Long non-coding RNAs in normal and malignant hematopoiesis

Oncotarget

Volumn 7, Issue 31, 2016, Pages 50666-50681

  Nobili, Lucia ^a   Lionetti, Marta ^a   Neri, Antonino ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Hematological malignancies; Hematopoiesis; Long noncoding RNAs; Transcriptional regulation; Translation regulation

Indexed keywords

LONG UNTRANSLATED RNA; NOTCH1 RECEPTOR; RNA H19; TUMOR MARKER;

ANRIL GENE; APOPTOSIS; BGL3 GENE; BONE MARROW CELL; CARCINOGENESIS; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SPECIFICITY; DLEU1 GENE; DLEU2 GENE; ERYTHROID CELL; GAS5 GENE; GENE EXPRESSION; GENETIC REGULATION; H19 GENE; HEMATOLOGIC MALIGNANCY; HEMATOPOIESIS; HUMAN; INTERACTIONS WITH RNA; IRAIN GENE; LYMPHOID CELL; MALAT1 GENE; MEG3 GENE; MYELOPROLIFERATIVE DISORDER; NONHUMAN; NOTCH1 GENE; PATHOGENESIS; REVIEW; RNA DEGRADATION; RNA GENE; RNA SPLICING; TUG1 GENE; ANIMAL; GENETICS; HEMATOLOGIC DISEASE; MOUSE; PROGNOSIS;

ANIMALS; BIOMARKERS, TUMOR; CELL DIFFERENTIATION; HEMATOLOGIC NEOPLASMS; HEMATOPOIESIS; HUMANS; MICE; PROGNOSIS; RNA, LONG NONCODING;

EID: 84981357163     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.9308     Document Type: Review

References (117)

1. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, Kuehn MS, Taylor CM, Neph S, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature. 2007; 447:799-816.
2. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, Xue C, Marinov GK, Khatun J, et al. Landscape of transcription in human cells. Nature. 2012; 489:101-108.
3. Fabian MR, and Sonenberg N. The mechanics of miRNAmediated gene silencing: a look under the hood of miRISC. Nature structural & molecular biology. 2012; 19:586-593.
4. Kong YW, Ferland-McCollough D, Jackson TJ, and Bushell M. microRNAs in cancer management. The Lancet Oncology. 2012; 13:e249-258.
5. Berindan-Neagoe I, Monroig Pdel C, Pasculli B, and Calin GA. MicroRNAome genome: a treasure for cancer diagnosis and therapy. CA: a cancer journal for clinicians. 2014; 64:311-336.
6. Garzon R, Marcucci G, and Croce CM. Targeting microRNAs in cancer: rationale, strategies and challenges. Nature reviews Drug discovery. 2010; 9:775-789.
7. Lawrie CH. MicroRNAs in hematological malignancies. Blood reviews. 2013; 27:143-154.
8. Amodio N, Rossi M, Raimondi L, Pitari MR, Botta C, Tagliaferri P, and Tassone P. miR-29s: a family of epimiRNAs with therapeutic implications in hematologic malignancies. Oncotarget. 2015; 6:12837-12861. doi: 10.18632/oncotarget.3805.
9. Kelley D, and Rinn J. Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome biology. 2012; 13:R107.
10. Johnsson P, Lipovich L, Grander D, and Morris KV. Evolutionary conservation of long non-coding RNAs; sequence, structure, function. Biochimica et biophysica acta. 2014; 1840:1063-1071.
11. Diederichs S. The four dimensions of noncoding RNA conservation. Trends in genetics: TIG. 2014; 30:121-123.
12. Smith MA, Gesell T, Stadler PF, and Mattick JS. Widespread purifying selection on RNA structure in mammals. Nucleic acids research. 2013; 41:8220-8236.
13. Hauptman N, and Glavac D. Long non-coding RNA in cancer. International journal of molecular sciences. 2013; 14:4655-4669.
14. Ponting CP, Oliver PL, and Reik W. Evolution and functions of long noncoding RNAs. Cell. 2009; 136:629-641.
15. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, and Rinn JL. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes & development. 2011; 25:1915-1927.
16. Mercer TR, and Mattick JS. Structure and function of long noncoding RNAs in epigenetic regulation. Nature structural & molecular biology. 2013; 20:300-307.
