Activation of P-TEFb by Androgen Receptor-Regulated Enhancer RNAs in Castration-Resistant Prostate Cancer

Cell Reports

Volumn 15, Issue 3, 2016, Pages 599-610

  Zhao, Yu ^a,b,c   Wang, Liguo ^b   Ren, Shancheng ^d   Wang, Lan ^a,b,c   Blackburn, Patrick R ^a   McNulty, Melissa S ^a   Gao, Xu ^d   Qiao, Meng ^d   Vessella, Robert L ^e   Kohli, Manish ^b   Zhang, Jun ^b   Karnes, R Jeffrey ^b   Tindall, Donald J ^b   Kim, Youngsoo ^f   MacLeod, Robert ^f   Ekker, Stephen C ^a   Kang, Tiebang ^g   Sun, Yinghao ^d   Huang, Haojie ^a,b,c  

^a MAYO GRADUATE SCHOOL   (United States)

^b Mayo Clinic College of Medicine   (United States)

^c MAYO CLINIC CANCER CENTER   (United States)

^d SECOND MILITARY MEDICAL UNIVERSITY   (China)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^f ISIS PHARMACEUTICALS   (United States)

^g SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROSTATE SPECIFIC ANTIGEN; RNA POLYMERASE II; AR PROTEIN, HUMAN; CYCLIN T; PROTEIN BINDING; RNA; SERINE;

ARTICLE; CASTRATION RESISTANT PROSTATE CANCER; CELL GROWTH; CONTROLLED STUDY; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; PRIORITY JOURNAL; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; UPREGULATION; BIOLOGICAL MODEL; CELL PROLIFERATION; ENHANCER REGION; GENE EXPRESSION REGULATION; GENE LOCUS; GENETICS; METABOLISM; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

BASE SEQUENCE; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN T; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC LOCI; HUMANS; MALE; MODELS, BIOLOGICAL; NUCLEOTIDE MOTIFS; PHOSPHORYLATION; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROSTATE-SPECIFIC ANTIGEN; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; PROTEIN BINDING; RECEPTORS, ANDROGEN; RNA; RNA POLYMERASE II; SERINE; UP-REGULATION;

EID: 84962715515     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.03.038     Document Type: Article

References (54)

