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http://dx.doi.org/10.14348/molcells.2014.0008

RNA Binding Protein-Mediated Post-Transcriptional Gene Regulation in Medulloblastoma  

Bish, Rebecca (New York University, Center for Genomics and Systems Biology)
Vogel, Christine (New York University, Center for Genomics and Systems Biology)
Abstract
Medulloblastoma, the most common malignant brain tumor in children, is a disease whose mechanisms are now beginning to be uncovered by high-throughput studies of somatic mutations, mRNA expression patterns, and epigenetic profiles of patient tumors. One emerging theme from studies that sequenced the tumor genomes of large cohorts of medulloblastoma patients is frequent mutation of RNA binding proteins. Proteins which bind multiple RNA targets can act as master regulators of gene expression at the post-transcriptional level to co-ordinate cellular processes and alter the phenotype of the cell. Identification of the target genes of RNA binding proteins may highlight essential pathways of medulloblastomagenesis that cannot be detected by study of transcriptomics alone. Furthermore, a subset of RNA binding proteins are attractive drug targets. For example, compounds that are under development as anti-viral targets due to their ability to inhibit RNA helicases could also be tested in novel approaches to medulloblastoma therapy by targeting key RNA binding proteins. In this review, we discuss a number of RNA binding proteins, including Musashi1 (MSI1), DEAD (Asp-Glu-Ala-Asp) box helicase 3 X-linked (DDX3X), DDX31, and cell division cycle and apoptosis regulator 1 (CCAR1), which play potentially critical roles in the growth and/or maintenance of medulloblastoma.
Keywords
medulloblastoma; pediatric cancer; RNA helicase; translation regulation;
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1 Jones, D.T., Jager, N., Kool, M., Zichner, T., Hutter, B., Sultan, M., Cho, Y.J., Pugh, T.J., Hovestadt, V., Stutz, A.M., et al. (2012). Dissecting the genomic complexity underlying medulloblastoma. Nature 488, 100-105.   DOI   ScienceOn
2 Jorba, N., Juarez, S., Torreira, E., Gastaminza, P., Zamarreno, N., Albar, J.P., and Ortin, J. (2008). Analysis of the interaction of influenza virus polymerase complex with human cell factors. Proteomics 8, 2077-2088.   DOI   ScienceOn
3 Kaderali, Z., Lamberti-Pasculli, M., and Rutka, J.T. (2009). The changing epidemiology of paediatric brain tumours: a review from the Hospital for Sick Children. Childs Nerv. Syst. 25, 787-793.   DOI
4 Kawauchi, D., Robinson, G., Uziel, T., Gibson, P., Rehg, J., Gao, C., Finkelstein, D., Qu, C., Pounds, S., Ellison, D.W., et al. (2012). A mouse model of the most aggressive subgroup of human medulloblastoma. Cancer Cell 21, 168-180.   DOI   ScienceOn
5 Kayahara, T., Sawada, M., Takaishi, S., Fukui, H., Seno, H., Fukuzawa, H., Suzuki, K., Hiai, H., Kageyama, R., Okano, H., et al. (2003). Candidate markers for stem and early progenitor cells, Musashi-1 and Hes1, are expressed in crypt base columnar cells of mouse small intestine. FEBS Lett. 535, 131-135.   DOI   ScienceOn
6 Kim, J.H., Yang, C.K., Heo, K., Roeder, R.G., An, W., and Stallcup, M.R. (2008). CCAR1, a key regulator of mediator complex recruitment to nuclear receptor transcription complexes. Mol. Cell 31, 510-519.   DOI   ScienceOn
7 Klass, D.M., Scheibe, M., Butter, F., Hogan, G.J., Mann, M., and Brown, P.O. (2013). Quantitative proteomic analysis reveals concurrent RNA-protein interactions and identifies new RNAbinding proteins in Saccharomyces cerevisiae. Genome Res. 23, 1028-1038.   DOI   ScienceOn
8 Kolobova, E., Efimov, A., Kaverina, I., Rishi, A.K., Schrader, J.W., Ham, A.J., Larocca, M.C., and Goldenring, J.R. (2009). Microtubule-dependent association of AKAP350A and CCAR1 with RNA stress granules. Exp. Cell Res. 315, 542-555.   DOI   ScienceOn
9 Geissler, R., Golbik, R.P., and Behrens, S.E. (2012). The DEADbox helicase DDX3 supports the assembly of functional 80S ribosomes. Nucleic Acids Res. 40, 4998-5011.   DOI