17. Volders PJ, Verheggen K, Menschaert G, Vandepoele K, Martens L, Vandesompele J, and Mestdagh P. An update on LNCipedia: a database for annotated human lncRNA sequences. Nucleic acids research. 2015; 43:D174-180.
18. Wang KC, and Chang HY. Molecular mechanisms of long noncoding RNAs. Molecular cell. 2011; 43:904-914.
19. Lee JT. Epigenetic regulation by long noncoding RNAs. Science (New York, NY). 2012; 338:1435-1439.
20. Wapinski O, and Chang HY. Long noncoding RNAs and human disease. Trends in cell biology. 2011; 21:354-361.
21. Hung T, and Chang HY. Long noncoding RNA in genome regulation: prospects and mechanisms. RNA biology. 2010; 7:582-585.
22. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, and Pandolfi PP. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature. 2010; 465:1033-1038.
23. Geisler S, and Coller J. RNA in unexpected places: long non-coding RNA functions in diverse cellular contexts. Nature reviews Molecular cell biology. 2013; 14:699-712.
24. Ling H, Vincent K, Pichler M, Fodde R, Berindan-Neagoe I, Slack FJ, and Calin GA. Junk DNA and the long noncoding RNA twist in cancer genetics. Oncogene. 2015.
25. Yang G, Lu X, and Yuan L. LncRNA: a link between RNA and cancer. Biochimica et biophysica acta. 2014; 1839:1097-1109.
26. Wagner LA, Christensen CJ, Dunn DM, Spangrude GJ, Georgelas A, Kelley L, Esplin MS, Weiss RB, and Gleich GJ. EGO, a novel, noncoding RNA gene, regulates eosinophil granule protein transcript expression. Blood. 2007; 109:5191-5198.
27. Zhang X, Lian Z, Padden C, Gerstein MB, Rozowsky J, Snyder M, Gingeras TR, Kapranov P, Weissman SM, and Newburger PE. A myelopoiesis-associated regulatory intergenic noncoding RNA transcript within the human HOXA cluster. Blood. 2009; 113:2526-2534.
28. Aoki K, Harashima A, Sano M, Yokoi T, Nakamura S, Kibata M, and Hirose T. A thymus-specific noncoding RNA, Thy-ncR1, is a cytoplasmic riboregulator of MFAP4 mRNA in immature T-cell lines. BMC molecular biology. 2010; 11:99.
29. Hu W, Yuan B, Flygare J, and Lodish HF. Long noncoding RNA-mediated anti-apoptotic activity in murine erythroid terminal differentiation. Genes & development. 2011; 25:2573-2578.
30. Han BW, and Chen YQ. Potential pathological and functional links between long noncoding RNAs and hematopoiesis. Science signaling. 2013; 6:re5.
31. Yu W, Gius D, Onyango P, Muldoon-Jacobs K, Karp J, Feinberg AP, and Cui H. Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA. Nature. 2008; 451:202-206.
32. Yildirim E, Kirby JE, Brown DE, Mercier FE, Sadreyev RI, Scadden DT, and Lee JT. Xist RNA is a potent suppressor of hematologic cancer in mice. Cell. 2013; 152:727-742.
33. Alvarez-Dominguez JR, Hu W, Yuan B, Shi J, Park SS, Gromatzky AA, van Oudenaarden A, and Lodish HF. Global discovery of erythroid long noncoding RNAs reveals novel regulators of red cell maturation. Blood. 2014; 123:570-581.
34. Paralkar VR, Mishra T, Luan J, Yao Y, Kossenkov AV, Anderson SM, Dunagin M, Pimkin M, Gore M, Sun D, Konuthula N, Raj A, An X, et al. Lineage and species-specific long noncoding RNAs during erythromegakaryocytic development. Blood. 2014; 123:1927-1937.
35. Ebralidze AK, Guibal FC, Steidl U, Zhang P, Lee S, Bartholdy B, Jorda MA, Petkova V, Rosenbauer F, Huang G, Dayaram T, Klupp J, O'Brien KB, et al. PU.1 expression is modulated by the balance of functional sense and antisense RNAs regulated by a shared cis-regulatory element. Genes & development. 2008; 22:2085-2092.
36. Dahl R, Walsh JC, Lancki D, Laslo P, Iyer SR, Singh H, and Simon MC. Regulation of macrophage and neutrophil cell fates by the PU.1:C/EBPalpha ratio and granulocyte colony-stimulating factor. Nature immunology. 2003; 4:1029-1036.
