MYCN and HDAC2 cooperate to repress miR-183 signaling in neuroblastoma

Nucleic Acids Research

Volumn 41, Issue 12, 2013, Pages 6018-6033

  Lodrini, Marco ^a   Oehme, Ina ^a   Schroeder, Christina ^a   Milde, Till ^a,b   Schier, Marie C ^a   Kopp Schneider, Annette ^a   Schulte, Johannes H ^c   Fischer, Matthias ^d   De Preter, Katleen ^e   Pattyn, Filip ^e   Castoldi, Mirco ^f   Muckenthaler, Martina U ^b,f   Kulozik, Andreas E ^b   Westermann, Frank ^a   Witt, Olaf ^a,b   Deubzer, Hedwig E ^a,b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

^d UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^e GHENT UNIVERSITY HOSPITAL   (Belgium)

^f EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE 2; MICRORNA; MICRORNA 183; MYCN PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; COLONY FORMATION; CONTROLLED STUDY; HISTONE ACETYLATION; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR PATHOLOGY; MOUSE; NEUROBLASTOMA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; TUMOR XENOGRAFT;

ANIMALS; CELL DEATH; CELL LINE, TUMOR; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE INHIBITORS; HUMANS; MICE; MICRORNAS; NEUROBLASTOMA; NUCLEAR PROTEINS; ONCOGENE PROTEINS; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION;

EID: 84880215077     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt346     Document Type: Article

References (65)

