CDK7 inhibition suppresses super-enhancer-linked oncogenic transcription in MYCN-driven cancer

Cell

Volumn 159, Issue 5, 2014, Pages 1126-1139

  Chipumuro, Edmond ^a,b   Marco, Eugenio ^c,d   Christensen, Camilla L ^c   Kwiatkowski, Nicholas ^e   Zhang, Tinghu ^b,c   Hatheway, Clark M ^a   Abraham, Brian J ^e   Sharma, Bandana ^a   Yeung, Caleb ^a,b   Altabef, Abigail ^c   Perez Atayde, Antonio ^a   Wong, Kwok Kin ^c   Yuan, Guo Cheng ^c,d   Gray, Nathanael S ^b,c   Young, Richard A ^e   George, Rani E ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLIN DEPENDENT KINASE 7; CYCLIN DEPENDENT KINASE INHIBITOR; MYC PROTEIN; THZ 1; UNCLASSIFIED DRUG; CYCLIN DEPENDENT KINASE; CYCLIN-DEPENDENT KINASE-ACTIVATING KINASE; MYCN PROTEIN, HUMAN; NUCLEAR PROTEIN; ONCOPROTEIN; PHENYLENEDIAMINE DERIVATIVE; PROTEIN KINASE INHIBITOR; PYRIMIDINE DERIVATIVE; THZ1 COMPOUND;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL CYCLE REGULATION; CONTROLLED STUDY; DOWN REGULATION; DRUG POTENCY; DRUG SELECTIVITY; ENZYME INHIBITION; FIBROBLAST; GENE AMPLIFICATION; GENE REPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MOUSE; MOUSE MODEL; NEUROBLASTOMA; NEUROBLASTOMA CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE MYC; TUMOR MODEL; TUMOR REGRESSION; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CYCLE; DISEASE MODEL; DRUG EFFECTS; METABOLISM; TUMOR CELL LINE;

ANIMALS; CELL CYCLE; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASES; DISEASE MODELS, ANIMAL; HUMANS; NEUROBLASTOMA; NUCLEAR PROTEINS; ONCOGENE PROTEINS; PHENYLENEDIAMINES; PROTEIN KINASE INHIBITORS; PYRIMIDINES; TRANSCRIPTION, GENETIC;

EID: 84911942289     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.10.024     Document Type: Article

References (75)

1. C. Arvanitis, and D.W. Felsher Conditional transgenic models define how MYC initiates and maintains tumorigenesis Semin. Cancer Biol. 16 2006 313 317
2. K. Boon, H.N. Caron, R. van Asperen, L. Valentijn, M.C. Hermus, P. van Sluis, I. Roobeek, I. Weis, P.A. Voûte, M. Schwab, and R. Versteeg N-myc enhances the expression of a large set of genes functioning in ribosome biogenesis and protein synthesis EMBO J. 20 2001 1383 1393
3. G.M. Brodeur, R.C. Seeger, M. Schwab, H.E. Varmus, and J.M. Bishop Amplification of N-myc in untreated human neuroblastomas correlates with advanced disease stage Science 224 1984 1121 1124
4. B. Chapuy, M.R. McKeown, C.Y. Lin, S. Monti, M.G. Roemer, J. Qi, P.B. Rahl, H.H. Sun, K.T. Yeda, and J.G. Doench Discovery and characterization of super-enhancer-associated dependencies in diffuse large B cell lymphoma Cancer Cell 24 2013 777 790
5. S.L. Cohn, H. Salwen, M.W. Quasney, N. Ikegaki, J.M. Cowan, C.V. Herst, R.H. Kennett, S.T. Rosen, J.A. DiGiuseppe, and G.M. Brodeur Prolonged N-myc protein half-life in a neuroblastoma cell line lacking N-myc amplification Oncogene 5 1990 1821 1827
6. J.E. Delmore, G.C. Issa, M.E. Lemieux, P.B. Rahl, J. Shi, H.M. Jacobs, E. Kastritis, T. Gilpatrick, R.M. Paranal, and J. Qi BET bromodomain inhibition as a therapeutic strategy to target c-Myc Cell 146 2011 904 917
7. M. Eilers, and R.N. Eisenman Myc's broad reach Genes Dev. 22 2008 2755 2766
8. R.P. Fisher, and D.O. Morgan A novel cyclin associates with MO15/CDK7 to form the CDK-activating kinase Cell 78 1994 713 724
9. J. Garriga, and X. Graña Cellular control of gene expression by T-type cyclin/CDK9 complexes Gene 337 2004 15 23
