The beginning of the road for non-coding RNAs in normal hematopoiesis and hematologic malignancies

Frontiers in Genetics

Volumn 2, Issue DEC, 2011, Pages

  Heuston, Elisabeth F ^a   Lemon, Kenya T ^a   Arceci, Robert J ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

ALL; AML; CLL; CML; Non coding RNA

Indexed keywords

EID: 84875917665     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2011.00094     Document Type: Review

References (76)

1. Astuti, D., Latif, F., Wagner, K., Gentle, D., Cooper, W. N., Catchpoole, D., Grundy, R., Ferguson-Smith, A. C., and Maher, E. R. (2005). Epigenetic alteration at the DLK1-GTL2 imprinted domain in human neoplasia: analysis of neuroblastoma, phaeochromocy-toma and Wilms' tumour. Br. J. Cancer 92, 1574-1580
2. Baker, M. (2011). Long noncoding RNAs: the search for function. Nat. Methods. 8, 379-383
3. Bandi, N., Zbinden, S., Gugger, M., Arnold, M., Kocher, V., Hasan, L., Kappeler, A., Brunner, T., and Vas-sella, E. (2009a). miR-15a and miR-16 are implicated in cell cycle regulation in a Rb-dependent manner and are frequently deleted or down-regulated in non-small cell lung cancer. Cancer Res. 69, 5553-5559.
4. Bandi, N., Zbinden, S., Gugger, M., Arnold, M., Kocher, V., Hasan, L., Kappeler, A., Brunner, T., and Vassella, E. (2009b). miR-15a and miR-16 are implicated in cell cycle regulation in a Rb-dependent manner and are frequently deleted or down-regulated in non,Ai Small cell lung cancer. Cancer Res. 69,5553-5559.
5. Bejerano, G., Pheasant, M., Makunin, I., Stephen, S., Kent, W. J., Mattick, J. S., and Haussler, D. (2004). Ultra-conserved elements in the human genome. Science 304, 1321-1325.
6. Benetatos, L., Hatzimichael, E., Dasoula, A., Dranitsaris, G., Tsiara, S., Syrrou, M., Georgiou, I., and Bourantas, K. L. (2009). CpG methylation analysis of the MEG3 and SNRPN imprinted genes in acute myeloid leukemia and myelodysplastic syndromes. Leuk. Res. 34, 148-153.
7. Blum, W., Garzon, R., Klisovic, R. B., Schwind, S., Walker, A., Geyer, S., Liu, S., Havelange, V., Becker, H., Schaaf, L., Mickle, J., Devine, H., Kefau-ver, C., Devine, S. M., Chan, K. K., Heerema, N. A., Bloomfield, C. D., Grever, M. R., Byrd, J. C., Villalona-Calero, M., Croce, C. M., and Mar-cucci, G. (2010). Clinical response and miR-29b predictive significance in older AML patients treated with a 10-day schedule of decitabine. Proc. Natl. Acad. Sci. U.S.A. 107, 7473-7478.
8. Braconi, C., Kogure, T., Valeri, N., Huang, N., Nuovo, G., Costinean, S., Negrini, M., Miotto, E., Croce, C. M., and Patel, T. (2011). MicroRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer. Oncogene 30,4750-4756.
9. Bullinger, L., DöHner, K., Bair, E., Fröhling, S., Schlenk, R. F., Tib-shirani, R., DöHner, H., and Pollack, J. R. (2004). Use of gene-expression profiling to identify prognostic subclasses in adult acute myeloid leukemia. N. Engl. J. Med. 350,1605-1616.
10. Calin, G. A., and Croce, C. M. (2006). MicroRNA-cancer connection: the beginning of a new tale. Cancer Res. 66, 7390-7394.
11. Calin, G. A., Dumitru, C. D., Shimizu, M., Bichi, R., Zupo, S., Noch, E., Aldler, H., Rattan, S., Keating, M., Rai, K., Rassenti, L., Kipps, T., Negrini, M., Bullrich, F., and Croce, C. M. (2002). Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. U.S.A. 99, 15524-15529.
12. Calin, G. A., Ferracin, M., Cimmino, A., Di Leva, G., Shimizu, M., Woj-cik, S. E., Iorio, M. V., Visone, R., Sever, N. I., Fabbri, M., Iuliano, R., Palumbo, T., Pichiorri, F., Roldo, C., Garzon, R., Sevignani, C., Rassenti, L., Alder, H., Volinia, S., Liu, C.-G., Kipps, T. J., Negrini, M., and Croce, C. M. (2005). A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N. Engl. J. Med. 353, 1793-1801.