10 Gibson, P., Tong, Y., Robinson, G., Thompson, M.C., Currle, D.S., Eden, C., Kranenburg, T.A., Hogg, T., Poppleton, H., Martin, J., et al. (2010). Subtypes of medulloblastoma have distinct developmental origins. Nature 468, 1095-1099.   DOI   ScienceOn
11 Glisovic, T., Bachorik, J.L., Yong, J., and Dreyfuss, G. (2008). RNAbinding proteins and post-transcriptional gene regulation. FEBS Lett. 582, 1977-1986.   DOI   ScienceOn
12 Hambardzumyan, D., Becher, O.J., and Holland, E.C. (2008a). Cancer stem cells and survival pathways. Cell Cycle 7, 1371-1378.   DOI   ScienceOn
13 Horisawa, K., Imai, T., Okano, H., and Yanagawa, H. (2009). 3'- Untranslated region of doublecortin mRNA is a binding target of the Musashi1 RNA-binding protein. FEBS Lett. 583, 2429-2434.   DOI   ScienceOn
14 Hunter, S., Jones, P., Mitchell, A., Apweiler, R., Attwood, T.K., Bateman, A., Bernard, T., Binns, D., Bork, P., Burge, S., et al. (2012). InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res. 40, D306-312.   DOI   ScienceOn
15 Imai, T., Tokunaga, A., Yoshida, T., Hashimoto, M., Mikoshiba, K., Weinmaster, G., Nakafuku, M., and Okano, H. (2001). The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol. Cell Biol. 21, 3888-3900.   DOI   ScienceOn
16 Francois, S., D'rlando, C., Fatone, T., Touvier, T., Pessina, P., Meneveri, R., and Brunelli, S. (2012). Necdin enhances myoblasts survival by facilitating the degradation of the mediator of apoptosis CCAR1/CARP1. PLoS One 7, e43335.   DOI
17 Epple, L.M., Griffiths, S.G., Dechkovskaia, A.M., Dusto, N.L., White, J., Ouellette, R.J., Anchordoquy, T.J., Bemis, L.T., and Graner, M.W. (2012). Medulloblastoma exosome proteomics yield functional roles for extracellular vesicles. PLoS One 7, e42064.   DOI
18 Fan, X., and Eberhart, C.G. (2008). Medulloblastoma stem cells. J. Clin. Oncol. 26, 2821-2827.   DOI   ScienceOn
19 Fogarty, M.P., Kessler, J.D., and Wechsler-Reya, R.J. (2005). Morphing into cancer: the role of developmental signaling pathways in brain tumor formation. J. Neurobiol. 64, 458-475.   DOI   ScienceOn
20 Frange, P., Alapetite, C., Gaboriaud, G., Bours, D., Zucker, J.M., Zerah, M., Brisse, H., Chevignard, M., Mosseri, V., Bouffet, E., et al. (2009). From childhood to adulthood: long-term outcome of medulloblastoma patients. The Institut Curie experience (1980-2000). J. Neurooncol. 95, 271-279.   DOI
21 Fukawa, T., Ono, M., Matsuo, T., Uehara, H., Miki, T., Nakamura, Y., Kanayama, H.O., and Katagiri, T. (2012). DDX31 regulates the p53-HDM2 pathway and rRNA gene transcription through its interaction with NPM1 in renal cell carcinomas. Cancer Res. 72, 5867-5877.   DOI   ScienceOn
22 Galante, P.A., Sandhu, D., de Sousa Abreu, R., Gradassi, M., Slager, N., Vogel, C., de Souza, S.J., and Penalva, L.O. (2009). A comprehensive in silico expression analysis of RNA binding proteins in normal and tumor tissue: Identification of potential players in tumor formation. RNA Biol. 6, 426-433.   DOI
23 Dubuc, A.M., Remke, M., Korshunov, A., Northcott, P.A., Zhan, S.H., Mendez-Lago, M., Kool, M., Jones, D.T., Unterberger, A., Morrissy, A.S., et al. (2013). Aberrant patterns of H3K4 and H3K27 histone lysine methylation occur across subgroups in medulloblastoma. Acta Neuropathol. 125, 373-384.   DOI   ScienceOn
24 Cruciat, C.M., Dolde, C., de Groot, R.E., Ohkawara, B., Reinhard, C., Korswagen, H.C., and Niehrs, C. (2013). RNA helicase DDX3 is a regulatory subunit of casein kinase 1 in Wnt-beta-catenin signaling. Science 339, 1436-1441.   DOI   ScienceOn
25 Daugeron, M.C., and Linder, P. (1998). Dbp7p, a putative ATPdependent RNA helicase from Saccharomyces cerevisiae, is required for 60S ribosomal subunit assembly. RNA 4, 566-581.   DOI
26 Di, C., Liao, S., Adamson, D.C., Parrett, T.J., Broderick, D.K., Shi, Q., Lengauer, C., Cummins, J.M., Velculescu, V.E., Fults, D.W., et al. (2005). Identification of OTX2 as a medulloblastoma oncogene whose product can be targeted by all-trans retinoic acid. Cancer Res. 65, 919-924.