10. R.E. George, T. Sanda, M. Hanna, S. Fröhling, W. Luther 2nd, J. Zhang, Y. Ahn, W. Zhou, W.B. London, and P. McGrady Activating mutations in ALK provide a therapeutic target in neuroblastoma Nature 455 2008 975 978
11. K. Glover-Cutter, S. Larochelle, B. Erickson, C. Zhang, K. Shokat, R.P. Fisher, and D.L. Bentley TFIIH-associated Cdk7 kinase functions in phosphorylation of C-terminal domain Ser7 residues, promoter-proximal pausing, and termination by RNA polymerase II Mol. Cell. Biol. 29 2009 5455 5464
12. D. Hnisz, B.J. Abraham, T.I. Lee, A. Lau, V. Saint-André, A.A. Sigova, H.A. Hoke, and R.A. Young Super-enhancers in the control of cell identity and disease Cell 155 2013 934 947
13. M.J. Howard, M. Stanke, C. Schneider, X. Wu, and H. Rohrer The transcription factor dHAND is a downstream effector of BMPs in sympathetic neuron specification Development 127 2000 4073 4081
14. N.E. Kohl, E. Legouy, R.A. DePinho, P.D. Nisen, R.K. Smith, C.E. Gee, and F.W. Alt Human N-myc is closely related in organization and nucleotide sequence to c-myc Nature 319 1986 73 77
15. N. Kwiatkowski, T. Zhang, P.B. Rahl, B.J. Abraham, J. Reddy, S.B. Ficarro, A. Dastur, A. Amzallag, S. Ramaswamy, and B. Tesar Targeting transcription regulation in cancer with a covalent CDK7 inhibitor Nature 511 2014 616 620
16. W.L. Labisso, M. Wirth, N. Stojanovic, R.H. Stauber, A. Schnieke, R.M. Schmid, O.H. Krämer, D. Saur, and G. Schneider MYC directs transcription of MCL1 and eIF4E genes to control sensitivity of gastric cancer cells toward HDAC inhibitors Cell Cycle 11 2012 1593 1602
17. L.T. Lam, O.K. Pickeral, A.C. Peng, A. Rosenwald, E.M. Hurt, J.M. Giltnane, L.M. Averett, H. Zhao, R.E. Davis, and M. Sathyamoorthy Genomic-scale measurement of mRNA turnover and the mechanisms of action of the anti-cancer drug flavopiridol Genome Biol. 2 2001 RESEARCH0041
18. B. Langmead, C. Trapnell, M. Pop, and S.L. Salzberg Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Genome Biol. 10 2009 R25
19. S. Lapenna, and A. Giordano Cell cycle kinases as therapeutic targets for cancer Nat. Rev. Drug Discov. 8 2009 547 566
20. S. Larochelle, K.A. Merrick, M.E. Terret, L. Wohlbold, N.M. Barboza, C. Zhang, K.M. Shokat, P.V. Jallepalli, and R.P. Fisher Requirements for Cdk7 in the assembly of Cdk1/cyclin B and activation of Cdk2 revealed by chemical genetics in human cells Mol. Cell 25 2007 839 850
21. S. Larochelle, R. Amat, K. Glover-Cutter, M. Sansó, C. Zhang, J.J. Allen, K.M. Shokat, D.L. Bentley, and R.P. Fisher Cyclin-dependent kinase control of the initiation-to-elongation switch of RNA polymerase II Nat. Struct. Mol. Biol. 19 2012 1108 1115
22. T.I. Lee, S.E. Johnstone, and R.A. Young Chromatin immunoprecipitation and microarray-based analysis of protein location Nat. Protoc. 1 2006 729 748
23. C.Y. Lin, J. Lovén, P.B. Rahl, R.M. Paranal, C.B. Burge, J.E. Bradner, T.I. Lee, and R.A. Young Transcriptional amplification in tumor cells with elevated c-Myc Cell 151 2012 56 67
24. J. Lovén, D.A. Orlando, A.A. Sigova, C.Y. Lin, P.B. Rahl, C.B. Burge, D.L. Levens, T.I. Lee, and R.A. Young Revisiting global gene expression analysis Cell 151 2012 476 482
25. J. Lovén, H.A. Hoke, C.Y. Lin, A. Lau, D.A. Orlando, C.R. Vakoc, J.E. Bradner, T.I. Lee, and R.A. Young Selective inhibition of tumor oncogenes by disruption of super-enhancers Cell 153 2013 320 334
26. B.A. Malynn, I.M. de Alboran, R.C. O'Hagan, R. Bronson, L. Davidson, R.A. DePinho, and F.W. Alt N-myc can functionally replace c-myc in murine development, cellular growth, and differentiation Genes Dev. 14 2000 1390 1399
