Mechanisms of the androgen receptor splicing in prostate cancer cells

Oncogene

Volumn 33, Issue 24, 2014, Pages 3140-3150

  Liu, L L ^a   Xie, N ^a   Sun, S ^b   Plymate, S ^b   Mostaghel, E ^c   Dong, X ^a,d  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

alternative splicing; androgen deprivation therapy; prostate cancer; RNA splice variant

Indexed keywords

ANDROGEN RECEPTOR; ANDROGEN RECEPTOR SPLICE VARIANT 7; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; IMMUNOGLOBULIN G; MESSENGER RNA; MESSENGER RNA PRECURSOR; PROSTATE SPECIFIC ANTIGEN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANDROGEN DEPRIVATION THERAPY; ARTICLE; BINDING SITE; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA FLANKING REGION; ENHANCER REGION; EXON; GENE DOSAGE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN RNA BINDING; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA SEQUENCE; RNA SPLICING; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

ALTERNATIVE SPLICING; ANDROGENS; ANIMALS; APOPTOSIS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOPRECIPITATION; MALE; MICE; MICE, SCID; PROSTATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ANDROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84902471998     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.284     Document Type: Article

References (48)

1. Sims 3rd RJ, Millhouse S, Chen CF, Lewis BA, Erdjument-Bromage H, Tempst P et al. Recognition of trimethylated histone H3 lysin. 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol Cell 2007; 28: 665-676.
2. Chen Y, Clegg NJ, Scher HI. Anti-androgens and androgen-depleting therapies in prostate cancer: new agents for an established target. Lancet Oncol 2009; 10: 981-991.
3. Scher HI, Sawyers CL. Biology of progressive, castration-resistant prostate cancer: directed therapies targeting the androgen-receptor signaling axis. J Clin Oncol 2005; 23: 8253-8261.
4. Chen CD, Welsbie DS, Tran C, Baek SH, Chen R, Vessella R et al. Molecular determinants of resistance to antiandrogen therapy. Nat Med 2004; 10: 33-39.
5. Taplin ME, Balk SP. Androgen receptor: a key molecule in the progression of prostate cancer to hormone independence. J Cell Biochem 2004; 91: 483-490.
6. Locke JA, Guns ES, Lubik AA, Adomat HH, Hendy SC, Wood CA et al. Androgen levels increase by intratumoral de novo steroidogenesis during progression of castration-resistant prostate cancer. Cancer Res 2008; 68: 6407-6415.
7. Mostaghel EA, Page ST, Lin DW, Fazli L, Coleman IM, True LD et al. Intraprostatic androgens and androgen-regulated gene expression persist after testosterone suppression: therapeutic implications for castration-resistant prostate cancer. Cancer Res 2007; 67: 5033-5041.
8. Heemers HV, Schmidt LJ, Kidd E, Raclaw KA, Regan KM, Tindall DJ. Differential regulation of steroid nuclear receptor coregulator expression between normal and neoplastic prostate epithelial cells. Prostate 2010; 70: 959-970.
9. Sadar MD. Androgen-independent induction of prostate-specific antigen gene expression via cross-talk between the androgen receptor and protein kinase A signal transduction pathways. J Biol Chem 1999; 274: 7777-7783.
10. Dehm SM, Schmidt LJ, Heemers HV, Vessella RL, Tindall DJ. Splicing of a novel androgen receptor exon generates a constitutively active androgen receptor that mediates prostate cancer therapy resistance. Cancer Res 2008; 68: 5469-5477.