27 Choi, Y.J., and Lee, S.G. (2012). The DEAD-box RNA helicase DDX3 interacts with DDX5, co-localizes with it in the cytoplasm during the G2/M phase of the cycle, and affects its shuttling during mRNP export. J. Cell Biochem. 113, 985-996.   DOI   ScienceOn
28 Clifford, S.C., Lusher, M.E., Lindsey, J.C., Langdon, J.A., Gilbertson, R.J., Straughton, D., and Ellison, D.W. (2006). Wnt/Wingless pathway activation and chromosome 6 loss characterize a distinct molecular sub-group of medulloblastomas associated with a favorable prognosis. Cell Cycle 5, 2666-2670.   DOI
29 Ashour, A.E., Jamal, S., Cheryan, V.T., Muthu, M., Zoheir, K.M., Alafeefy, A.M., Abd-Allah, A.R., Levi, E., Tarca, A.L., Polin, L.A., et al. (2013). CARP-1 functional mimetics: a novel class of small molecule inhibitors of medulloblastoma cell growth. PLoS One 8, e66733.   DOI
30 Baltz, A.G., Munschauer, M., Schwanhausser, B., Vasile, A., Murakawa, Y., Schueler, M., Youngs, N., Penfold-Brown, D., Drew, K., Milek, M., et al. (2012). The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol. Cell 46, 674-690.   DOI   ScienceOn
31 Abdelhaleem, M. (2004). Do human RNA helicases have a role in cancer? Biochim. Biophys. Acta 1704, 37-46.
32 Battelli, C., Nikopoulos, G.N., Mitchell, J.G., and Verdi, J.M. (2006). The RNA-binding protein Musashi-1 regulates neural development through the translational repression of p21WAF-1. Mol. Cell Neurosci. 31, 85-96.   DOI   ScienceOn
33 Castello, A., Fischer, B., Hentze, M.W., and Preiss, T. (2013). RNAbinding proteins in Mendelian disease. Trends Genet. 29, 318-327.   DOI   ScienceOn
34 CBTRUS (2012). CBTRUS Statistical Report: Primary Brain and Central Nervous System Tumors Diagnosed in the United States in 2004-2008 (March 23, 2012 Revision). Hinsdale, IL, Central Brain Tumor Registry of the United States.