13. Calin, G. A., Liu, C.-G., Ferracin, M., Hyslop, T., Spizzo, R., Sevignani, C., Fabbri, M., Cimmino, A., Lee, E. J., Wojcik, S. E., Shimizu, M., Tili, E., Rossi, S., Taccioli, C., Pichiorri, F., Liu, X., Zupo, S., Herlea, V., Gra-mantieri, L., Lanza, G., Alder, H., Rassenti, L., Volinia, S., Schmittgen, Thomasâ d., Kipps, T. J., Negrini, M., and Croce, C. M. (2007). Ultra-conserved regions encoding ncR-NAs are altered in human leukemias and carcinomas. Cancer Cell 12, 215-229.
14. Calin, G. A., Sevignani, C., Dumitru, C. D., Hyslop, T., Noch, E., Yendamuri, S., Shimizu, M., Rattan, S., Bullrich, F., Negrini, M., and Croce, C. M. (2004). Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc. Natl. Acad. Sci. U.S.A. 101, 2999-3004.
15. Carninci, P., Kasukawa, T., Katayama, S., Gough, J., Frith, M. C., Maeda, N., Oyama, R., Ravasi, T., Lenhard, B., Wells, C., Kodzius, R., Shimokawa, K., Bajic, V. B., Brenner, S. E., Bat-alov, S., Forrest, A. R. R.,Zavolan, M., Davis, M. J., Wilming, L. G., Aidinis, V., Allen, J. E., Ambesi-Impiombato, A., Apweiler, R., Aturaliya, R. N., Bailey, T. L., Bansal, M., Baxter, L., Beisel, K. W., Bersano, T., Bono, H., Chalk, A. M., Chiu, K. P., Choud-hary,V., Christoffels, A., Clutterbuck, D. R., Crowe, M. L., Dalla, E., Dal-rymple, B. P., De Bono, B., Gatta, G. D., Di Bernardo, D., Down, T., Engstrom, P., Fagiolini, M., Faulkner, G., Fletcher, C. F., Fukushima, T., Furuno, M., Futaki, S., Gariboldi, M., Georgii-Hemming, P., Gingeras, T. R., Gojobori, T., Green, R. E., Gustincich, S., Harbers, M., Hayashi, Y., Hensch, T. K., Hirokawa, N., Hill, D., Huminiecki, L., Iacono, M., Ikeo, K., Iwama, A., Ishikawa, T., Jakt, M., Kanapin, A., Katoh, M., Kawasawa, Y., Kelso, J., Kitamura, H., Kitano, H., Kollias, G., Krish-nan, S. P. T., Kruger, A., Kummer-feld, S. K., Kurochkin, I. V., Lareau, L. F., Lazarevic, D., Lipovich, L., Liu, J., Liuni, S., Mcwilliam, S., Babu, M. M., Madera, M., Marchionni, L., Matsuda, H., Matsuzawa, S., Miki, H., Mignone, F., Miyake, S., Morris, K., Mottagui-Tabar, S., Mulder, N., Nakano, N., Nakauchi, H., Ng, P., Nilsson, R., Nishiguchi, S., Nishikawa, S., Nori, F., Ohara, O., Okazaki, Y., Orlando, V., Pang, K. C., Pavan, W J., Pavesi, G., Pesole, G., Petrovsky, N., Piazza, S., Reed, J., Reid, J. F., Ring, B. Z., Ringwald, M., Rost, B., Ruan, Y., Salzberg, S. L., Sandelin, A., Schneider, C., Schön-bach, C., Sekiguchi, K., Semple, C. A., Seno, S., Sessa, L., Sheng, Y., Shi-bata, Y., Shimada, H., Shimada, K., Silva, D., Sinclair, B., Sperling, S., Stupka, E., Sugiura, K., Sultana, R., Takenaka, Y., Taki, K., Tammoja, K., Tan, S. L., Tang, S., Taylor, M. S., Tegner, J., Teichmann, S. A., Ueda, H. R., van Nimwegen, E., Verardo, R., Wei, C. L., Yagi, K., Yamanishi, H., Zabarovsky, E., Zhu, S., Zimmer, A., Hide, W., Bult, C., Grimmond, S. M., Teasdale, R. D., Liu, E. T., Bru-sic, V., Quackenbush, J., Wahlestedt, C., Mattick, J. S., Hume, D. A., Kai, C., Sasaki, D., Tomaru, Y., Fukuda, S., Kanamori-Katayama, M., Suzuki, M., Aoki, J., Arakawa, T., Iida, J., Ima-mura, K., Itoh, M., Kato, T., Kawaji, H., Kawagashira, N., Kawashima, T., Kojima, M., Kondo, S., Konno, H., Nakano, K., Ninomiya, N., Nishio, T., Okada, M., Plessy, C., Shibata, K., Shiraki, T., Suzuki, S., Tagami, M., Waki, K., Watahiki, A., Okamura-Oho, Y., Suzuki, H., Kawai, J., Hayashizaki, Y., FANTOM Consortium, and RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group). (2005). The transcriptional landscape of the mammalian genome. Science 309, 1559-1563.
