SUMO ligase PIAS1 functions as a target gene selective androgen receptor coregulator on prostate cancer cell chromatin

Nucleic Acids Research

Volumn 43, Issue 2, 2015, Pages 848-861

  Toropainen, Sari ^a   Malinen, Marjo ^a   Kaikkonen, Sanna ^a   Rytinki, Miia ^a   Jääskeläinen, Tiina ^a   Sahu, Biswajyoti ^b,c   Jänne, Olli A ^b   Palvimo, Jorma J ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; CHROMATIN; FOXA1 PROTEIN, HUMAN; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; PIAS1 PROTEIN, HUMAN; PROTEIN INHIBITOR OF ACTIVATED STAT; SUMO PROTEIN; UBIQUITIN PROTEIN LIGASE;

BINDING SITE; CELL PROLIFERATION; CHROMATIN; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; METABOLISM; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

BINDING SITES; CELL LINE, TUMOR; CELL PROLIFERATION; CHROMATIN; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HUMANS; MALE; PROSTATIC NEOPLASMS; PROTEIN INHIBITORS OF ACTIVATED STAT; RECEPTORS, ANDROGEN; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84941068215     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1375     Document Type: Article

References (55)

1. Heemers,H.V. and Tindall,D.J. (2007) Androgen receptor (AR) coregulators: a diversity of functions converging on and regulating the AR transcriptional complex. Endocr. Rev., 28, 778-808.
2. Palvimo,J.J. (2012) The androgen receptor. Mol. Cell. Endocrinol., 352, 1-3.
3. Bray,F., Lortet-Tieulent,J., Ferlay,J., Forman,D. and Auvinen,A. (2010) Prostate cancer incidence and mortality trends in 37 european countries: an overview. Eur. J. Cancer, 46, 3040-3052.
4. Sharifi,N. (2013) Mechanisms of androgen receptor activation in castration-resistant prostate cancer. Endocrinology, 154, 4010-4017.
5. Cai,C. and Balk,S.P. (2011) Intratumoral androgen biosynthesis in prostate cancer pathogenesis and response to therapy. Endocr. Relat. Cancer, 18, R175-82.
6. Yuan,X., Cai,C., Chen,S., Chen,S., Yu,Z. and Balk,S.P. (2014) Androgen receptor functions in castration-resistant prostate cancer and mechanisms of resistance to new agents targeting the androgen axis. Oncogene, 33, 2815-2825.
7. Sahu,B., Laakso,M., Ovaska,K., Mirtti,T., Lundin,J., Rannikko,A., Sankila,A., Turunen,J.P., Lundin,M., Konsti,J. et al. (2011) Dual role of FoxA1 in androgen receptor binding to chromatin, androgen signalling and prostate cancer. EMBO J., 30, 3962-3976.
8. Massie,C.E., Lynch,A., Ramos-Montoya,A., Boren,J., Stark,R., Fazli,L.,Warren,A., Scott,H., Madhu,B., Sharma,N. et al. (2011) The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J., 30, 2719-2733.
9. Yu,J., Yu,J., Mani,R.S., Cao,Q., Brenner,C.J., Cao,X., Wang,X., Wu,L., Li,J., Hu,M. et al. (2010) An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer. Cell., 17, 443-454.
10. Sahu,B., Pihlajamaa,P., Dubois,V., Kerkhofs,S., Claessens,F. and Jänne,O.A. (2014) Androgen receptor uses relaxed response element stringency for selective chromatin binding and transcriptional regulation in vivo. Nucleic Acids Res., 42, 4230-4240.
11. Gao,N., Zhang,J., Rao,M.A., Case,T.C., Mirosevich,J., Wang,Y., Jin,R., Gupta,A., Rennie,P.S. and Matusik,R.J. (2003) The role of hepatocyte nuclear factor-3 alpha (forkhead box A1) and androgen receptor in transcriptional regulation of prostatic genes. Mol. Endocrinol., 17, 1484-1507.
12. Wu,D., Sunkel,B., Chen,Z., Liu,X., Ye,Z., Li,Q., Grenade,C., Ke,J., Zhang,C., Chen,H. et al. (2014) Three-tiered role of the pioneer factor GATA2 in promoting androgen-dependent gene expression in prostate cancer. Nucleic Acids Res., 42, 3607-3622.
