, 2013. The raw microarray data is accesible at public NCBI GEO database. Accession no. GSE45437.
108. Liu, Q.; Sun, S.; Yu, W.; Jiang, J.; Zhuo, F.; Qiu, G.; Xu, S.; Jiang, X. Altered expression of long non-coding RNAs during genotoxic stress-induced cell death in human glioma cells. J. Neuro Oncol. 2015, 122, 283–292. [CrossRef] [PubMed]
109. Qin, X.; Yao, J.; Geng, P.; Fu, X.; Xue, J.; Zhang, Z. LncRNA TSLC1-AS1 is a novel tumor suppressor in glioma. Int. J. Clin. Exp. Pathol. 2014, 7, 3065. [PubMed]
110. Wang, P.; Liu, Y.-H.; Yao, Y.-L.; Li, Z.; Li, Z.-Q.; Ma, J.; Xue, Y.-X. Long non-coding RNA CASC2 suppresses malignancy in human gliomas by miR-21. Cell. Signal. 2015, 27, 275–282. [CrossRef] [PubMed]
111. Hao, Y.; Crenshaw, T.; Moulton, T.; Newcomb, E.; Tycko, B. Tumour-suppressor activity of H19 RNA. Nature 1993, 365, 764–767. [CrossRef] [PubMed]
112. Brannan, C.I.; Dees, E.C.; Ingram, R.S.; Tilghman, S.M. The product of the H19 gene may function as an RNA. Mol. Cell. Biol. 1990, 10, 28–36. [PubMed]
113. Tanos, V.; Ariel, I.; Prus, D.; De-Groot, N.; Hochberg, A. H19 and IGF2 gene expression in human normal, hyperplastic, and malignant endometrium. Int. J. Gynecol. Cancer 2004, 14, 521–525. [CrossRef] [PubMed]
114. Kondo, M.; Suzuki, H.; Ueda, R.; Osada, H.; Takagi, K.; Takahashi, T. Frequent loss of imprinting of the H19 gene is often associated with its overexpression in human lung cancers. Oncogene 1995, 10, 1193–1198. [PubMed]
115. Keniry, A.; Oxley, D.; Monnier, P.; Kyba, M.; Dandolo, L.; Smits, G.; Reik, W. The H19 lincRNA is a developmental reservoir of miR-675 that suppresses growth and Igf1r. Nat. Cell Biol. 2012, 14, 659–665. [CrossRef] [PubMed]
116. Poirier, F.; Chan, C.; Timmons, P.; Robertson, E.; Evans, M.; Rigby, P. The murine H19 gene is activated during embryonic stem cell differentiation in vitro and at the time of implantation in the developing embryo. Development 1991, 113, 1105–1114. [PubMed]
117. Venkatraman, A.; He, X.C.; Thorvaldsen, J.L.; Sugimura, R.; Perry, J.M.; Tao, F.; Zhao, M.; Christenson, M.K.; Sanchez, R.; Jaclyn, Y.Y. Maternal imprinting at the H19-IGF2 locus maintains adult haematopoietic stem cell quiescence. Nature 2013, 500, 345–349. [CrossRef] [PubMed]
118. Yin, Y.; Wang, H.; Liu, K.; Wang, F.; Ye, X.; Liu, M.; Xiang, R.; Liu, N.; Liu, L. Knockdown of H19 enhances differentiation capacity to epidermis of parthenogenetic embryonic stem cells. Curr. Mol. Med. 2014, 14, 737–748. [CrossRef] [PubMed]
119. Zhou, X.; Ren, Y.; Zhang, J.; Zhang, C.; Zhang, K.; Han, L.; Kong, L.; Wei, J.; Chen, L.; Yang, J. Hotair is a therapeutic target in glioblastoma. Oncotarget 2015, 6, 8353–8365. [PubMed]
120. Kogo, R.; Shimamura, T.; Mimori, K.; Kawahara, K.; Imoto, S.; Sudo, T.; Tanaka, F.; Shibata, K.; Suzuki, A.; Komune, S. Long noncoding RNA hotair regulates polycomb-dependent chromatin modification and is associated with poor prognosis in colorectal cancers. Cancer Res. 2011, 71, 6320–6326. [CrossRef] [PubMed]
121. Hong, Y.; Ho, K.S.; Eu, K.W.; Cheah, P.Y. A susceptibility gene set for early onset colorectal cancer that integrates diverse signaling pathways: Implication for tumorigenesis. Clin. Cancer Res. 2007, 13, 1107–1114. [CrossRef] [PubMed]