1. Antonarakis E.S., Lu C., Wang H., Luber B., Nakazawa M., Roeser J.C., Chen Y., Mohammad T.A., Chen Y., Fedor H.L., et al. AR-V7 and resistance to enzalutamide and abiraterone in prostate cancer. N. Engl. J. Med. 2014, 371:1028-1038.
2. Attard G., Reid A.H., Yap T.A., Raynaud F., Dowsett M., Settatree S., Barrett M., Parker C., Martins V., Folkerd E., et al. Phase I clinical trial of a selective inhibitor of CYP17, abiraterone acetate, confirms that castration-resistant prostate cancer commonly remains hormone driven. J. Clin. Oncol. 2008, 26:4563-4571.
3. Bedell V.M., Wang Y., Campbell J.M., Poshusta T.L., Starker C.G., Krug R.G., Tan W., Penheiter S.G., Ma A.C., Leung A.Y., et al. In vivo genome editing using a high-efficiency TALEN system. Nature 2012, 491:114-118.
4. Boyer L.A., Lee T.I., Cole M.F., Johnstone S.E., Levine S.S., Zucker J.P., Guenther M.G., Kumar R.M., Murray H.L., Jenner R.G., et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122:947-956.
5. Burel S.A., Han S.R., Lee H.S., Norris D.A., Lee B.S., Machemer T., Park S.Y., Zhou T., He G., Kim Y., et al. Preclinical evaluation of the toxicological effects of a novel constrained ethyl modified antisense compound targeting signal transducer and activator of transcription 3 in mice and cynomolgus monkeys. Nucleic Acid Ther. 2013, 23:213-227.
6. Carver B.S., Tran J., Gopalan A., Chen Z., Shaikh S., Carracedo A., Alimonti A., Nardella C., Varmeh S., Scardino P.T., et al. Aberrant ERG expression cooperates with loss of PTEN to promote cancer progression in the prostate. Nat. Genet. 2009, 41:619-624.
7. Cho E.J., Kobor M.S., Kim M., Greenblatt J., Buratowski S. Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser 2 of the RNA polymerase II C-terminal domain. Genes Dev. 2001, 15:3319-3329.
8. Davidson L., Muniz L., West S. 3' end formation of pre-mRNA and phosphorylation of Ser2 on the RNA polymerase II CTD are reciprocally coupled in human cells. Genes Dev. 2014, 28:342-356.
9. de Bono J.S., Logothetis C.J., Molina A., Fizazi K., North S., Chu L., Chi K.N., Jones R.J., Goodman O.B., Saad F., et al. Abiraterone and increased survival in metastatic prostate cancer. N. Engl. J. Med. 2011, 364:1995-2005. COU-AA-301 Investigators.
10. De Santa F., Barozzi I., Mietton F., Ghisletti S., Polletti S., Tusi B.K., Muller H., Ragoussis J., Wei C.L., Natoli G. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol. 2010, 8:e1000384.
11. Debes J.D., Tindall D.J. Mechanisms of androgen-refractory prostate cancer. N. Engl. J. Med. 2004, 351:1488-1490.
12. Dehm S.M., Tindall D.J. Ligand-independent androgen receptor activity is activation function-2-independent and resistant to antiandrogens in androgen refractory prostate cancer cells. J. Biol. Chem. 2006, 281:27882-27893.
13. Dingwall C., Ernberg I., Gait M.J., Green S.M., Heaphy S., Karn J., Lowe A.D., Singh M., Skinner M.A. HIV-1 tat protein stimulates transcription by binding to a U-rich bulge in the stem of the TAR RNA structure. EMBO J. 1990, 9:4145-4153.
14. Egloff S., Van Herreweghe E., Kiss T. Regulation of polymerase II transcription by 7SK snRNA: two distinct RNA elements direct P-TEFb and HEXIM1 binding. Mol. Cell. Biol. 2006, 26:630-642.
15. Feldman B.J., Feldman D. The development of androgen-independent prostate cancer. Nat. Rev. Cancer 2001, 1:34-45.
16. Glinsky G.V., Berezovska O., Glinskii A.B. Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. J. Clin. Invest. 2005, 115:1503-1521.
17. Grasso C.S., Wu Y.M., Robinson D.R., Cao X., Dhanasekaran S.M., Khan A.P., Quist M.J., Jing X., Lonigro R.J., Brenner J.C., et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 2012, 487:239-243.
18. Hah N., Benner C., Chong L.W., Yu R.T., Downes M., Evans R.M. Inflammation-sensitive super enhancers form domains of coordinately regulated enhancer RNAs. Proc. Natl. Acad. Sci. USA 2015, 112:E297-E302.
19. He H.H., Meyer C.A., Shin H., Bailey S.T., Wei G., Wang Q., Zhang Y., Xu K., Ni M., Lupien M., et al. Nucleosome dynamics define transcriptional enhancers. Nat. Genet. 2010, 42:343-347.
20. Hsieh C.L., Fei T., Chen Y., Li T., Gao Y., Wang X., Sun T., Sweeney C.J., Lee G.S., Chen S., et al. Enhancer RNAs participate in androgen receptor-driven looping that selectively enhances gene activation. Proc. Natl. Acad. Sci. USA 2014, 111:7319-7324.
21. Jang M.K., Mochizuki K., Zhou M., Jeong H.S., Brady J.N., Ozato K. The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Mol. Cell 2005, 19:523-534.
22. Kim T.K., Hemberg M., Gray J.M., Costa A.M., Bear D.M., Wu J., Harmin D.A., Laptewicz M., Barbara-Haley K., Kuersten S., et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 2010, 465:182-187.
23. Lam M.T., Cho H., Lesch H.P., Gosselin D., Heinz S., Tanaka-Oishi Y., Benner C., Kaikkonen M.U., Kim A.S., Kosaka M., et al. Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature 2013, 498:511-515.
24. Larochelle S., Amat R., Glover-Cutter K., Sansó M., Zhang C., Allen J.J., Shokat K.M., Bentley D.L., Fisher R.P. Cyclin-dependent kinase control of the initiation-to-elongation switch of RNA polymerase II. Nat. Struct. Mol. Biol. 2012, 19:1108-1115.
25. Li Q., Price J.P., Byers S.A., Cheng D., Peng J., Price D.H. Analysis of the large inactive P-TEFb complex indicates that it contains one 7SK molecule, a dimer of HEXIM1 or HEXIM2, and two P-TEFb molecules containing Cdk9 phosphorylated at threonine 186. J. Biol. Chem. 2005, 280:28819-28826.