35 Cho, Y.J., Tsherniak, A., Tamayo, P., Santagata, S., Ligon, A., Greulich, H., Berhoukim, R., Amani, V., Goumnerova, L., Eberhart, C.G., et al. (2011). Integrative genomic analysis of medulloblastoma identifies a molecular subgroup that drives poor clinical outcome. J. Clin. Oncol. 29, 1424-1430.   DOI   ScienceOn
36 Northcott, P.A., Shih, D.J., Peacock, J., Garzia, L., Morrissy, A.S., Zichner, T., Stutz, A.M., Korshunov, A., Reimand, J., Schumacher, S.E., et al. (2012b). Subgroup-specific structural variation across 1,000 medulloblastoma genomes. Nature 488, 49-56.   DOI   ScienceOn
37 Owsianka, A.M., and Patel, A.H. (1999). Hepatitis C virus core protein interacts with a human DEAD box protein DDX3. Virology 257, 330-340.   DOI   ScienceOn
38 Pek, J.W., and Kai, T. (2011). DEAD-box RNA helicase Belle/DDX3 and the RNA interference pathway promote mitotic chromosome segregation. Proc. Natl. Acad. Sci. USA 108, 12007-12012.   DOI   ScienceOn
39 Packer, R.J., and Vezina, G. (2008). Management of and prognosis with medulloblastoma: therapy at a crossroads. Arch. Neurol. 65, 1419-1424.   DOI   ScienceOn
40 Pei, Y., Moore, C.E., Wang, J., Tewari, A.K., Eroshkin, A., Cho, Y.J., Witt, H., Korshunov, A., Read, T.A., Sun, J.L., et al. (2012). An animal model of MYC-driven medulloblastoma. Cancer Cell 21, 155-167.   DOI   ScienceOn
41 Pugh, T.J., Weeraratne, S.D., Archer, T.C., Pomeranz Krummel, D. A., Auclair, D., Bochicchio, J., Carneiro, M.O., Carter, S.L., Cibulskis, K., Erlich, R.L., et al. (2012). Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 488, 106-110.   DOI   ScienceOn
42 Puliyappadamba, V.T., Wu, W., Bevis, D., Zhang, L., Polin, L., Kilkuskie, R., Finley, R.L. Jr., Larsen, S.D., Levi, E., Miller, F.R., et al. (2011). Antagonists of anaphase-promoting complex (APC)-2-cell cycle and apoptosis regulatory protein (CARP)-1 interaction are novel regulators of cell growth and apoptosis. J. Biol. Chem. 286, 38000-38017.   DOI   ScienceOn
43 Sakakibara, S., and Okano, H. (1997). Expression of neural RNAbinding proteins in the postnatal CNS: implications of their roles in neuronal and glial cell development. J. Neurosci. 17, 8300-8312.
44 Sakakibara, S., Imai, T., Hamaguchi, K., Okabe, M., Aruga, J., Nakajima, K., Yasutomi, D., Nagata, T., Kurihara, Y., Uesugi, S., et al. (1996). Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev. Biol. 176, 230-242.   DOI   ScienceOn
45 Northcott, P.A., Korshunov, A., Witt, H., Hielscher, T., Eberhart, C.G., Mack, S., Bouffet, E., Clifford, S.C., Hawkins, C.E., French, P., et al. (2011). Medulloblastoma comprises four distinct molecular variants. J. Clin. Oncol. 29, 1408-1414.   DOI   ScienceOn
46 Moghbeli, M., Forghanifard, M.M., Aarabi, A., Mansourian, A., and Abbaszadegan, M.R. (2013). Clinicopathological sex- related relevance of Musashi1 mRNA expression in esophageal squamous cell carcinoma patients. Pathol. Oncol Res. [Epub ahead of print]
47 Nakamura, M., Okano, H., Blendy, J.A., and Montell, C. (1994). Musashi, a neural RNA-binding protein required for Drosophila adult external sensory organ development. Neuron 13, 67-81.   DOI   ScienceOn
48 Nakano, A., Kanemura, Y., Mori, K., Kodama, E., Yamamoto, A., Sakamoto, H., Nakamura, Y., Okano, H., Yamasaki, M., and Arita, N. (2007). Expression of the Neural RNA-binding protein Musashi1 in pediatric brain tumors. Pediatr. Neurosurg. 43, 279-284.   DOI   ScienceOn
49 Northcott, P.A., Korshunov, A., Pfister, S.M., and Taylor, M.D. (2012a). The clinical implications of medulloblastoma subgroups. Nat. Rev. Neurol. 8, 340-351.   DOI   ScienceOn
50 Reifenberger, J., Wolter, M., Weber, R.G., Megahed, M., Ruzicka, T., Lichter, P., and Reifenberger, G. (1998). Missense mutations in SMOH in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system. Cancer Res. 58, 1798-1803.