11. Hu R, Dunn TA, Wei S, Isharwal S, Veltri RW, Humphreys E et al. Ligand-independent androgen receptor variants derived from splicing of cryptic exons signify hormone-refractory prostate cancer. Cancer Res 2009; 69: 16-22.
12. Hu R, Isaacs WB, Luo J. A snapshot of the expression signature of androgen receptor splicing variants and their distinctive transcriptional activities. Prostate 2011; 71: 1656-1667.
13. Guo Z, Yang X, Sun F, Jiang R, Linn DE, Chen H et al. A novel androgen receptor splice variant is up-regulated during prostate cancer progression and promotes androgen depletion-resistant growth. Cancer Res 2009; 69: 2305-2313.
14. Yang X, Guo Z, Sun F, Li W, Alfano A, Shimelis H et al. Novel membrane-associated androgen receptor splice variant potentiates proliferative and survival responses in prostate cancer cells. J Biol Chem 2011; 286: 36152-36160.
15. Sun S, Sprenger CC, Vessella RL, Haugk K, Soriano K, Mostaghel EA et al. Castration resistance in human prostate cancer is conferred by a frequently occurring androgen receptor splice variant. J Clin Invest 2010; 120: 2715-2730.
16. Li Y, Chan SC, Brand LJ, Hwang TH, Silverstein KA, Dehm SM. Androgen receptor splice variants mediate enzalutamide resistance in castration-resistant prostate cancer cell lines. Cancer Res 2013; 73: 483-489.
17. Cai C, He HH, Chen S, Coleman I, Wang H, Fang Z et al. Androgen receptor gene expression in prostate cancer is directly suppressed by the androgen receptor through recruitment of lysine-specific demethylase 1. Cancer Cell 2011; 20: 457-471.
18. Hu R, Lu C, Mostaghel EA, Yegnasubramanian S, Gurel M, Tannahill C et al. Distinct transcriptional programs mediated by the ligand-dependent full-length androgen receptor and its splice variants in castration-resistant prostate cancer. Cancer Res 2012; 72: 3457-3462.
19. Zhang X, Morrissey C, Sun S, Ketchandji M, Nelson PS, True LD et al. Androgen receptor variants occur frequently in castration resistant prostate cancer metastases. PLoS ONE 2011; 6: e27970.
20. Hornberg E, Ylitalo EB, Crnalic S, Antti H, Stattin P, Widmark A et al. Expression of androgen receptor splice variants in prostate cancer bone metastases is associated with castration-resistance and short survival. PLoS ONE 2011; 6: e19059.
21. Srebrow A, Kornblihtt AR. The connection between splicing and cancer. J Cell Sci 2006; 119(Pt 13): 2635-2641.
22. Goldstrohm AC, Greenleaf AL, Garcia-Blanco MA. Co-transcriptional splicing of pre-messenger RNAs: considerations for the mechanism of alternative splicing. Gene 2001; 277: 31-47.
23. Chew SL, Liu HX, Mayeda A, Krainer AR. Evidence for the function of an exonic splicing enhancer after the first catalytic step of pre-mRNA splicing. Proc Natl Acad Sci USA. 1999; 96: 10655-10660.
24. Chen M, Manley JL. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat Rev Mol Cell Biol 2009; 10: 741-754.
25. Kornblihtt AR. Coupling transcription and alternative splicing. Adv Exp Med Biol 2007; 623: 175-189.
26. Auboeuf D, Honig A, Berget SM, O'Malley BW. Coordinate regulation of transcription and splicing by steroid receptor coregulators. Science 2002; 298: 416-419.
27. Nogues G, Kadener S, Cramer P, Bentley D, Kornblihtt AR. Transcriptional activators differ in their abilities to control alternative splicing. J Biol Chem 2002; 277: 43110-43114.
28. Batsche E, Yaniv M, Muchardt C. The human SWI/SNF subunit Brm is a regulator of alternative splicing. Nat Struct Mol Biol 2006; 13: 22-29.
29. McCracken S, Fong N, Yankulov K, Ballantyne S, Pan G, Greenblatt J et al. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 1997; 385: 357-361.