37. Zhang X, Weissman SM, and Newburger PE. Long intergenic non-coding RNA HOTAIRM1 regulates cell cycle progression during myeloid maturation in NB4 human promyelocytic leukemia cells. RNA biology. 2014; 11:777-787.
38. Pang KC, Dinger ME, Mercer TR, Malquori L, Grimmond SM, Chen W, and Mattick JS. Genome-wide identification of long noncoding RNAs in CD8+ T cells. Journal of immunology (Baltimore, Md: 1950). 2009; 182:7738-7748.
39. Sharma S, Findlay GM, Bandukwala HS, Oberdoerffer S, Baust B, Li Z, Schmidt V, Hogan PG, Sacks DB, and Rao A. Dephosphorylation of the nuclear factor of activated T cells (NFAT) transcription factor is regulated by an RNAprotein scaffold complex. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108:11381-11386.
40. Zhang CC, Kaba M, Ge G, Xie K, Tong W, Hug C, and Lodish HF. Angiopoietin-like proteins stimulate ex vivo expansion of hematopoietic stem cells. Nature medicine. 2006; 12:240-245.
41. Vigneau S, Rohrlich PS, Brahic M, and Bureau JF. Tmevpg1, a candidate gene for the control of Theiler's virus persistence, could be implicated in the regulation of gamma interferon. Journal of virology. 2003; 77:5632-5638.
42. Collier SP, Collins PL, Williams CL, Boothby MR, and Aune TM. Cutting edge: influence of Tmevpg1, a long intergenic noncoding RNA, on the expression of Ifng by Th1 cells. Journal of immunology (Baltimore, Md: 1950). 2012; 189:2084-2088.
43. Gomez JA, Wapinski OL, Yang YW, Bureau JF, Gopinath S, Monack DM, Chang HY, Brahic M, and Kirkegaard K. The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-gamma locus. Cell. 2013; 152:743-754.
44. Ranzani V, and Rossetti G. The long intergenic noncoding RNA landscape of human lymphocytes highlights the regulation of T cell differentiation by linc-MAF-4. 2015; 16:318-325.
45. Eis PS, Tam W, Sun L, Chadburn A, Li Z, Gomez MF, Lund E, and Dahlberg JE. Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102:3627-3632.
46. Tam W. Identification and characterization of human BIC, a gene on chromosome 21 that encodes a noncoding RNA. Gene. 2001; 274:157-167.
47. Elton TS, Selemon H, Elton SM, and Parinandi NL. Regulation of the MIR155 host gene in physiological and pathological processes. Gene. 2013; 532:1-12.
48. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, Lin C, Socci ND, Hermida L, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007; 129:1401-1414.
49. Calin GA, Liu CG, Ferracin M, Hyslop T, Spizzo R, Sevignani C, Fabbri M, Cimmino A, Lee EJ, Wojcik SE, Shimizu M, Tili E, Rossi S, et al. Ultraconserved regions encoding ncRNAs are altered in human leukemias and carcinomas. Cancer cell. 2007; 12:215-229.
50. Petri A, Dybkaer K, Bogsted M, Thrue CA, Hagedorn PH, Schmitz A, Bodker JS, Johnsen HE, and Kauppinen S. Long Noncoding RNA Expression during Human B-Cell Development. PloS one. 2015; 10:e0138236.
51. Chaligne R, and Heard E. X-chromosome inactivation in development and cancer. FEBS letters. 2014; 588:2514-2522.
52. Gabory A, Jammes H, and Dandolo L. The H19 locus: role of an imprinted non-coding RNA in growth and development. BioEssays: news and reviews in molecular, cellular and developmental biology. 2010; 32:473-480.
53. Bock O, Schlue J, and Kreipe H. Reduced expression of H19 in bone marrow cells from chronic myeloproliferative disorders. Leukemia. 2003; 17:815-816.
54. Tessema M, Langer F, Bock O, Seltsam A, Metzig K, Hasemeier B, Kreipe H, and Lehmann U. Down-regulation of the IGF-2/H19 locus during normal and malignant hematopoiesis is independent of the imprinting pattern. International journal of oncology. 2005; 26:499-507.
55. Guo G, Kang Q, Chen Q, Chen Z, Wang J, Tan L, and Chen JL. High expression of long non-coding RNA H19 is required for efficient tumorigenesis induced by Bcr-Abl oncogene. FEBS letters. 2014; 588:1780-1786.