51 Remke, M., Hielscher, T., Korshunov, A., Northcott, P.A., Bender, S., Kool, M., Westermann, F., Benner, A., Cin, H., Ryzhova, M., et al. (2011). FSTL5 is a marker of poor prognosis in non-WNT/non-SHH medulloblastoma. J. Clin. Oncol. 29, 3852-3861.   DOI   ScienceOn
52 Robinson, G., Parker, M., Kranenburg, T.A., Lu, C., Chen, X., Ding, L., Phoenix, T.N., Hedlund, E., Wei, L., Zhu, X., et al. (2012). Novel mutations target distinct subgroups of medulloblastoma. Nature 488, 43-48.   DOI   ScienceOn
53 Remke, M., Ramaswamy, V., Peacock, J., Shih, D.J., Koelsche, C., Northcott, P.A., Hill, N., Cavalli, F.M., Kool, M., Wang, X., et al. (2013). TERT promoter mutations are highly recurrent in SHH subgroup medulloblastoma. Acta Neuropathol. 126, 917-929.   DOI   ScienceOn
54 Richter, K., Good, P.J., and Dawid, I.B. (1990). A developmentally regulated, nervous system-specific gene in Xenopus encodes a putative RNA-binding protein. New Biol. 2, 556-565.
55 Rishi, A.K., Zhang, L., Yu, Y., Jiang, Y., Nautiyal, J., Wali, A., Fontana, J.A., Levi, E., and Majumdar, A.P. (2006). Cell cycleand apoptosis-regulatory protein-1 is involved in apoptosis signaling by epidermal growth factor receptor. J. Biol. Chem. 281, 13188-13198.   DOI   ScienceOn
56 Soulat, D., Burckstummer, T., Westermayer, S., Goncalves, A., Bauch, A., Stefanovic, A., Hantschel, O., Bennett, K.L., Decker, T., and Superti-Furga, G. (2008). The DEAD-box helicase DDX3X is a critical component of the TANK-binding kinase 1-dependent innate immune response. EMBO J. 27, 2135-2146.   DOI   ScienceOn
57 Sugiyama-Nakagiri, Y., Akiyama, M., Shibata, S., Okano, H., and Shimizu, H. (2006). Expression of RNA-binding protein Musashi in hair follicle development and hair cycle progression. Am. J. Pathol. 168, 80-92.   DOI   ScienceOn
58 Sun, M., Zhou, T., Jonasch, E., and Jope, R.S. (2013). DDX3 regulates DNA damage-induced apoptosis and p53 stabilization. Biochim. Biophys. Acta 1833, 1489-1497.   DOI   ScienceOn
59 Putnam, A.A., and Jankowsky, E. (2013). DEAD-box helicases as integrators of RNA, nucleotide and protein binding. Biochim. Biophys. Acta 1829, 884-893.   DOI   ScienceOn
60 Sureban, S.M., May, R., George, R.J., Dieckgraefe, B.K., McLeod, H.L., Ramalingam, S., Bishnupuri, K.S., Natarajan, G., Anant, S., and Houchen, C.W. (2008). Knockdown of RNA binding protein musashi-1 leads to tumor regression in vivo. Gastroenterology 134, 1448-1458.   DOI   ScienceOn
61 Radi, M., Falchi, F., Garbelli, A., Samuele, A., Bernardo, V., Paolucci, S., Baldanti, F., Schenone, S., Manetti, F., Maga, G., et al. (2012). Discovery of the first small molecule inhibitor of human DDX3 specifically designed to target the RNA binding site: towards the next generation HIV-1 inhibitors. Bioorg. Med. Chem. Lett. 22, 2094-2098.   DOI   ScienceOn
62 Raffel, C., Jenkins, R.B., Frederick, L., Hebrink, D., Alderete, B., Fults, D.W., and James, C.D. (1997). Sporadic medulloblastomas contain PTCH mutations. Cancer Res. 57, 842-845.