27. K.K. Matthay, J.G. Villablanca, R.C. Seeger, D.O. Stram, R.E. Harris, N.K. Ramsay, P. Swift, H. Shimada, C.T. Black, G.M. Brodeur Children's Cancer Group Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid N. Engl. J. Med. 341 1999 1165 1173
28. C.Y. McLean, D. Bristor, M. Hiller, S.L. Clarke, B.T. Schaar, C.B. Lowe, A.M. Wenger, and G. Bejerano GREAT improves functional interpretation of cis-regulatory regions Nat. Biotechnol. 28 2010 495 501
29. E.H. Mercer, G.W. Hoyle, R.P. Kapur, R.L. Brinster, and R.D. Palmiter The dopamine beta-hydroxylase gene promoter directs expression of E. coli lacZ to sympathetic and other neurons in adult transgenic mice Neuron 7 1991 703 716
30. Z. Nie, G. Hu, G. Wei, K. Cui, A. Yamane, W. Resch, R. Wang, D.R. Green, L. Tessarollo, and R. Casellas c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells Cell 151 2012 68 79
31. K. Nishikura, J. Erikson, A. ar-Rushdi, K. Huebner, and C.M. Croce The translocated c-myc oncogene of Raji Burkitt lymphoma cells is not expressed in human lymphoblastoid cells Proc. Natl. Acad. Sci. USA 82 1985 2900 2904
32. B. Palancade, and O. Bensaude Investigating RNA polymerase II carboxyl-terminal domain (CTD) phosphorylation FEBS 270 2003 3859 3870
33. A. Pattyn, X. Morin, H. Cremer, C. Goridis, and J.F. Brunet The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives Nature 399 1999 366 370
34. A. Puissant, S.M. Frumm, G. Alexe, C.F. Bassil, J. Qi, Y.H. Chanthery, E.A. Nekritz, R. Zeid, W.C. Gustafson, and P. Greninger Targeting MYCN in neuroblastoma by BET bromodomain inhibition Cancer Discov. 3 2013 308 323
35. J.T. Robinson, H. Thorvaldsdóttir, W. Winckler, M. Guttman, E.S. Lander, G. Getz, and J.P. Mesirov Integrative genomics viewer Nat. Biotechnol. 29 2011 24 26
36. M. Rossignol, I. Kolb-Cheynel, and J.M. Egly Substrate specificity of the cdk-activating kinase (CAK) is altered upon association with TFIIH EMBO J. 16 1997 1628 1637
37. A. Sabò, T.R. Kress, M. Pelizzola, S. de Pretis, M.M. Gorski, A. Tesi, M.J. Morelli, P. Bora, M. Doni, and A. Verrecchia Selective transcriptional regulation by Myc in cellular growth control and lymphomagenesis Nature 511 2014 488 492
38. M. Schuhmacher, and D. Eick Dose-dependent regulation of target gene expression and cell proliferation by c-Myc levels Transcription 4 2013 192 197
39. M. Schwab, K. Alitalo, K.H. Klempnauer, H.E. Varmus, J.M. Bishop, F. Gilbert, G. Brodeur, M. Goldstein, and J. Trent Amplified DNA with limited homology to myc cellular oncogene is shared by human neuroblastoma cell lines and a neuroblastoma tumour Nature 305 1983 245 248
40. R.C. Seeger, G.M. Brodeur, H. Sather, A. Dalton, S.E. Siegel, K.Y. Wong, and D. Hammond Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastomas N. Engl. J. Med. 313 1985 1111 1116
41. H. Serizawa, T.P. Mäkelä, J.W. Conaway, R.C. Conaway, R.A. Weinberg, and R.A. Young Association of Cdk-activating kinase subunits with transcription factor TFIIH Nature 374 1995 280 282
42. A. Slack, Z. Chen, R. Tonelli, M. Pule, L. Hunt, A. Pession, and J.M. Shohet The p53 regulatory gene MDM2 is a direct transcriptional target of MYCN in neuroblastoma Proc. Natl. Acad. Sci. USA 102 2005 731 736
43. L. Soucek, J. Whitfield, C.P. Martins, A.J. Finch, D.J. Murphy, N.M. Sodir, A.N. Karnezis, L.B. Swigart, S. Nasi, and G.I. Evan Modelling Myc inhibition as a cancer therapy Nature 455 2008 679 683