56. Takeuchi S, Hofmann WK, Tsukasaki K, Takeuchi N, Ikezoe T, Matsushita M, Uehara Y, and Phillip Koeffler H. Loss of H19 imprinting in adult T-cell leukaemia/lymphoma. British journal of haematology. 2007; 137:380-381.
57. Cai X, and Cullen BR. The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA (New York, NY). 2007; 13:313-316.
58. Tsang WP, Ng EK, Ng SS, Jin H, Yu J, Sung JJ, and Kwok TT. Oncofetal H19-derived miR-675 regulates tumor suppressor RB in human colorectal cancer. Carcinogenesis. 2010; 31:350-358.
59. Guo G, Kang Q, Zhu X, Chen Q, Wang X, Chen Y, Ouyang J, Zhang L, Tan H, Chen R, Huang S, and Chen JL. A long noncoding RNA critically regulates Bcr-Ablmediated cellular transformation by acting as a competitive endogenous RNA. Oncogene. 2015; 34:1768-1779.
60. Sun J, Li W, Sun Y, Yu D, Wen X, Wang H, Cui J, Wang G, Hoffman AR, and Hu JF. A novel antisense long noncoding RNA within the IGF1R gene locus is imprinted in hematopoietic malignancies. Nucleic acids research. 2014; 42:9588-9601.
61. Chapuis N, Tamburini J, Cornillet-Lefebvre P, Gillot L, Bardet V, Willems L, Park S, Green AS, Ifrah N, Dreyfus F, Mayeux P, Lacombe C, and Bouscary D. Autocrine IGF-1/IGF-1R signaling is responsible for constitutive PI3K/Akt activation in acute myeloid leukemia: therapeutic value of neutralizing anti-IGF-1R antibody. Haematologica. 2010; 95:415-423.
62. Zhou Y, Zhong Y, Wang Y, Zhang X, Batista DL, Gejman R, Ansell PJ, Zhao J, Weng C, and Klibanski A. Activation of p53 by MEG3 non-coding RNA. The Journal of biological chemistry. 2007; 282:24731-24742.
63. Benetatos L, Hatzimichael E, Dasoula A, Dranitsaris G, Tsiara S, Syrrou M, Georgiou I, and Bourantas KL. CpG methylation analysis of the MEG3 and SNRPN imprinted genes in acute myeloid leukemia and myelodysplastic syndromes. Leukemia research. 2010; 34:148-153.
64. Khoury H, Suarez-Saiz F, Wu S, and Minden MD. An upstream insulator regulates DLK1 imprinting in AML. Blood. 2010; 115:2260-2263.
65. Benetatos L, Dasoula A, Hatzimichael E, Georgiou I, Syrrou M, and Bourantas KL. Promoter hypermethylation of the MEG3 (DLK1/MEG3) imprinted gene in multiple myeloma. Clinical lymphoma & myeloma. 2008; 8:171-175.
66. Zhang X, Gejman R, Mahta A, Zhong Y, Rice KA, Zhou Y, Cheunsuchon P, Louis DN, and Klibanski A. Maternally expressed gene 3, an imprinted noncoding RNA gene, is associated with meningioma pathogenesis and progression. Cancer research. 2010; 70:2350-2358.
67. Benetatos L, Vartholomatos G, and Hatzimichael E. MEG3 imprinted gene contribution in tumorigenesis. International journal of cancer Journal international du cancer. 2011; 129:773-779.
68. Garzon R, Volinia S, Papaioannou D, Nicolet D, Kohlschmidt J, Yan PS, Mrozek K, Bucci D, Carroll AJ, Baer MR, Wetzler M, Carter TH, Powell BL, et al. Expression and prognostic impact of lncRNAs in acute myeloid leukemia. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111:18679-18684.
69. Diaz-Beya M, Brunet S, Nomdedeu J, Pratcorona M, Cordeiro A, Gallardo D, Escoda L, Tormo M, Heras I, Ribera JM, Duarte R, de Llano MP, Bargay J, et al. The lincRNA HOTAIRM1, located in the HOXA genomic region, is expressed in acute myeloid leukemia, impacts prognosis in patients in the intermediate-risk cytogenetic category, and is associated with a distinctive microRNA signature. Oncotarget. 2015; 6:31613-31627. doi: 10.18632/oncotarget.5148.