26. Li W., Notani D., Ma Q., Tanasa B., Nunez E., Chen A.Y., Merkurjev D., Zhang J., Ohgi K., Song X., et al. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 2013, 498:516-520.
27. Liu W., Tanasa B., Tyurina O.V., Zhou T.Y., Gassmann R., Liu W.T., Ohgi K.A., Benner C., Garcia-Bassets I., Aggarwal A.K., et al. PHF8 mediates histone H4 lysine 20 demethylation events involved in cell cycle progression. Nature 2010, 466:508-512.
28. Liu W., Ma Q., Wong K., Li W., Ohgi K., Zhang J., Aggarwal A.K., Rosenfeld M.G. Brd4 and JMJD6-associated anti-pause enhancers in regulation of transcriptional pause release. Cell 2013, 155:1581-1595.
29. Maston G.A., Evans S.K., Green M.R. Transcriptional regulatory elements in the human genome. Annu. Rev. Genomics Hum. Genet. 2006, 7:29-59.
30. Melo C.A., Drost J., Wijchers P.J., van de Werken H., de Wit E., Oude Vrielink J.A., Elkon R., Melo S.A., Léveillé N., Kalluri R., et al. eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol. Cell 2013, 49:524-535.
31. Mousavi K., Zare H., Dell'orso S., Grontved L., Gutierrez-Cruz G., Derfoul A., Hager G.L., Sartorelli V. eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol. Cell 2013, 51:606-617.
32. Murillo H., Schmidt L.J., Karter M., Hafner K.A., Kondo Y., Ballman K.V., Vasmatzis G., Jenkins R.B., Tindall D.J. Prostate cancer cells use genetic and epigenetic mechanisms for progression to androgen independence. Genes Chromosomes Cancer 2006, 45:702-716.
33. Nguyen V.T., Kiss T., Michels A.A., Bensaude O. 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature 2001, 414:322-325.
34. Ni Z., Schwartz B.E., Werner J., Suarez J.R., Lis J.T. Coordination of transcription, RNA processing, and surveillance by P-TEFb kinase on heat shock genes. Mol. Cell 2004, 13:55-65.
35. Ong C.T., Corces V.G. Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat. Rev. Genet. 2011, 12:283-293.
36. Ørom U.A., Shiekhattar R. Long noncoding RNAs usher in a new era in the biology of enhancers. Cell 2013, 154:1190-1193.
37. Ørom U.A., Derrien T., Beringer M., Gumireddy K., Gardini A., Bussotti G., Lai F., Zytnicki M., Notredame C., Huang Q., et al. Long noncoding RNAs with enhancer-like function in human cells. Cell 2010, 143:46-58.
38. Pekowska A., Benoukraf T., Zacarias-Cabeza J., Belhocine M., Koch F., Holota H., Imbert J., Andrau J.C., Ferrier P., Spicuglia S. H3K4 tri-methylation provides an epigenetic signature of active enhancers. EMBO J. 2011, 30:4198-4210.
39. Peng J., Zhu Y., Milton J.T., Price D.H. Identification of multiple cyclin subunits of human P-TEFb. Genes Dev. 1998, 12:755-762.
40. Peterlin B.M., Price D.H. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 2006, 23:297-305.
41. Qian J., Wang Q., Dose M., Pruett N., Kieffer-Kwon K.R., Resch W., Liang G., Tang Z., Mathé E., Benner C., et al. B cell super-enhancers and regulatory clusters recruit AID tumorigenic activity. Cell 2014, 159:1524-1537.
42. Roy S., Delling U., Chen C.H., Rosen C.A., Sonenberg N. A bulge structure in HIV-1 TAR RNA is required for Tat binding and Tat-mediated trans-activation. Genes Dev. 1990, 4:1365-1373.
43. Schaukowitch K., Joo J.Y., Liu X., Watts J.K., Martinez C., Kim T.K. Enhancer RNA facilitates NELF release from immediate early genes. Mol. Cell 2014, 56:29-42.
44. Scher H.I., Beer T.M., Higano C.S., Anand A., Taplin M.E., Efstathiou E., Rathkopf D., Shelkey J., Yu E.Y., Alumkal J., et al. Antitumour activity of MDV3100 in castration-resistant prostate cancer: a phase 1-2 study. Lancet 2010, 375:1437-1446. Prostate Cancer Foundation/Department of Defense Prostate Cancer Clinical Trials Consortium.
45. Scher H.I., Fizazi K., Saad F., Taplin M.E., Sternberg C.N., Miller K., de Wit R., Mulders P., Chi K.N., Shore N.D., et al. Increased survival with enzalutamide in prostate cancer after chemotherapy. N. Engl. J. Med. 2012, 367:1187-1197. AFFIRM Investigators.
46. Tran C., Ouk S., Clegg N.J., Chen Y., Watson P.A., Arora V., Wongvipat J., Smith-Jones P.M., Yoo D., Kwon A., et al. Development of a second-generation antiandrogen for treatment of advanced prostate cancer. Science 2009, 324:787-790.
47. van der Steen T., Tindall D.J., Huang H. Posttranslational modification of the androgen receptor in prostate cancer. Int. J. Mol. Sci. 2013, 14:14833-14859.
48. Wang D., Garcia-Bassets I., Benner C., Li W., Su X., Zhou Y., Qiu J., Liu W., Kaikkonen M.U., Ohgi K.A., et al. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature 2011, 474:390-394.
49. Xie W., Ren B. Developmental biology. Enhancing pluripotency and lineage specification. Science 2013, 341:245-247.
50. Yamaguchi Y., Takagi T., Wada T., Yano K., Furuya A., Sugimoto S., Hasegawa J., Handa H. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 1999, 97:41-51.
51. Yang Z., Zhu Q., Luo K., Zhou Q. The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 2001, 414:317-322.
52. Yang Z., Yik J.H., Chen R., He N., Jang M.K., Ozato K., Zhou Q. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol. Cell 2005, 19:535-545.
53. Yu Y.P., Landsittel D., Jing L., Nelson J., Ren B., Liu L., McDonald C., Thomas R., Dhir R., Finkelstein S., et al. Gene expression alterations in prostate cancer predicting tumor aggression and preceding development of malignancy. J. Clin. Oncol. 2004, 22:2790-2799.
54. Zhou Q., Li T., Price D.H. RNA polymerase II elongation control. Annu. Rev. Biochem. 2012, 81:119-143.