44. M. Stanke, D. Junghans, M. Geissen, C. Goridis, U. Ernsberger, and H. Rohrer The Phox2 homeodomain proteins are sufficient to promote the development of sympathetic neurons Development 126 1999 4087 4094
45. M. Toyoshima, H.L. Howie, M. Imakura, R.M. Walsh, J.E. Annis, A.N. Chang, J. Frazier, B.N. Chau, A. Loboda, and P.S. Linsley Functional genomics identifies therapeutic targets for MYC-driven cancer Proc. Natl. Acad. Sci. USA 109 2012 9545 9550
46. K. Tsarovina, A. Pattyn, J. Stubbusch, F. Müller, J. van der Wees, C. Schneider, J.F. Brunet, and H. Rohrer Essential role of Gata transcription factors in sympathetic neuron development Development 131 2004 4775 4786
47. M.L. Veronese, M. Ohta, J. Finan, P.C. Nowell, and C.M. Croce Detection of myc translocations in lymphoma cells by fluorescence in situ hybridization with yeast artificial chromosomes Blood 85 1995 2132 2138
48. A.R. Wasylishen, and L.Z. Penn Myc: the beauty and the beast Genes Cancer 1 2010 532 541
49. W.A. Whyte, D.A. Orlando, D. Hnisz, B.J. Abraham, C.Y. Lin, M.H. Kagey, P.B. Rahl, T.I. Lee, and R.A. Young Master transcription factors and mediator establish super-enhancers at key cell identity genes Cell 153 2013 307 319
50. A. Wyce, G. Ganji, K.N. Smitheman, C.W. Chung, S. Korenchuk, Y. Bai, O. Barbash, B. Le, P.D. Craggs, and M.T. McCabe BET inhibition silences expression of MYCN and BCL2 and induces cytotoxicity in neuroblastoma tumor models PLoS ONE 8 2013 e72967
51. Y. Zhang, T. Liu, C.A. Meyer, J. Eeckhoute, D.S. Johnson, B.E. Bernstein, C. Nusbaum, R.M. Myers, M. Brown, W. Li, and X.S. Liu Model-based analysis of ChIP-Seq (MACS) Genome Biol. 9 2008 R137
52. S. Ali, D.A. Heathcote, S.H. Kroll, A.S. Jogalekar, B. Scheiper, H. Patel, J. Brackow, A. Siwicka, M.J. Fuchter, and M. Periyasamy The development of a selective cyclin-dependent kinase inhibitor that shows antitumor activity Cancer Res. 69 2009 6208 6215
53. T. Berry, W. Luther, N. Bhatnagar, Y. Jamin, E. Poon, T. Sanda, D. Pei, B. Sharma, W.R. Vetharoy, and A. Hallsworth The ALK(F1174L) mutation potentiates the oncogenic activity of MYCN in neuroblastoma Cancer Cell 22 2012 117 130
54. K. Bettayeb, N. Oumata, A. Echalier, Y. Ferandin, J.A. Endicott, H. Galons, and L. Meijer CR8, a potent and selective, roscovitine-derived inhibitor of cyclin-dependent kinases Oncogene 27 2008 5797 5807
55. K.F. Byth, A. Thomas, G. Hughes, C. Forder, A. McGregor, C. Geh, S. Oakes, C. Green, M. Walker, and N. Newcombe AZD5438, a potent oral inhibitor of cyclin-dependent kinases 1, 2, and 9, leads to pharmacodynamic changes and potent antitumor effects in human tumor xenografts Mol. Cancer Ther. 8 2009 1856 1866
56. B.A. Carlson, M.M. Dubay, E.A. Sausville, L. Brizuela, and P.J. Worland Flavopiridol induces G1 arrest with inhibition of cyclin-dependent kinase (CDK) 2 and CDK4 in human breast carcinoma cells Cancer Res. 56 1996 2973 2978
57. L. Gautier, L. Cope, B.M. Bolstad, and R.A. Irizarry affy - analysis of Affymetrix GeneChip data at the probe level Bioinformatics 20 2004 307 315
58. I. Janoueix-Lerosey, D. Lequin, L. Brugières, A. Ribeiro, L. de Pontual, V. Combaret, V. Raynal, A. Puisieux, G. Schleiermacher, and G. Pierron Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma Nature 455 2008 967 970
59. T. Kamenecka, R. Jiang, X. Song, D. Duckett, W. Chen, Y.Y. Ling, J. Habel, J.D. Laughlin, J. Chambers, and M. Figuera-Losada Synthesis, biological evaluation, X-ray structure, and pharmacokinetics of aminopyrimidine c-jun-N-terminal kinase (JNK) inhibitors J. Med. Chem. 53 2010 419 431