16. Chen, C., Frierson, Jr. H. F., Haggerty, P. F., Theodorescu, D., Gregory, C. W., and Dong, J.-T. (2001). An 800-kb region of deletion at 13q14 in human prostate and other carcinomas. Genomics 77, 135-144.
17. Cheng, A. M., Byrom, M. W., Shel-ton, J., and Ford, L. P. (2005). Anti-sense inhibition of human miR-NAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res. 33, 1290-1297.
18. Cimmino, A., Calin, G. A., Fabbri, M., Iorio, M. V., Ferracin, M., Shimizu, M., Wojcik, S. E., Aqeilan, R. I., Zupo, S., Dono, M., Rassenti, L., Alder, H., Volinia, S., Liu, C.-G., Kipps, T. J., Negrini, M., and Croce, C. M. (2005). miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc. Natl. Acad. Sci. U.S.A. 102, 13944-13949.
19. Dou, L., Zheng, D., Li, J., Li, Y., Gao, L., Wang, L., and Yu, L. (2011). Methylation-mediated repression of microRNA-143 enhances MLL-AF4 oncogene expression. Oncogene. doi: 10.1038/onc.2011.248
20. Du, Q., Wang, L., Zhu, H., Zhang, S., Xu, L., Zheng, W., and Liu, X. (2010). The role of heterogeneous nuclear ribonucleoprotein K in the progression of chronic myeloid leukemia. Med. Oncol. 27, 673-679.
21. Esquela-Kerscher, A., and Slack, F. J. (2006). Oncomirs [mdash] microR-NAs with a role in cancer. Nat. Rev. Cancer 6, 259-269.
22. Faraoni, I., Antonetti, F. R., Cardone, J., and Bonmassar, E. (2009). miR-155 gene: a typical multifunctional microRNA. Biochim. Biophys. Acta 1792,497-505.
23. Garzon, R., Garofalo, M., Martelli, M. P., Briesewitz, R., Wang, L., Fernandez-Cymering, C., Volinia, S., Liu, C. G., Schnittger, S., Haferlach, T., Liso, A., Diverio, D., Mancini, M., Mel-oni, G., Foa, R., Martelli, M. F., Mecucci, C., Croce, C. M., and Falini, B. (2008a). Distinctive microRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucle-ophosmin. Proc. Natl. Acad. Sci. U.S.A. 105, 3945-3950.
24. Garzon, R., Volinia, S., Liu, C.-G., Fernandez-Cymering, C., Palumbo, T., Pichiorri, F., Fabbri, M., Coombes, K., Alder, H., Nakamura, T., Flomenberg, N., Marcucci, G., Calin, G. A., Kornblau, S. M., Kantar-jian, H., Bloomfield, C. D., Andreeff, M., and Croce, C. M. (2008b). MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia. Blood 111, 3183-3189.
25. Garzon, R., Heaphy, C. E. A., Havelange, V., Fabbri, M., Volinia, S., Tsao, T., Zanesi, N., Kornblau, S. M., Marcucci, G., Calin, G. A., Andreeff, M., and Croce, C. M. (2009a). MicroRNA 29b functions in acute myeloid leukemia. Blood 114,5331-5341.