63 Scherrer, T., Mittal, N., Janga, S.C., and Gerber, A.P. (2010). A screen for RNA-binding proteins in yeast indicates dual functions for many enzymes. PLoS One 5, e15499.   DOI   ScienceOn
64 Schroder, M. (2010). Human DEAD-box protein 3 has multiple functions in gene regulation and cell cycle control and is a prime target for viral manipulation. Biochem. Pharmacol. 79, 297-306.   DOI   ScienceOn
65 Schroder, M. (2011). Viruses and the human DEAD-box helicase DDX3: inhibition or exploitation? Biochem. Soc. Trans. 39, 679-683.   DOI   ScienceOn
66 Schuller, U., Heine, V.M., Mao, J., Kho, A.T., Dillon, A.K., Han, Y.G., Huillard, E., Sun, T., Ligon, A.H., Qian, Y., et al. (2008). Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 14, 123-134.   DOI   ScienceOn
67 Sanchez-Diaz, P.C., Burton, T.L., Burns, S.C., Hung, J.Y., and Penalva, L.O. (2008). Musashi1 modulates cell proliferation genes in the medulloblastoma cell line Daoy. BMC Cancer 8, 280.   DOI   ScienceOn
68 Schwanhausser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., and Selbach, M. (2011). Global quantification of mammalian gene expression control. Nature 473, 337-342.   DOI   ScienceOn
69 Smoll, N.R. (2012). Relative survival of childhood and adult medulloblastomas and primitive neuroectodermal tumors (PNETs). Cancer 118, 1313-1322.   DOI   ScienceOn
70 Soto-Rifo, R., Rubilar, P.S., Limousin, T., de Breyne, S., Decimo, D., and Ohlmann, T. (2012). DEAD-box protein DDX3 associates with eIF4F to promote translation of selected mRNAs. EMBO J. 31, 3745-3756.   DOI
71 Sawyers, C. (2004). Targeted cancer therapy. Nature 432, 294-297.   DOI   ScienceOn
72 Wang, X.Y., Yin, Y., Yuan, H., Sakamaki, T., Okano, H., and Glazer, R.I. (2008). Musashi1 modulates mammary progenitor cell expansion through proliferin-mediated activation of the Wnt and Notch pathways. Mol. Cell. Biol. 28, 3589-3599.   DOI   ScienceOn
73 Wang, X.Y., Penalva, L.O., Yuan, H., Linnoila, R.I., Lu, J., Okano, H., and Glazer, R.I. (2010). Musashi1 regulates breast tumor cell proliferation and is a prognostic indicator of poor survival. Mol. Cancer 9, 221.   DOI   ScienceOn
74 Wang, X.Y., Yu, H., Linnoila, R.I., Li, L., Li, D., Mo, B., Okano, H., Penalva, L.O., and Glazer, R.I. (2013). Musashi1 as a potential thera- peutic target and diagnostic marker for lung cancer. Oncotarget 4, 739-750.
75 Wilkie, G.S., Dickson, K.S., and Gray, N.K. (2003). Regulation of mRNA translation by 5'- and 3'-UTR-binding factors. Trends Biochem. Sci. 28, 182-188.   DOI   ScienceOn
76 Yedavalli, V.S., Neuveut, C., Chi, Y.H., Kleiman, L., and Jeang, K.T. (2004). Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell 119, 381-392.   DOI   ScienceOn
77 Wilson, D., Pethica, R., Zhou, Y., Talbot, C., Vogel, C., Madera, M., Chothia, C., and Gough, J. (2009). SUPERFAMILY--sophisticated comparative genomics, data mining, visualization and phylogeny. Nucleic Acids Res. 37, D380-386.   DOI   ScienceOn
78 Yang, Z.J., Ellis, T., Markant, S.L., Read, T.A., Kessler, J.D., Bourboulas, M., Schuller, U., Machold, R., Fishell, G., Rowitch, D.H., et al. (2008). Medulloblastoma can be initiated by deletion of Patched in lineage-restricted progenitors or stem cells. Cancer Cell 14, 135-145.   DOI   ScienceOn
79 Yauch, R.L., Dijkgraaf, G.J., Alicke, B., Januario, T., Ahn, C.P., Holcomb, T., Pujara, K., Stinson, J., Callahan, C.A., Tang, T., et al. (2009). Smoothened mutation confers resistance to a Hedgehog pathway inhibitor in medulloblastoma. Science 326, 572-574.   DOI   ScienceOn
80 Yokota, N., Mainprize, T.G., Taylor, M.D., Kohata, T., Loreto, M.,Ueda, S., Dura, W., Grajkowska, W., Kuo, J.S., and Rutka, J.T.(2004). Identification of differentially expressed and developmentallyregulated genes in medulloblastoma using suppressionsubtraction hybridization. Oncogene 23, 3444-3453.   DOI   ScienceOn