60. L.J. Kong, J.T. Chang, A.H. Bild, and J.R. Nevins Compensation and specificity of function within the E2F family Oncogene 26 2007 321 327
61. H. Li, B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, R. Durbin 1000 Genome Project Data Processing Subgroup The Sequence Alignment/Map format and SAMtools Bioinformatics 25 2009 2078 2079
62. L. Meijer, A. Borgne, O. Mulner, J.P. Chong, J.J. Blow, N. Inagaki, M. Inagaki, J.G. Delcros, and J.P. Moulinoux Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5 FEBS 243 1997 527 536
63. R.N. Misra, H.Y. Xiao, K.S. Kim, S. Lu, W.C. Han, S.A. Barbosa, J.T. Hunt, D.B. Rawlins, W. Shan, and S.Z. Ahmed N-(cycloalkylamino)acyl-2-aminothiazole inhibitors of cyclin-dependent kinase 2. N-[5-[[[5-(1,1-dimethylethyl)-2-oxazolyl]methyl]thio]-2-thiazolyl]-4- piperidinecarboxamide (BMS-387032), a highly efficacious and selective antitumor agent J. Med. Chem. 47 2004 1719 1728
64. G. Mousseau, M.A. Clementz, W.N. Bakeman, N. Nagarsheth, M. Cameron, J. Shi, P. Baran, R. Fromentin, N. Chomont, and S.T. Valente An analog of the natural steroidal alkaloid cortistatin A potently suppresses Tat-dependent HIV transcription Cell Host Microbe 12 2012 97 108
65. G. Németh, Z. Varga, Z. Greff, G. Bencze, A. Sipos, C. Szántai-Kis, F. Baska, A. Gyuris, K. Kelemenics, and Z. Szathmáry Novel, selective CDK9 inhibitors for the treatment of HIV infection Curr. Med. Chem. 18 2011 342 358
66. A.R. Quinlan, and I.M. Hall BEDTools: a flexible suite of utilities for comparing genomic features Bioinformatics 26 2010 841 842
67. I. Schlosser, M. Hölzel, R. Hoffmann, H. Burtscher, F. Kohlhuber, M. Schuhmacher, R. Chapman, U.H. Weidle, and D. Eick Dissection of transcriptional programmes in response to serum and c-Myc in a human B-cell line Oncogene 24 2005 520 524
68. J. Shi, G. Manolikakes, C.H. Yeh, C.A. Guerrero, R.A. Shenvi, H. Shigehisa, and P.S. Baran Scalable synthesis of cortistatin A and related structures J. Am. Chem. Soc. 133 2011 8014 8027
69. G.K. Smyth, Y.H. Yang, and T. Speed Statistical issues in cDNA microarray data analysis Methods Mol. Biol. 224 2003 111 136
70. M.S. Squires, R.E. Feltell, N.G. Wallis, E.J. Lewis, D.M. Smith, D.M. Cross, J.F. Lyons, and N.T. Thompson Biological characterization of AT7519, a small-molecule inhibitor of cyclin-dependent kinases, in human tumor cell lines Mol. Cancer Ther. 8 2009 324 332
71. A. Subramanian, P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, M.A. Gillette, A. Paulovich, S.L. Pomeroy, T.R. Golub, E.S. Lander, and J.P. Mesirov Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles Proc. Natl. Acad. Sci. USA 102 2005 15545 15550
72. H. Thorvaldsdóttir, J.T. Robinson, and J.P. Mesirov Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration Brief. Bioinform. 14 2013 178 192
73. M.M. Tomayko, and C.P. Reynolds Determination of subcutaneous tumor size in athymic (nude) mice Cancer Chemother. Pharmacol. 24 1989 148 154
74. M.L. Whitfield, G. Sherlock, A.J. Saldanha, J.I. Murray, C.A. Ball, K.E. Alexander, J.C. Matese, C.M. Perou, M.M. Hurt, P.O. Brown, and D. Botstein Identification of genes periodically expressed in the human cell cycle and their expression in tumors Mol. Biol. Cell 13 2002 1977 2000
75. D. Yu, D. Cozma, A. Park, and A. Thomas-Tikhonenko Functional validation of genes implicated in lymphomagenesis: an in vivo selection assay using a Myc-induced B-cell tumor Ann. N Y Acad. Sci. 1059 2005 145 159