1. Cole, K.A. and Maris, J.M. (2012) New strategies in refractory and recurrent neuroblastoma: translational opportunities to impact patient outcome. Clin. Cancer Res., 18, 2423-2428.
2. Brodeur, G.M. (2003) Neuroblastoma: biological insights into a clinical enigma. Nat. Rev. Cancer, 3, 203-216.
3. Schwab, M., Westermann, F., Hero, B. and Berthold, F. (2003) Neuroblastoma: biology and molecular and chromosomal pathology. Lancet Oncol., 4, 472-480.
4. Westermark, U.K., Wilhelm, M., Frenzel, A. and Henriksson, M.A. (2011) The MYCN oncogene and differentiation in neuroblastoma. Semin. Cancer Biol., 21, 256-266.
5. Bartel, D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
6. Filipowicz, W., Bhattacharyya, S.N. and Sonenberg, N. (2008) Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat. Rev. Genet., 9, 102-114.
7. Garzon, R., Calin, G.A. and Croce, C.M. (2009) MicroRNAs in Cancer. Annu. Rev. Med., 60, 167-179.
8. Calin, G.A. and Croce, C.M. (2006) MicroRNA signatures in human cancers. Nat. Rev. Cancer, 6, 857-866.
9. Schulte, J.H., Horn, S., Otto, T., Samans, B., Heukamp, L.C., Eilers, U.C., Krause, M., Astrahantseff, K., Klein-Hitpass, L., Buettner, R. et al. (2008) MYCN regulates oncogenic MicroRNAs in neuroblastoma. Int. J. Cancer, 122, 699-704.
10. Chen, Y. and Stallings, R.L. (2007) Differential patterns of microRNA expression in neuroblastoma are correlated with prognosis, differentiation, and apoptosis. Cancer Res., 67, 976-983.
11. Schulte, J.H., Schowe, B., Mestdagh, P., Kaderali, L., Kalaghatgi, P., Schlierf, S., Vermeulen, J., Brockmeyer, B., Pajtler, K., Thor, T. et al. (2010) Accurate prediction of neuroblastoma outcome based on mirna expression profiles. Int. J. Cancer, 127, 2374-2385.
12. Shohet, J.M., Ghosh, R., Coarfa, C., Ludwig, A., Benham, A.L., Chen, Z., Patterson, D.M., Barbieri, E., Mestdagh, P., Sikorski, D.N. et al. (2011) A genome-wide search for promoters that respond to increased MYCN reveals both new oncogenic and tumor suppressor microRNAs associated with aggressive neuroblastoma. Cancer Res., 71, 3841-3851.
13. Scott, G.K., Mattie, M.D., Berger, C.E., Benz, S.C. and Benz, C.C. (2006) Rapid alteration of microRNA levels by histone deacetylase inhibition. Cancer Res., 66, 1277-1281.
14. Yang, X.J. and Seto, E. (2008) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol., 9, 206-218.
15. de Ruijter, A.J., van Gennip, A.H., Caron, H.N., Kemp, S. and van Kuilenburg, A.B. (2003) Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem. J., 370, 737-749.
16. Bolden, J.E., Peart, M.J. and Johnstone, R.W. (2006) Anticancer activities of histone deacetylase inhibitors. Nat. Rev. Drug Discov., 5, 769-784.
17. Witt, O., Deubzer, H.E., Milde, T. and Oehme, I. (2009) HDAC family: What are the cancer relevant targets? Cancer Lett., 277, 8-21.
18. Fraga, M.F., Ballestar, E., Villar-Garea, A., Boix-Chornet, M., Espada, J., Schotta, G., Bonaldi, T., Haydon, C., Ropero, S., Petrie, K. et al. (2005) Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat. Genet., 37, 391-400.
19. Deubzer, H.E., Ehemann, V., Westermann, F., Heinrich, R., Mechtersheimer, G., Kulozik, A.E., Schwab, M. and Witt, O. (2008) Histone deacetylase inhibitor Helminthosporium carbonum (HC)-toxin suppresses the malignant phenotype of neuroblastoma cells. Int. J. Cancer, 122, 1891-1900.
20. Witt, O., Deubzer, H.E., Lodrini, M., Milde, T. and Oehme, I. (2009) Targeting histone deacetylases in neuroblastoma. Curr. Pharm. Des., 15, 436-447.
21. Schmitt, M. and Pawlita, M. (2009) High-throughput detection and multiplex identification of cell contaminations. Nucleic Acids Res., 37, e119.
22. Fischer, M., Skowron, M. and Berthold, F. (2005) Reliable transcript quantification by real-time reverse transcriptase-polymerase chain reaction in primary neuroblastoma using normalization to averaged expression levels of the control genes HPRT1 and SDHA. J. Mol. Diagn, 7, 89-96.
23. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25.
24. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G. and Durbin, R. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25, 2078-2079.
25. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W. et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol., 9, R137.