13. Wang,Q., Li,W., Liu,X.S., Carroll,J.S., Jänne,O.A., Keeton,E.K., Chinnaiyan,A.M., Pienta,K.J. and Brown,M. (2007) A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol. Cell, 27, 380-392.
14. Mills,I.G. (2014) Maintaining and reprogramming genomic androgen receptor activity in prostate cancer. Nat. Rev. Cancer, 14, 187-198.
15. van de Wijngaart,D.J., Dubbink,H.J., van Royen,M.E., Trapman,J. and Jenster,G. (2012) Androgen receptor coregulators: recruitment via the coactivator binding groove. Mol. Cell. Endocrinol., 352, 57-69.
16. Rosenfeld,M.G., Lunyak,V.V. and Glass,C.K. (2006) Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev., 20, 1405-1428.
17. Coffey,K. and Robson,C.N. (2012) Regulation of the androgen receptor by post-translational modifications. J. Endocrinol., 215, 221-237.
18. Gross,M., Liu,B., Tan,J., French,F.S., Carey,M. and Shuai,K. (2001) Distinct effects of PIAS proteins on androgen-mediated gene activation in prostate cancer cells. Oncogene, 20, 3880-3887.
19. Nishida,T. and Yasuda,H. (2002) PIAS1 and PIASxalpha function as SUMO-E3 ligases toward androgen receptor and repress androgen receptor-dependent transcription. J. Biol. Chem., 277, 41311-41317.
20. Kotaja,N., Karvonen,U., Jänne,O.A. and Palvimo,J.J. (2002) PIAS proteins modulate transcription factors by functioning as SUMO-1 ligases. Mol. Cell. Biol., 22, 5222-5234.
21. Sharrocks,A.D. (2006) PIAS proteins and transcriptional regulation-more than just SUMO E3 ligases? Genes Dev., 20, 754-758.
22. Rytinki,M.M., Kaikkonen,S., Pehkonen,P., Jääskeläinen,T. and Palvimo,J.J. (2009) PIAS proteins: pleiotropic interactors associated with SUMO. Cell. Mol. Life Sci., 66, 3029-3041.
23. Hoefer,J., Schafer,G., Klocker,H., Erb,H.H., Mills,I.G., Hengst,L., Puhr,M. and Culig,Z. (2012) PIAS1 is increased in human prostate cancer and enhances proliferation through inhibition of p21. Am. J. Pathol., 180, 2097-2107.
24. Li,P., Yu,X., Ge,K., Melamed,J., Roeder,R.G. and Wang,Z. (2002) Heterogeneous expression and functions of androgen receptor co-factors in primary prostate cancer. Am. J. Pathol., 161, 1467-1474.
25. Korenchuk,S., Lehr,J.E., MClean,L., Lee,Y.G., Whitney,S., Vessella,R., Lin,D.L. and Pienta,K.J. (2001) VCaP, a cell-based model system of human prostate cancer. In Vivo, 15, 163-168.
26. Knuuttila,M., Yatkin,E., Kallio,J., Savolainen,S., Laajala,T.D., Aittokallio,T., Oksala,R., Häkkinen,M., Keski-Rahkonen,P., Auriola,S. et al. (2014) Castration induces up-regulation of intratumoral androgen biosynthesis and androgen receptor expression in an orthotopic VCaP human prostate cancer xenograft model. Am. J. Pathol., 184, 2163-2173.
27. Makkonen,H., Kauhanen,M., Paakinaho,V., Jääskeläinen,T. and Palvimo,J.J. (2009) Long-range activation of FKBP51 transcription by the androgen receptor via distal intronic enhancers. Nucleic Acids Res., 37, 4135-4148.
28. Karvonen,U., Kallio,P.J., Jänne,O.A. and Palvimo,J.J. (1997) Interaction of androgen receptors with androgen response element in intact cells. roles of amino-and carboxyl-terminal regions and the ligand. J. Biol. Chem., 272, 15973-15979.
29. Makkonen,H., Jääskeläinen,T., Rytinki,M.M. and Palvimo,J.J. (2011) Analysis of androgen receptor activity by reporter gene assays. Methods Mol. Biol., 776, 71-80.
30. Paakinaho,V., Kaikkonen,S., Makkonen,H., Benes,V. and Palvimo,J.J. (2014) SUMOylation regulates the chromatin occupancy and anti-proliferative gene programs of glucocorticoid receptor. Nucleic Acids Res., 42, 1575-1592.