26. Garzon, R., Liu, S., Fabbri, M., Liu, Z., Heaphy, C. E. A., Callegari, E., Schwind, S., Pang, J., Yu, J., Muthusamy, N., Havelange, V., Volinia, S., Blum, W., Rush, L. J., Per-rotti, D., Andreeff, M., Bloomfield, C. D., Byrd, J. C., Chan, K., Wu, L.-C., Croce, C. M., and Marcucci, G. (2009b). MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by tar geting directly DNMT3A and 3B and indirectly DNMT1. Blood 113, 6411-6418.
27. Gibb, E. A., Brown, C. J., and Lam, W L. (2011). The functional role of long non-coding RNA in human carcinomas. Mol. Cancer 10,38.
28. Golub, T. R., Slonim, D. K., Tamayo, P., Huard, C., Gaasenbeek, M., Mesirov, J. P., Coller, H., Loh, M. L., Downing, J. R., Caligiuri, M. A., Bloomfield, C. D., and Lander, E.S. (1999). Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 286, 531-537.
29. Group, R. G. E. R., Genome Science, G., The, R C., Katayama, S., Tomaru, Y., Kasukawa, T., Waki, K., Nakan-ishi, M., Nakamura, M., Nishida, H., Yap, C. C., Suzuki, M., Kawai, J., Suzuki, H., Carninci, P., Hayashizaki, Y., Wells, C., Frith, M., Ravasi, T., Pang, K. C., Hallinan, J., Mattick, J., Hume, D. A., Lipovich, L., Bat-alov, S., Engström, P. G., Mizuno, Y., Faghihi, M. A., Sandelin, A., Chalk, A. M., Mottagui-Tabar, S., Liang, Z., Lenhard, B., and Wahlestedt, C. (2005). Antisense Transcription in the mammalian transcriptome. Science 309,1564-1566.
30. Guttman, M., Amit, I., Garber, M., French, C., Lin, M. F., Feldser, D., Huarte, M., Zuk, O., Carey, B. W., Cassady, J. P., Cabili, M. N., Jaenisch, R., Mikkelsen, T. S., Jacks, T., Haco-hen, N., Bernstein, B. E., Kellis, M., Regev, A., Rinn, J. L., and Lander, E. S. (2009). Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458, 223-227.
31. Hayashita, Y., Osada, H., Tatematsu, Y., Yamada, H., Yanagisawa, K., Tomida, S., Yatabe, Y., Kawahara, K., Sekido, Y., and Takahashi, T. (2005). A poly-cistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res. 65,9628-9632.
32. Heerema-McKenney, A., and Arber, D. A. (2009). Acute myeloid leukemia. Hematol Oncol Clin. North Am. 23, 633-654.
33. Huarte, M., Guttman, M., Feldser, D., Garber, M., Koziol, M. J., Kenzelmann-Broz, D., Khalil, A. M., Zuk, O., Amit, I., Rabani, M., Attar di, L. D., Regev, A., Lander, E. S., Jacks, T., and Rinn, J. L. (2010). A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142, 409-419.
34. Huarte, M., and Rinn, J. L. (2010). Large non-coding RNAs: missing links in cancer Hum. Mol Genet. 19, R152-R161.
35. 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., Vignetti, M., Baccarani, M., and Martinelli, G. (2011). A polymorphism in the chromosome 9p21 ANRIL locus is associated to Philadelphia positive acute lymphoblastic leukemia. Leuk. Res. 35, 1052-1059.
36. Ivanovska, I., Ball, A. S., Diaz, R. L., Magnus, J. F., Kibukawa, M., Schelter, J. M., Kobayashi, S. V., Lim, L., Bur-chard, J., Jackson, A. L., Linsley P. S., and Cleary, M. A. (2008). MicroR-NAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol Cell. Biol. 28, 2167-2174.
37. Jose-Eneriz, S. E., Roman-Gomez, J., Jimenez-Velasco, A., Garate, L., Martin,V., Cordeu, L.,Vilas-Zornoza, A., Rodriguez-Otero, P., Calasanz, M. J., Prosper, F., and Agirre, X. (2009). MicroRNA expression profiling in imatinib-resistant chronic myeloid leukemia patients without clinically significant ABL1-mutations. Mol. Cancer 8, 69.