81 Zhou, J., Shum, K.T., Burnett, J.C., and Rossi, J.J. (2013). Nanoparticle-based delivery of RNAi therapeutics: progress and challenges. Pharmaceuticals 6, 85-107.   DOI   ScienceOn
82 Toda, M., Iizuka, Y., Yu, W., Imai, T., Ikeda, E., Yoshida, K., Kawase, T., Kawakami, Y., Okano, H., and Uyemura, K. (2001). Expression of the neural RNA-binding protein Musashi1 in human gliomas. Glia 34, 1-7.   DOI   ScienceOn
83 Lindqvist, L., Oberer, M., Reibarkh, M., Cencic, R., Bordeleau, M.E,. Vogt, E., Marintchev, A., Tanaka, J., Fagotto, F., Altmann, M., et al. (2008). Selective pharmacological targeting of a DEAD box RNA helicase. PLoS One 3, e1583.   DOI   ScienceOn
84 Tsvetanova, N.G., Klass, D.M., Salzman, J., and Brown, P.O. (2010). Proteome-wide search reveals unexpected RNA-binding proteins in Saccharomyces cerevisiae. PLoS One 5, pii: e12671.   DOI
85 Vo, D.T., Subramaniam, D., Remke, M., Burton, T.L., Uren, P.J., Gelfond, J.A., de Sousa Abreu, R., Burns, S.C., Qiao, M., Suresh, U., et al. (2012). The RNA-binding protein Musashi1 affects medulloblastoma growth via a network of cancer-related genes and is an indicator of poor prognosis. Am. J. Pathol. 181, 1762-1772.   DOI   ScienceOn
86 Lee, M.J., Hatton, B.A., Villavicencio, E.H., Khanna, P.C., Friedman, S.D., Ditzler, S., Pullar, B., Robison, K., White, K.F., Tunkey, C., et al. (2012). Hedgehog pathway inhibitor saridegib (IPI-926) increases lifespan in a mouse medulloblastoma model. Proc. Natl. Acad. Sci. USA 109, 7859-7864.   DOI
87 Li, D., Peng, X., Yan, D., Tang, H., Huang, F., Yang, Y., and Peng, Z. (2011). Msi-1 is a predictor of survival and a novel therapeutic target in colon cancer. Ann. Surg. Oncol. 18, 2074-2083.   DOI
88 Linder, P., and Jankowsky, E. (2011). From unwinding to clamping - the DEAD box RNA helicase family. Nat. Rev. Mol. Cell Biol. 12, 505-516.   DOI   ScienceOn
89 Liu, D.C., Yang, Z.L., and Jiang, S. (2010). Identification of musashi-1 and ALDH1 as carcinogenesis, progression, and poor-prognosis related biomarkers for gallbladder adenocarcinoma. Cancer Biomark 8, 113-121.
90 Lorkovic, Z.J. (2012). RNA binding proteins. Austin, Tex., Landes Bioscience.
91 Kong, D.S., Kim, M.H., Park, W.Y., Suh, Y.L., Lee, J.I., Park, K., Kim, J.H., and Nam, D.H. (2008). The progression of gliomas is associated with cancer stem cell phenotype. Oncol. Rep. 19, 639-643.
92 Kool, M., Koster, J., Bunt, J., Hasselt, N.E., Lakeman, A., van Sluis, P., Troost, D., Meeteren, N.S., Caron, H.N., Cloos, J., et al. (2008). Integrated genomics identifies five medulloblastoma subtypes with distinct genetic profiles, pathway signatures and clinicopathological features. PLoS One 3, e3088.   DOI   ScienceOn
93 Kuwako, K., Kakumoto, K., Imai, T., Igarashi, M., Hamakubo, T., Sakakibara, S., Tessier-Lavigne, M., Okano, H.J., and Okano, H. (2010). Neural RNA-binding protein Musashi1 controls midline crossing of precerebellar neurons through posttranscriptional regulation of Robo3/Rig-1 expression. Neuron 67, 407-421.   DOI   ScienceOn
94 Kwong, A.D., Rao, B.G., and Jeang, K.T. (2005). Viral and cellular RNA helicases as antiviral targets. Nat. Rev. Drug Discov. 4, 845-853.   DOI   ScienceOn
95 Lai, M.C., Lee, Y.H., and Tarn, W.Y. (2008). The DEAD-box RNA helicase DDX3 associates with export messenger ribonucleoproteins as well as tip-associated protein and participates in translational control. Mol. Biol. Cell 19, 3847-3858.   DOI   ScienceOn
96 Lai, M.C., Chang, W.C., Shieh, S.Y., and Tarn, W.Y. (2010). DDX3 regulates cell growth through translational control of cyclin E1. Mol. Cell. Biol. 30, 5444-5453.   DOI   ScienceOn