26. Westermann, F., Muth, D., Benner, A., Bauer, T., Henrich, K.O., Oberthuer, A., Brors, B., Beissbarth, T., Vandesompele, J., Pattyn, F. et al. (2008) Distinct transcriptional MYCN/c-MYC activities are associated with spontaneous regression or malignant progression in neuroblastomas. Genome Biol., 9, R150.
27. Strieder, V. and Lutz, W. (2003) E2F proteins regulate MYCN expression in neuroblastomas. J. Biol. Chem., 278, 2983-2989.
28. Lee, T.I., Johnstone, S.E. and Young, R.A. (2006) Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc., 1, 729-748.
29. Robinson, J.T., Thorvaldsdottir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G. and Mesirov, J.P. (2011) Integrative genomics viewer. Nat. Biotechnol., 29, 24-26.
30. Shao, W., Growney, J.D., Feng, Y., O'Connor, G., Pu, M., Zhu, W., Yao, Y.M., Kwon, P., Fawell, S. and Atadja, P. (2010) Activity of deacetylase inhibitor panobinostat (LBH589) in cutaneous T-cell lymphoma models: defining molecular mechanisms of resistance. Int. J. Cancer, 127, 2199-2208.
31. Arrowsmith, C.H., Bountra, C., Fish, P.V., Lee, K. and Schapira, M. (2012) Epigenetic protein families: a new frontier for drug discovery. Nat. Rev. Drug Discov., 11, 384-400.
32. Tweddle, D.A., Malcolm, A.J., Bown, N., Pearson, A.D. and Lunec, J. (2001) Evidence for the development of p53 mutations after cytotoxic therapy in a neuroblastoma cell line. Cancer Res., 61, 8-13.
33. Barretina, J., Caponigro, G., Stransky, N., Venkatesan, K., Margolin, A.A., Kim, S., Wilson, C.J., Lehar, J., Kryukov, G.V., Sonkin, D. et al. (2012) The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature, 483, 603-607.
34. Wang, G., Mao, W. and Zheng, S. (2008) MicroRNA-183 regulates Ezrin expression in lung cancer cells. FEBS Lett., 582, 3663-3668.
35. Khan, N., Jeffers, M., Kumar, S., Hackett, C., Boldog, F., Khramtsov, N., Qian, X., Mills, E., Berghs, S.C., Carey, N. et al. (2008) Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem. J., 409, 581-589.
36. Krennhrubec, K., Marshall, B.L., Hedglin, M., Verdin, E. and Ulrich, S.M. (2007) Design and evaluation of 'Linkerless' hydroxamic acids as selective HDAC8 inhibitors. Bioorg. Med. Chem. Lett., 17, 2874-2878.
37. Minucci, S. and Pelicci, P.G. (2006) Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat. Rev. Cancer, 6, 38-51.
38. Marshall, G.M., Gherardi, S., Xu, N., Neiron, Z., Trahair, T., Scarlett, C.J., Chang, D.K., Liu, P.Y., Jankowski, K., Iraci, N. et al. (2010) Transcriptional upregulation of histone deacetylase 2 promotes Myc-induced oncogenic effects. Oncogene, 29, 5957-5968.
39. Ozsolak, F., Poling, L.L., Wang, Z., Liu, H., Liu, X.S., Roeder, R.G., Zhang, X., Song, J.S. and Fisher, D.E. (2008) Chromatin structure analyses identify miRNA promoters. Genes Dev., 22, 3172-3183.
40. Chien, C.H., Sun, Y.M., Chang, W.C., Chiang-Hsieh, P.Y., Lee, T.Y., Tsai, W.C., Horng, J.T., Tsou, A.P. and Huang, H.D. (2011) Identifying transcriptional start sites of human microRNAs based on high-throughput sequencing data. Nucleic Acids Res., 39, 9345-9356.
41. Ahringer, J. (2000) NuRD and SIN3 histone deacetylase complexes in development. Trends Genet., 16, 351-356.
42. Motoyama, K., Inoue, H., Takatsuno, Y., Tanaka, F., Mimori, K., Uetake, H., Sugihara, K. and Mori, M. (2009) Over-and under-expressed microRNAs in human colorectal cancer. Int. J. Oncol., 34, 1069-1075.
43. Bandres, E., Cubedo, E., Agirre, X., Malumbres, R., Zarate, R., Ramirez, N., Abajo, A., Navarro, A., Moreno, I., Monzo, M. et al. (2006) Identification by Real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Mol. Cancer, 5, 29.
44. Schaefer, A., Jung, M., Mollenkopf, H.J., Wagner, I., Stephan, C., Jentzmik, F., Miller, K., Lein, M., Kristiansen, G. and Jung, K. (2010) Diagnostic and prognostic implications of microRNA profiling in prostate carcinoma. Int. J. Cancer, 126, 1166-1176.
45. Li, J., Fu, H., Xu, C., Tie, Y., Xing, R., Zhu, J., Qin, Y., Sun, Z. and Zheng, X. (2010) miR-183 inhibits TGF-beta1-induced apoptosis by downregulation of PDCD4 expression in human hepatocellular carcinoma cells. BMC Cancer, 10, 354.
46. Dahiya, N., Sherman-Baust, C.A., Wang, T.L., Davidson, B., Shih Ie, M., Zhang, Y., Wood, W. III, Becker, K.G. and Morin, P.J. (2008) MicroRNA expression and identification of putative miRNA targets in ovarian cancer. PLoS One, 3, e2436.