38. Kagami, M., O'sullivan, M. J., Green, A. J., Watabe, Y., Arisaka, O., Masawa, N., Matsuoka, K., Fukami, M., Matsubara, K., Kato, F., Ferguson-Smith, A. C., and Ogata, T. (2010). The IG-DMR and the MEG3-DMR at human chromosome 14q32.2: hierarchical interaction and distinct functional properties as imprinting control centers. PLoS Genet 6, e1000992. doi:10.1371/journal.pgen.1000992
39. Kantarjian, H., Sawyers, C., Hochhaus, A., Guilhot, F., Schiffer, C., Gambacorti-Passerini, C., Nieder-wieser, D., Resta, D., Capdeville, R., Zoellner, U., Talpaz, M., and Druker, B. (2002). Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia. N Engl J. Med. 346, 645-652.
40. Kapranov, P., St Laurent, G., Raz, T., Ozsolak, F., Reynolds, C. P., Sorensen, P. H., Reaman, G., Milos, P., Arceci, R. J., Thompson, J. F., and Triche, T. J. (2010). The majority of total nuclear-encoded non-ribosomal RNA in a human cell is "dark matter" un-annotated RNA. BMC Biol. 8, 149. doi:10.1186/1741-7007-8-149
41. Khoury, H., Suarez-Saiz, F., Wu, S., and Minden, M. D. (2010). An upstream insulator regulates DLK1 imprinting in AML. Blood 115,2260-2263.
42. Kim, W. Y., and Sharpless, N. E. (2006). The regulation of INK4/ARF in cancer and aging. Cell 127, 265-275.
43. Kivelä, T., Tuppurainen, K., Riiko-nen, P., and Vapalahti, M. (2003). Retinoblastoma associated with chromosomal 13q14 deletion mosaicism. Ophthalmology 110, 1983-1988.
44. Klein, U., Lia, M., Crespo, M., Siegel, R., Shen, Q., Mo, T., Ambesi-Impiombato, A., Califano, A., Migli-azza, A., Bhagat, G., and Dalla-Favera, R. (2010). The DLEU2/miR-15a/16-1 Cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 17,28-40.
45. Kotake, Y., Nakagawa, T., Kitagawa, K., Suzuki, S., Liu, N., Kitagawa, M., and Xiong, Y (2011). Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15INK4B tumor suppressor gene. Oncogene 30, 1956-1962.
46. Lee, R. C., and Ambros, V. (2001). An Extensive Class of Small RNAs in Caenorhabditis elegans. Science 294, 862-864.
47. Lerner, M., Harada, M., Lovén, J., Castro, J., Davis, Z., Oscier, D., Henriksson, M., Sangfelt, O., Grandér, D., and Corcoran, M. M. (2009). DLEU2, frequently deleted in malignancy, functions as a critical host gene of the cell cycle inhibitory microRNAs miR-15a and miR-16-1. Exp. Cell Res. 315,2941-2952.
48. Li, S., Moffett, H. F., Lu, J., Werner, L., Zhang, H., Ritz, J., Neuberg, D., Wucherpfennig, K. W., Brown, J. R., and Novina, C. D. (2011). MicroRNA expression profiling identifies activated B cell status in chronic lymphocytic leukemia cells. PLoS ONE 6,e16956. doi:10.1371/journal.pone.0016956
49. Li, Z., Lu, J., Sun, M., Mi, S., Zhang, H., Luo, R. T., Chen, P., Wang, Y., Yan, M., Qian, Z., Neilly, M. B., Jin, J., Zhang, Y., Bohlander, S. K., Zhang, D.-E., Larson, R. A., Le Beau, M. M., Thirman, M. J., Golub, T. R., Rowley, J. D., and Chen, J. (2008). Distinct microRNA expression profiles in acute myeloid leukemia with common translocations. Proc. Natl Acad. Sci. U.S.A. 105, 15535-15540.
50. Liu, Y., Corcoran, M., Rasool, O., Ivanova, G., Ibbotson, R., Grander, D., Iyengar, A., Baranova, A., Kashuba, V., Merup, M., Wu, X., Gardiner, A., Mullenbach, R., Polta-raus, A., Hultstrom, A. L., Julius-son, G., Chapman, R., Tiller, M., Cotter, F., Gahrton, G., Yankovsky, N., Zabarovsky, E., Einhorn, S., and Oscier, D. (1997). Cloning of two candidate tumor suppressor genes within a 10 kb region on chromosome 13q14, frequently deleted in chronic lymphocytic leukemia. Oncogene 15,2463-2473.