70. Tanigaki K, and Honjo T. Regulation of lymphocyte development by Notch signaling. Nature immunology. 2007; 8:451-456.
71. Tzoneva G, and Ferrando AA. Recent advances on NOTCH signaling in T-ALL. Current topics in microbiology and immunology. 2012; 360:163-182.
72. Trimarchi T, Bilal E, Ntziachristos P, Fabbri G, Dalla-Favera R, Tsirigos A, and Aifantis I. Genome-wide mapping and characterization of Notch-regulated long noncoding RNAs in acute leukemia. Cell. 2014; 158:593-606.
73. Medyouf H, Gusscott S, Wang H, Tseng JC, Wai C, Nemirovsky O, Trumpp A, Pflumio F, Carboni J, Gottardis M, Pollak M, Kung AL, Aster JC, et al. High-level IGF1R expression is required for leukemia-initiating cell activity in T-ALL and is supported by Notch signaling. The Journal of experimental medicine. 2011; 208:1809-1822.
74. Gaidano G, Foa R, and Dalla-Favera R. Molecular pathogenesis of chronic lymphocytic leukemia. The Journal of clinical investigation. 2012; 122:3432-3438.
75. Dohner H, Stilgenbauer S, Benner A, Leupolt E, Krober A, Bullinger L, Dohner K, Bentz M, and Lichter P. Genomic aberrations and survival in chronic lymphocytic leukemia. The New England journal of medicine. 2000; 343:1910-1916.
76. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M, Rassenti L, Alder H, Volinia S, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102:13944-13949.
77. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, Iorio MV, Visone R, Sever NI, Fabbri M, Iuliano R, Palumbo T, Pichiorri F, et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. The New England journal of medicine. 2005; 353:1793-1801.
78. Klein U, Lia M, Crespo M, Siegel R, Shen Q, Mo T, Ambesi-Impiombato A, Califano A, Migliazza A, Bhagat G, and Dalla-Favera R. The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer cell. 2010; 17:28-40.
79. Lerner M, Harada M, Loven J, Castro J, Davis Z, Oscier D, Henriksson M, Sangfelt O, Grander D, and Corcoran MM. DLEU2, frequently deleted in malignancy, functions as a critical host gene of the cell cycle inhibitory microRNAs miR-15a and miR-16-1. Experimental cell research. 2009; 315:2941-2952.
80. Garding A, Bhattacharya N, Claus R, Ruppel M, Tschuch C, Filarsky K, Idler I, Zucknick M, Caudron-Herger M, Oakes C, Fleig V, Keklikoglou I, Allegra D, et al. Epigenetic upregulation of lncRNAs at 13q14.3 in leukemia is linked to the In Cis downregulation of a gene cluster that targets NF-kB. PLoS genetics. 2013; 9:e1003373.
81. Kohlhammer H, Schwaenen C, Wessendorf S, Holzmann K, Kestler HA, Kienle D, Barth TF, Moller P, Ott G, Kalla J, Radlwimmer B, Pscherer A, Stilgenbauer S, et al. Genomic DNA-chip hybridization in t(11;14)-positive mantle cell lymphomas shows a high frequency of aberrations and allows a refined characterization of consensus regions. Blood. 2004; 104:795-801.
82. Bigoni R, Cuneo A, Milani R, Roberti MG, Bardi A, Rigolin GM, Cavazzini F, Agostini P, and Castoldi G. Secondary chromosome changes in mantle cell lymphoma: cytogenetic and fluorescence in situ hybridization studies. Leukemia & lymphoma. 2001; 40:581-590.
83. Harrison CJ, Mazzullo H, Cheung KL, Gerrard G, Jalali GR, Mehta A, Osier DG, and Orchard KH. Cytogenetics of multiple myeloma: interpretation of fluorescence in situ hybridization results. British journal of haematology. 2003; 120:944-952.
84. Elnenaei MO, Hamoudi RA, Swansbury J, Gruszka-Westwood AM, Brito-Babapulle V, Matutes E, and Catovsky D. Delineation of the minimal region of loss at 13q14 in multiple myeloma. Genes, chromosomes & cancer. 2003; 36:99-106.
85. Ronchetti D, Agnelli L, Taiana E, Galletti S, Manzoni M, Todoerti K, Musto P, Strozzi F, and Neri A. Distinct lncRNA transcriptional fingerprints characterize progressive stages of multiple myeloma. Oncotarget. 2016; doi: 10.18632/oncotarget.7442.