97 Lane, D. (1988). Enlarged family of putative helicases. Nature 334, 478.
98 Forbes, S.A., Bindal, N., Bamford, S., Cole, C., Kok, C.Y., Beare, D., Jia, M., Shepherd, R., Leung, K., Menzies, A., et al. (2011). COSMIC: mining complete cancer genomes in the catalogue of somatic mutations in cancer. Nucleic Acids Res. 39, D945-950.   DOI
99 Kool, M., Korshunov, A., Remke, M., Jones, D.T., Schlanstein, M., Northcott, P.A., Cho, Y.J., Koster, J., Schouten-van Meeteren, A., van Vuurden, D., et al. (2012). Molecular subgroups of medulloblastoma: an international meta-analysis of transcriptome, genetic aberrations, and clinical data of WNT, SHH, Group 3, and Group 4 medulloblastomas. Acta Neuropathol. 123, 473-484.   DOI   ScienceOn
100 Hambardzumyan, D., Becher, O.J., Rosenblum, M.K., Pandolfi, P.P., Manova-Todorova, K., and Holland, E.C. (2008b). PI3K path- way regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo. Genes Dev. 22, 436-448.   DOI   ScienceOn
101 Clark, J., Lu, Y.J., Sidhar, S.K., Parker, C., Gill, S., Smedley, D., Hamoudi, R., Linehan, W.M., Shipley, J., and Cooper, C.S. (1997). Fusion of splicing factor genes PSF and NonO (p54nrb) to the TFE3 gene in papillary renal cell carcinoma. Oncogene 15, 2233-2239.   DOI
102 Castello, A., Fischer, B., Eichelbaum, K., Horos, R., Beckmann, B.M., Strein, C., Davey, N.E., Humphreys, D.T., Preiss, T., Steinmetz, L.M., et al. (2012). Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149, 1393-1406.   DOI   ScienceOn
103 Schiffner, S., Zimara, N., Schmid, R., and Bosserhoff, A.K. (2011). p54nrb is a new regulator of progression of malignant melanoma. Carcinogenesis 32, 1176-1182.   DOI   ScienceOn
104 Adamson, D.C., Shi, Q., Wortham, M., Northcott, P.A., Di, C., Duncan, C.G., Li, J., McLendon, R.E., Bigner, D.D., Taylor, M.D., et al. (2010). OTX2 is critical for the maintenance and progression of Shh-independent medulloblastomas. Cancer Res. 70, 181-191.   DOI   ScienceOn
105 Muto, J., Imai, T., Ogawa, D., Nishimoto, Y., Okada, Y., Mabuchi, Y., Kawase, T., Iwanami, A., Mischel, P.S., Saya, H., et al. (2012). RNA-binding protein Musashi1 modulates glioma cell growth through the post-transcriptional regulation of Notch and PI3 kinase/Akt signaling pathways. PLoS One 7, e33431.   DOI
106 Rishi, A.K., Zhang, L., Boyanapalli, M., Wali, A., Mohammad, R.M., Yu, Y., Fontana, J.A., Hatfield, J.S., Dawson, M.I., Majumdar, A.P., et al. (2003). Identification and characterization of a cell cycle and apoptosis regulatory protein-1 as a novel mediator of apoptosis signaling by retinoid CD437. J. Biol. Chem. 278, 33422-33435.   DOI   ScienceOn
107 Vogel, C., Abreu Rde, S., Ko, D., Le, S.Y., Shapiro, B.A., Burns, S.C., Sandhu, D., Boutz, D.R., Marcotte, E.M., and Penalva, L.O. (2010). Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line. Mol. Syst. Biol. 6, 400.
108 Thompson, M.C., Fuller, C., Hogg, T.L., Dalton, J., Finkelstein, D., Lau, C.C., Chintagumpala, M., Adesina, A., Ashley, D.M., Kellie, S.J., et al. (2006). Genomics identifies medulloblastoma subgroups that are enriched for specific genetic alterations. J. Clin. Oncol. 24, 1924-1931.   DOI   ScienceOn