51. Lujambio, A., Portela, A., Liz, J., Melo, S. A., Rossi, S., Spizzo, R., Croce, C. M., Calin, G. A., and Esteller, M. (2010). CpG island hypermethylation-associated silencing of non-coding RNAs transcribed from ultraconserved regions in human cancer. Oncogene 29, 6390-6401.
52. Marcucci, G., Radmacher, M. D., Maharry, K., Mrózek, K., Ruppert, A. S., Paschka, P., Vukosavljevic, T., Whitman, S. P., Baldus, C. D., Langer, C., Liu, C.-G., Carroll, A. J., Powell, B. L., Garzon, R., Croce, C. M., Kolitz, J. E., Caligiuri, M. A., Larson, R. A., and Bloomfield, C. D. (2008). MicroRNA expression in cytogenetically normal acute myeloid leukemia. N. Engl. J. Med. 358,1919-1928.
53. Margueron, R., and Reinberg, D. (2011). The Polycomb complex PRC2 and its mark in life. Nature 469, 343-349.
54. Mestdagh, P., Fredlund, E., Pattyn, F., Rihani, A., Van Maerken, T., Ver-meulen, J., Kumps, C., Menten, B., De Preter, K., Schramm, A., Schulte, J., Noguera, R., Schleiermacher, G., Janoueix-Lerosey, I., Laureys, G., Powel, R., Nittner, D., Marine, J. C., Ringner, M., Speleman, F., and Vandesompele, J. (2010). An inte-grative genomics screen uncovers ncRNA T-UCR functions in neu-roblastoma tumours. Oncogene 29, 3583-3592.
55. Mi, S., Lu, J., Sun, M., Li, Z., Zhang, H., Neilly, M. B., Wang, Y., Qian, Z., Jin, J., Zhang, Y., Bohlander, S. K., Le Beau, M. M., Larson, R. A., Golub, T. R., Rowley, J. D., and Chen, J. (2007). MicroRNA expression signatures accurately discriminate acute lymphoblastic leukemia from acute myeloid leukemia. Proc. Natl Acad. Sci. U.S.A. 104, 19971-19976.
56. Migliazza, A., Bosch, F., Komatsu, H., Cayanis, E., Martinotti, S., Toni-ato, E., Guccione, E., Qu, X., Chien, M., Murty, V. V. V., Gaidano, G., Inghirami, G., Zhang, P., Fischer, S., Kalachikov, S. M., Russo, J., Edelman, I., Efstratiadis, A., and Dalla-Favera, R. (2001). Nucleotide sequence, transcription map, and mutation analysis of the 13q14 chromosomal region deleted in B-cell chronic lymphocytic leukemia. Blood 97,2098-2104.
57. Mishra, P. J., Song, B., Mishra, P. J., Wang, Y., Humeniuk, R., Banerjee, D., Merlino, G., Ju, J., and Bertino, J. R. (2009). MiR-24 Tumor suppressor activity is regulated independent of p53 and through a target site polymorphism. PLoS ONE 4, e8445. doi:10.1371/journal.pone.0008445
58. Notari, M., Neviani, P., Santhanam, R., Blaser, B. W., Chang, J.-S., Galietta, A., Willis, A. E., Roy, D. C., Caligiuri, M. A., Marcucci, G., and Perrotti, D. (2006). A MAPK/HNRPK pathway controls BCR/ABL oncogenic potential by regulating MYC mRNA translation. Blood 107, 2507-2516.
59. Ørom, U. A., Derrien, T., Beringer, M., Gumireddy, K., Gardini, A., Bussotti, G., Lai, F., Zytnicki, M., Notredame, C., Huang, Q., Guigo, R., and Shiekhattar, R. (2010). Long noncoding RNAs with enhancer-like function in human cells. Cell 143, 46-58.
60. Ørom, U. A., Nielsen, F. C., and Lund, A. H. (2008). MicroRNA-10a binds the 52UTR of ribosomal protein mRNAs and enhances their translation. Mol. Cell 30,460-471.
61. Pasmant, E., Laurendeau, I., Héron, D., Vidaud, M., Vidaud, D., and Bièche, I. (2007). Characterization of a germ-line deletion, including the entire INK4/ARF locus, in a melanoma-neural system tumor family: identification of ANRIL, an antisense noncoding RNA whose expression coclusters with ARF. Cancer Res. 67, 3963-3969.