86. Popov N, and Gil J. Epigenetic regulation of the INK4b-ARF-INK4a locus: in sickness and in health. Epigenetics. 2010; 5:685-690.
87. Drexler HG. Review of alterations of the cyclin-dependent kinase inhibitor INK4 family genes p15, p16, p18 and p19 in human leukemia-lymphoma cells. Leukemia. 1998; 12:845-859.
88. Iacobucci I, Sazzini M, Garagnani P, Ferrari A, Boattini A, Lonetti A, Papayannidis C, Mantovani V, Marasco E, Ottaviani E, Soverini S, Girelli D, Luiselli D, et al. A polymorphism in the chromosome 9p21 ANRIL locus is associated to Philadelphia positive acute lymphoblastic leukemia. Leukemia research. 2011; 35:1052-1059.
89. Yap KL, Li S, Munoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ, and Zhou MM. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Molecular cell. 2010; 38:662-674.
90. Coccia EM, Cicala C, Charlesworth A, Ciccarelli C, Rossi GB, Philipson L, and Sorrentino V. Regulation and expression of a growth arrest-specific gene (gas5) during growth, differentiation, and development. Molecular and cellular biology. 1992; 12:3514-3521.
91. Mourtada-Maarabouni M, Pickard MR, Hedge VL, Farzaneh F, and Williams GT. GAS5, a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancer. Oncogene. 2009; 28:195-208.
92. Nakamura Y, Takahashi N, Kakegawa E, Yoshida K, Ito Y, Kayano H, Niitsu N, Jinnai I, and Bessho M. The GAS5 (growth arrest-specific transcript 5) gene fuses to BCL6 as a result of t(1;3)(q25;q27) in a patient with B-cell lymphoma. Cancer genetics and cytogenetics. 2008; 182:144-149.
93. Qiao HP, Gao WS, Huo JX, and Yang ZS. Long non-coding RNA GAS5 functions as a tumor suppressor in renal cell carcinoma. Asian Pacific journal of cancer prevention: APJCP. 2013; 14:1077-1082.
94. Shi X, Sun M, Liu H, Yao Y, Kong R, Chen F, and Song Y. A critical role for the long non-coding RNA GAS5 in proliferation and apoptosis in non-small-cell lung cancer. Molecular carcinogenesis. 2015; 54 Suppl 1:E1-e12.
95. Kino T, Hurt DE, Ichijo T, Nader N, and Chrousos GP. Noncoding RNA gas5 is a growth arrest-and starvationassociated repressor of the glucocorticoid receptor. Science signaling. 2010; 3:ra8.
96. Dave BJ, Nelson M, Pickering DL, Chan WC, Greiner TC, Weisenburger DD, Armitage JO, and Sanger WG. Cytogenetic characterization of diffuse large cell lymphoma using multi-color fluorescence in situ hybridization. Cancer genetics and cytogenetics. 2002; 132:125-132.
97. Tu ZQ, Li RJ, Mei JZ, and Li XH. Down-regulation of long non-coding RNA GAS5 is associated with the prognosis of hepatocellular carcinoma. International journal of clinical and experimental pathology. 2014; 7:4303-4309.
98. Cao S, Liu W, Li F, Zhao W, and Qin C. Decreased expression of lncRNA GAS5 predicts a poor prognosis in cervical cancer. International journal of clinical and experimental pathology. 2014; 7:6776-6783.
99. Williams GT, Mourtada-Maarabouni M, and Farzaneh F. A critical role for non-coding RNA GAS5 in growth arrest and rapamycin inhibition in human T-lymphocytes. Biochemical Society transactions. 2011; 39:482-486.
100. Mourtada-Maarabouni M, Hasan AM, Farzaneh F, and Williams GT. Inhibition of human T-cell proliferation by mammalian target of rapamycin (mTOR) antagonists requires noncoding RNA growth-arrest-specific transcript 5 (GAS5). Molecular pharmacology. 2010; 78:19-28.
101. Isin M, Ozgur E, Cetin G, Erten N, Aktan M, Gezer U, and Dalay N. Investigation of circulating lncRNAs in B-cell neoplasms. Clinica chimica acta; international journal of clinical chemistry. 2014; 431:255-259.
102. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, Regev A, Lander ES, and Rinn JL. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proceedings of the National Academy of Sciences of the United States of America. 2009; 106:11667-11672.
103. Han Y, Liu Y, Gui Y, and Cai Z. Long intergenic noncoding RNA TUG1 is overexpressed in urothelial carcinoma of the bladder. Journal of surgical oncology. 2013; 107:555-559.
104. Schmidt LH, Spieker T, Koschmieder S, Schaffers S, Humberg J, Jungen D, Bulk E, Hascher A, Wittmer D, Marra A, Hillejan L, Wiebe K, Berdel WE, et al. The long noncoding MALAT-1 RNA indicates a poor prognosis in non-small cell lung cancer and induces migration and tumor growth. Journal of thoracic oncology. 2011; 6:1984-1992.
105. Xu C, Yang M, Tian J, Wang X, and Li Z. MALAT-1: a long non-coding RNA and its important 3' end functional motif in colorectal cancer metastasis. International journal of oncology. 2011; 39:169-175.
106. Ying L, Chen Q, Wang Y, Zhou Z, Huang Y, and Qiu F. Upregulated MALAT-1 contributes to bladder cancer cell migration by inducing epithelial-to-mesenchymal transition. Molecular bioSystems. 2012; 8:2289-2294.
107. Gutschner T, Hammerle M, Eissmann M, Hsu J, Kim Y, Hung G, Revenko A, Arun G, Stentrup M, Gross M, Zornig M, MacLeod AR, Spector DL, et al. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer research. 2013; 73:1180-1189.
108. Bernard D, Prasanth KV, Tripathi V, Colasse S, Nakamura T, Xuan Z, Zhang MQ, Sedel F, Jourdren L, Coulpier F, Triller A, Spector DL, and Bessis A. A long nuclearretained non-coding RNA regulates synaptogenesis by modulating gene expression. The EMBO journal. 2010; 29:3082-3093.
109. Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT, Freier SM, Bennett CF, Sharma A, Bubulya PA, Blencowe BJ, Prasanth SG, and Prasanth KV. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Molecular cell. 2010; 39:925-938.
110. Yang F, Yi F, Han X, Du Q, and Liang Z. MALAT-1 interacts with hnRNP C in cell cycle regulation. FEBS letters. 2013; 587:3175-3181.
111. Tripathi V, Shen Z, Chakraborty A, Giri S, Freier SM, Wu X, Zhang Y, Gorospe M, Prasanth SG, Lal A, and Prasanth KV. Long noncoding RNA MALAT1 controls cell cycle progression by regulating the expression of oncogenic transcription factor B-MYB. PLoS genetics. 2013; 9:e1003368.
112. Cho SF, Chang YC, Chang CS, Lin SF, Liu YC, Hsiao HH, Chang JG, and Liu TC. MALAT1 long non-coding RNA is overexpressed in multiple myeloma and may serve as a marker to predict disease progression. BMC cancer. 2014; 14:809.
113. Li B, Chen P, Qu J, Shi L, Zhuang W, Fu J, Li J, Zhang X, Sun Y, and Zhuang W. Activation of LTBP3 gene by a long noncoding RNA (lncRNA) MALAT1 transcript in mesenchymal stem cells from multiple myeloma. The Journal of biological chemistry. 2014; 289:29365-29375.
114. Matsumoto T, and Abe M. TGF-beta-related mechanisms of bone destruction in multiple myeloma. Bone. 2011; 48:129-134.
115. Dal Bo M, Rossi FM, Rossi D, Deambrogi C, Bertoni F, Del Giudice I, Palumbo G, Nanni M, Rinaldi A, Kwee I, Tissino E, Corradini G, Gozzetti A, et al. 13q14 deletion size and number of deleted cells both influence prognosis in chronic lymphocytic leukemia. Genes, chromosomes & cancer. 2011; 50:633-643.
116. Hutchinson JN, Ensminger AW, Clemson CM, Lynch CR, Lawrence JB, and Chess A. A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains. BMC genomics. 2007; 8:39.
117. Miyagawa R, Tano K, Mizuno R, Nakamura Y, Ijiri K, Rakwal R, Shibato J, Masuo Y, Mayeda A, Hirose T, and Akimitsu N. Identification of cis-and trans-acting factors involved in the localization of MALAT-1 noncoding RNA to nuclear speckles. RNA (New York, NY). 2012; 18:738-751.