122. Sabates-Bellver, J.; van der Flier, L.G.; de Palo, M.; Cattaneo, E.; Maake, C.; Rehrauer, H.; Laczko, E.; Kurowski, M.A.; Bujnicki, J.M.; Menigatti, M. Transcriptome profile of human colorectal adenomas. Mol. Cancer Res. 2007, 5, 1263–1275. [CrossRef] [PubMed]
123. Graham, L.D.; Pedersen, S.K.; Brown, G.S.; Ho, T.; Kassir, Z.; Moynihan, A.T.; Vizgoft, E.K.; Dunne, R.; Pimlott, L.; Young, G.P. Colorectal neoplasia differentially expressed (crnde), a novel gene with elevated expression in colorectal adenomas and adenocarcinomas. Genes Cancer 2011, 2, 829–840. [CrossRef] [PubMed]
124. Payton, J.E.; Grieselhuber, N.R.; Chang, L.-W.; Murakami, M.; Geiss, G.K.; Link, D.C.; Nagarajan, R.; Watson, M.A.; Ley, T.J. High throughput digital quantification of mRNA abundance in primary human acute myeloid leukemia samples. J. Clin. Investig. 2009, 119, 1714. [CrossRef] [PubMed]
125. Eckerle, S.; Brune, V.; Döring, C.; Tiacci, E.; Bohle, V.; Sundström, C.; Kodet, R.; Paulli, M.; Falini, B.; Klapper, W. Gene expression profiling of isolated tumour cells from anaplastic large cell lymphomas: Insights into its cellular origin, pathogenesis and relation to hodgkin lymphoma. Leukemia 2009, 23, 2129–2138. [CrossRef] [PubMed]
126. Ellis, B.C.; Molloy, P.L.; Graham, L.D. CRNDE: A long non-coding RNA involved in cancer, neurobiology, and development. Front. Genet. 2012, [CrossRef] [PubMed]
127. Guttman, M.; Donaghey, J.; Carey, B.W.; Garber, M.; Grenier, J.K.; Munson, G.; Young, G.; Lucas, A.B.; Ach, R.; Bruhn, L. LincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 2011, 477, 295–300. [CrossRef] [PubMed]
128. Mazzoleni, S.; Politi, L.S.; Pala, M.; Cominelli, M.; Franzin, A.; Sergi, L.S.; Falini, A.; de Palma, M.; Bulfone, A.; Poliani, P.L. Epidermal growth factor receptor expression identifies functionally and molecularly distinct tumor-initiating cells in human glioblastoma multiforme and is required for gliomagenesis. Cancer Res. 2010, 70, 7500–7513. [CrossRef] [PubMed]
129. Jin, X.; Yin, J.; Kim, S.-H.; Sohn, Y.-W.; Beck, S.; Lim, Y.C.; Nam, D.-H.; Choi, Y.-J.; Kim, H. EGFR-AKT-Smad signaling promotes formation of glioma stem-like cells and tumor angiogenesis by ID3-driven cytokine induction. Cancer Res. 2011, 71, 7125–7134. [CrossRef] [PubMed]
130. Ducray, F.; Idbaih, A.; de Reyniès, A.; Bièche, I.; Thillet, J.; Mokhtari, K.; Lair, S.; Marie, Y.; Paris, S.; Vidaud, M. Anaplastic oligodendrogliomas with 1p19q codeletion have a proneural gene expression profile. Mol. Cancer 2008, 7, [CrossRef] [PubMed]
131. Zhang, X.; Zhou, Y.; Mehta, K.R.; Danila, D.C.; Scolavino, S.; Johnson, S.R.; Klibanski, A. A pituitary-derived meg3 isoform functions as a growth suppressor in tumor cells. J. Clin. Endocrinol. Metab. 2003, 88, 5119–5126. [CrossRef] [PubMed]
132. Zhou, Y.; Zhong, Y.; Wang, Y.; Zhang, X.; Batista, D.L.; Gejman, R.; Ansell, P.J.; Zhao, J.; Weng, C.; Klibanski, A. Activation of p53 by MEG3 non-coding RNA. J. Biol. Chem. 2007, 282, 24731–24742. [CrossRef] [PubMed]
133. Tinzl, M.; Marberger, M.; Horvath, S.; Chypre, C. DD3 PCA3 RNA analysis in urine—A new perspective for detecting prostate cancer. Eur. Urol. 2004, 46, 182–187. [CrossRef] [PubMed]
134. Hessels, D.; Gunnewiek, J.M.K.; van Oort, I.; Karthaus, H.F.; van Leenders, G.J.; van Balken, B.; Kiemeney, L.A.; Witjes, J.A.; Schalken, J.A. DD3 PCA3-based molecular urine analysis for the diagnosis of prostate cancer. Eur. Urol. 2003, 44, 8–16. [CrossRef]