62. Pekarsky, Y., Santanam, U., Cimmino, A., Palamarchuk, A., Efanov, A., Maximov, V., Volinia, S., Alder, H., Liu, C.-G., Rassenti, L., Calin, G. A., Hagan, J. P., Kipps, T., and Croce, C. M. (2006). Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res. 66, 11590-11593.
63. San Jose-Eneriz, E., Roman-Gomez, J., Jimenez-Velasco, A., Garate, L., Martin, V., Cordeu, L., Vilas-Zornoza, A., Rodriguez-Otero, P., Calasanz, M. J., Prosper, F., and Agirre, X. (2009). MicroRNA expression profiling in imatinib-resistant chronic myeloid leukemia patients without clinically significant ABL1-mutations. Mol. Cancer 8, 69.
64. Sherr, C. J. (1998). Tumor surveillance via the ARF-p53 pathway. Genes Dev. 12,2984-2991.
65. Tay, Y., Zhang, J., Thomson, A. M., Lim, B., and Rigoutsos, I. (2008). MicroR-NAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455, 1124-1128.
66. Valk, P. J. M., Verhaak, R. G. W., Bei-jen, M. A., Erpelinck, C. A. J., Van Doorn-Khosrovani, S. B. V. W., Boer, J. M., Beverloo, H. B., Moorhouse, M. J., Van Der Spek, P. J., LãWenberg, B., and Delwel, R. (2004). Prognosti-cally useful gene-expression profiles in acute myeloid leukemia. N. Engl. J. Med. 350, 1617-1628.
67. Wagner, L. A., Christensen, C. J., Dunn, D. M., Spangrude, G. J., George-las, A., Kelley, L., Esplin, M. S., Weiss, R. B., and Gleich, G. J. (2007). EGO, a novel, noncoding RNA gene, regulates eosinophil granule protein transcript expression. Blood 109, 5191-5198.
68. Yap, K. L., Li, S., Muñoz-Cabello, A. M., Raguz, S., Zeng, L., Mujtaba, S., Gil, J., Walsh, M. J., and Zhou, M.-M. (2010). Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol. Cell 38, 662-674.
69. Yu, W., Gius, D., Onyango, P., Muldoon-Jacobs, K., Karp, J., Feinberg, A. P., and Cui, H. (2008). Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA. Nature 451,202-206.
70. Zhang, B., Pan, X., Cobb, G. P., and Anderson, T. A. (2007). microRNAs as oncogenes and tumor suppressors. Dev. Biol. 302,1-12.
71. Zhang, H., Luo, X.-Q., Zhang, P., Huang, L.-B., Zheng, Y.-S., Wu, J., Zhou, H., Qu, L.-H., Xu, L., and Chen, Y.-Q. (2009a). MicroRNA patterns associated with clinical prognostic parameters and cns relapse prediction in pediatric acute leukemia. PLoS ONE 4, e7826. doi:10.1371/jour-nal.pone.0007826
72. Zhang, X., Lian,Z., Padden, C., Gerstein, M. B., Rozowsky, J., Snyder, M., Gin-geras, T. R., Kapranov, P., Weissman, S. M., and Newburger, P. E. (2009b). A myelopoiesis-associated regulatory intergenic noncoding RNA transcript within the human HOXA cluster. Blood 113, 2526-2534.
73. Zhang, X., Rice, K., Wang, Y., Chen, W., Zhong, Y., Nakayama, Y., Zhou, Y., and Klibanski, A. (2010a). Maternally expressed gene 3 (MEG3) non-coding ribonucleic acid: isoform structure, expression, and functions. Endocrinology 151, 939-947.
74. Zhang, X., Zhou, Y., and Klibanski, A. (2010b). Isolation and characterization of novel pituitary tumor related genes: a cDNA representational difference approach. Mol. Cell. Endocrinol. 326, 40-47.
75. Zhang, X., Zhou, Y., Mehta, K. R., Danila, D. C., Scolavino, S., Johnson, S. R., and Klibanski, A. (2003). A pituitary-derived MEG3 isoform functions as a growth suppressor in tumor cells. J. Clin. Endocrinol. Metab. 88, 5119-5126
76. Zhou, Y.,Zhong,Y., Wang, Y., Zhang, X., Batista, D. L., Gejman, R., Ansell, P. J., Zhao, J., Weng, C., and Klibanski, A. (2007). activation of p53 by MEG3 non-coding RNA. J. Biol. Chem. 282, 24731-24742.