30. Maniatis T, Reed R. An extensive network of coupling among gene expression machines. Nature 2002; 416: 499-506.
31. Moore MJ, Proudfoot NJ. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 2009; 136: 688-700.
32. Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T. Epigenetics in alternative premRNA splicing. Cell 2011; 144: 16-26.
33. Kornblihtt AR. Promoter usage and alternative splicing. Curr Opin Cell Biol 2005; 17: 262-268.
34. Kadener S, Cramer P, Nogues G, Cazalla D, de la Mata M, Fededa JP et al. Antagonistic effects of T-Ag and VP16 reveal a role for RNA pol II elongation on alternative splicing. EMBO J. 2001; 20: 5759-5768.
35. Li Y, Hwang TH, Oseth LA, Hauge A, Vessella RL, Schmechel SC et al. AR intragenic deletions linked to androgen receptor splice variant expression and activity in models of prostate cancer progression. Oncogene 2012; 31: 4759-4767.
36. Watson PA, Chen YF, Balbas MD, Wongvipat J, Socci ND, Viale A et al. Constitutively active androgen receptor splice variants expressed in castration-resistant prostate cancer require full-length androgen receptor. Proc Natl Acad Sci USA. 2010; 107: 16759-16765.
37. Welsbie DS, Xu J, Chen Y, Borsu L, Scher HI, Rosen N et al. Histone deacetylases are required for androgen receptor function in hormone-sensitive and castrateresistant prostate cancer. Cancer Res 2009; 69: 958-966.
38. Rokhlin OW, Glover RB, Guseva NV, Taghiyev AF, Kohlgraf KG, Cohen MB. Mechanisms of cell death induced by histone deacetylase inhibitors in androgen receptor-positive prostate cancer cells. Mol Cancer Res 2006; 4: 113-123.
39. Caceres JF, Kornblihtt AR. Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet 2002; 18: 186-193.
40. Stamm S, Riethoven JJ, Le Texier V, Gopalakrishnan C, Kumanduri V, Tang Y et al. ASD: a bioinformatics resource on alternative splicing. Nucleic Acids Rese 2006; 34(Database issue): D46-D55.
41. Cartegni L, Wang J, Zhu Z, Zhang MQ, Krainer AR. ESEfinder: A web resource to identify exonic splicing enhancers. Nucleic Acids Res 2003; 31: 3568-3571.
42. Li Y, Alsagabi M, Fan D, Bova GS, Tewfik AH, Dehm SM. Intragenic rearrangement and altered RNA splicing of the androgen receptor in a cell-based model of prostate cancer progression. Cancer Res 2011; 71: 2108-2117.
43. Xie N, Liu L, Li Y, Yu C, Lam S, Shynlova O et al. Expression and function of myometrial PSF suggest a role in progesterone withdrawal and the initiation of labor. Mol Endocrinol 2012; 26: 1370-1379.
44. Luco RF, Pan Q, Tominaga K, Blencowe BJ, Pereira-Smith OM, Misteli T. Regulation of alternative splicing by histone modifications. Science 2010; 327: 996-1000.
45. Dong X, Sweet J, Challis JR, Brown T, Lye SJ. Transcriptional activity of androgen receptor is modulated by two RNA splicing factors, PSF and p54nrb. Mol Cell Biol 2007; 27: 4863-4875.
46. Olshavsky NA, Comstock CE, Schiewer MJ, Augello MA, Hyslop T, Sette C et al. Identification of ASF/SF2 as a critical, allele-specific effector of the cyclin D1b oncogene. Cancer Res 2010; 70: 3975-3984.
47. Paronetto MP, Achsel T, Massiello A, Chalfant CE, Sette C. The RNA-binding protein Sam68 modulates the alternative splicing of Bcl-x. J Cell Biol 2007; 176: 929-939.
48. Cheng H, Snoek R, Ghaidi F, Cox ME, Rennie PS.. Short hairpin RNA knockdown of the androgen receptor attenuates ligand-independent activation and delays tumor progression. Cancer Res 2006; 66: 10613-10620.