47. Shimono, Y., Zabala, M., Cho, R.W., Lobo, N., Dalerba, P., Qian, D., Diehn, M., Liu, H., Panula, S.P., Chiao, E. et al. (2009) Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell, 138, 592-603.
48. Zhu, J., Feng, Y., Ke, Z., Yang, Z., Zhou, J., Huang, X. and Wang, L. (2012) Down-regulation of miR-183 promotes migration and invasion of osteosarcoma by targeting Ezrin. Am. J. Pathol., 180, 2440-2451.
49. Li, G., Luna, C., Qiu, J., Epstein, D.L. and Gonzalez, P. (2010) Targeting of integrin beta1 and kinesin 2alpha by microRNA 183. J. Biol. Chem., 285, 5461-5471.
50. Rozzo, C., Chiesa, V., Caridi, G., Pagnan, G. and Ponzoni, M. (1997) Induction of apoptosis in human neuroblastoma cells by abrogation of integrin-mediated cell adhesion. Int. J. Cancer, 70, 688-698.
51. Wellner, U., Schubert, J., Burk, U.C., Schmalhofer, O., Zhu, F., Sonntag, A., Waldvogel, B., Vannier, C., Darling, D., zur Hausen, A. et al. (2009) The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat. Cell Biol., 11, 1487-1495.
52. Cui, H., Hu, B., Li, T., Ma, J., Alam, G., Gunning, W.T. and Ding, H.F. (2007) Bmi-1 is essential for the tumorigenicity of neuroblastoma cells. Am. J. Pathol., 170, 1370-1378.
53. Tanaka, H., Sasayama, T., Tanaka, K., Nakamizo, S., Nishihara, M., Mizukawa, K., Kohta, M., Koyama, J., Miyake, S., Taniguchi, M. et al. (2013) MicroRNA-183 upregulates HIF-1alpha by targeting isocitrate dehydrogenase 2 (IDH2) in glioma cells. J. Neurooncol., 111, 273-283.
54. Kim, S.J., Yune, T.Y., Han, C.T., Kim, Y.C., Oh, Y.J., Markelonis, G.J. and Oh, T.H. (2007) Mitochondrial isocitrate dehydrogenase protects human neuroblastoma SH-SY5Y cells against oxidative stress. J. Neurosci. Res., 85, 139-152.
55. Oehme, I., Deubzer, H.E., Wegener, D., Pickert, D., Linke, J.P., Hero, B., Kopp-Schneider, A., Westermann, F., Ulrich, S.M., von Deimling, A. et al. (2009) Histone deacetylase 8 in neuroblastoma tumorigenesis. Clin. Cancer Res., 15, 91-99.
56. Kim, M.K. and Carroll, W.L. (2004) Autoregulation of the N-myc gene is operative in neuroblastoma and involves histone deacetylase 2. Cancer, 101, 2106-2115.
57. Liu, T., Tee, A.E., Porro, A., Smith, S.A., Dwarte, T., Liu, P.Y., Iraci, N., Sekyere, E., Haber, M., Norris, M.D. et al. (2007) Activation of tissue transglutaminase transcription by histone deacetylase inhibition as a therapeutic approach for Myc oncogenesis. Proc. Natl Acad. Sci. USA, 104, 18682-18687.
58. Iraci, N., Diolaiti, D., Papa, A., Porro, A., Valli, E., Gherardi, S., Herold, S., Eilers, M., Bernardoni, R., Della Valle, G. et al. (2011) A SP1/MIZ1/MYCN repression complex recruits HDAC1 at the TRKA and p75NTR promoters and affects neuroblastoma malignancy by inhibiting the cell response to NGF. Cancer Res., 71, 404-412.
59. Fan, J.B., Yeakley, J.M., Bibikova, M., Chudin, E., Wickham, E., Chen, J., Doucet, D., Rigault, P., Zhang, B., Shen, R. et al. (2004) A versatile assay for high-throughput gene expression profiling on universal array matrices. Genome Res., 14, 878-885.
60. Fan, J.B., Gunderson, K.L., Bibikova, M., Yeakley, J.M., Chen, J., Wickham Garcia, E., Lebruska, L.L., Laurent, M., Shen, R. and Barker, D. (2006) Illumina universal bead arrays. Methods Enzymol., 410, 57-73.
61. Galinsky, V.L. (2003) Automatic registration of microarray images. II. Hexagonal grid. Bioinformatics, 19, 1832-1836.
62. Kallio, M.A., Tuimala, J.T., Hupponen, T., Klemela, P., Gentile, M., Scheinin, I., Koski, M., Kaki, J. and Korpelainen, E.I. (2011) Chipster: user-friendly analysis software for microarray and other high-throughput data. BMC Genomics, 12, 507.
63. Muth, D., Ghazaryan, S., Eckerle, I., Beckett, E., Pohler, C., Batzler, J., Beisel, C., Gogolin, S., Fischer, M., Henrich, K.O. et al. (2010) Transcriptional repression of SKP2 is impaired in MYCN-amplified neuroblastoma. Cancer Res., 70, 3791-3802.
64. Oehme, I., Bosser, S. and Zornig, M. (2006) Agonists of an ecdysone-inducible mammalian expression system inhibit Fas Ligand-and TRAIL-induced apoptosis in the human colon carcinoma cell line RKO. Cell Death Differ., 13, 189-201.
65. Gao, L., Cueto, M.A., Asselbergs, F. and Atadja, P. (2002) Cloning and functional characterization of HDAC11, a novel member of the human histone deacetylase family. J. Biol. Chem., 277, 25748-25755.