31. Sutinen,P., Malinen,M., Heikkinen,S. and Palvimo,J.J. (2014) SUMOylation modulates the transcriptional activity of androgen receptor in a target gene and pathway selective manner. Nucleic Acids Res., 42, 8310-8319.
32. Rytinki,M., Kaikkonen,S., Sutinen,P., Paakinaho,V., Rahkama,V. and Palvimo,J.J. (2012) Dynamic SUMOylation is linked to the activity cycles of androgen receptor in the cell nucleus. Mol. Cell. Biol., 32, 4195-4205.
33. Li,H., Handsaker,B.,Wysoker,A., Fennell,T., Ruan,J., Homer,N., Marth,G., Abecasis,G., Durbin,R. and 1000 Genome Project Data Processing Subgroup. (2009) The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078-2079.
34. Heinz,S., Benner,C., Spann,N., Bertolino,E., Lin,Y.C., Laslo,P., Cheng,J.X., Murre,C., Singh,H. and Glass,C.K. (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell, 38, 576-589.
35. Landt,S.G., Marinov,G.K., Kundaje,A., Kheradpour,P., Pauli,F., Batzoglou,S., Bernstein,B.E., Bickel,P., Brown,J.B., Cayting,P. et al. (2012) ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res., 22, 1813-1831.
36. Furey,T.S. (2012) ChIP-seq and beyond: new and improved methodologies to detect and characterize protein-DNA interactions. Nat. Rev. Genet., 13, 840-852.
37. Quinlan,A.R. and Hall,I.M. (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26, 841-842.
38. Ovaska,K., Laakso,M., Haapa-Paananen,S., Louhimo,R., Chen,P., Aittomäki,V., Valo,E., Nunez-Fontarnau,J., Rantanen,V., Karinen,S. et al. (2010) Large-scale data integration framework provides a comprehensive view on glioblastoma multiforme. Genome Med., 2, 65.
39. Edgar,R., Domrachev,M. and Lash,A.E. (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res., 30, 207-210.
40. Benod,C., Vinogradova,M.V., Jouravel,N., Kim,G.E., Fletterick,R.J. and Sablin,E.P. (2011) Nuclear receptor liver receptor homologue 1 (LRH-1) regulates pancreatic cancer cell growth and proliferation. Proc. Natl. Acad. Sci. U.S.A., 108, 16927-16931.
41. Kataoka,K., Noda,M. and Nishizawa,M. (1994) Maf nuclear oncoprotein recognizes sequences related to an AP-1 site and forms heterodimers with both fos and jun. Mol. Cell. Biol., 14, 700-712.
42. Walker,S.R., Liu,S., Xiang,M., Nicolais,M., Hatzi,K., Giannopoulou,E., Elemento,O., Cerchietti,L., Melnick,A. and Frank,D.A. (2014) The transcriptional modulator BCL6 as a molecular target for breast cancer therapy. Oncogene., doi:10.1038/onc.2014.61.
43. Mehta,H.H., Gao,Q., Galet,C., Paharkova,V., Wan,J., Said,J., Sohn,J.J., Lawson,G., Cohen,P., Cobb,L.J. et al. (2011) IGFBP-3 is a metastasis suppression gene in prostate cancer. Cancer Res., 71, 5154-5163.
44. Zou,J.X., Guo,L., Revenko,A.S., Tepper,C.G., Gemo,A.T., Kung,H.J. and Chen,H.W. (2009) Androgen-induced coactivator ANCCA mediates specific androgen receptor signaling in prostate cancer. Cancer Res., 69, 3339-3346.
45. Gery,S., Sawyers,C.L., Agus,D.B., Said,J.W. and Koeffler,H.P. (2002) TMEFF2 is an androgen-regulated gene exhibiting antiproliferative effects in prostate cancer cells. Oncogene, 21, 4739-4746.
46. Selimovic,D., Sprenger,A., Hannig,M., Haikel,Y. and Hassan,M. (2012) Apoptosis related protein-1 triggers melanoma cell death via interaction with the juxtamembrane region of p75 neurotrophin receptor. J. Cell. Mol. Med., 16, 349-361.
47. Wang,D., Lu,J. and Tindall,D.J. (2013) Androgens regulate TRAIL-induced cell death in prostate cancer cells via multiple mechanisms. Cancer Lett., 335, 136-144.
48. Weiskirchen,R., Moser,M., Weiskirchen,S., Erdel,M., Dahmen,S., Buettner,R. and Gressner,A.M. (2001) LIM-domain protein cysteine-and glycine-rich protein 2 (CRP2) is a novel marker of hepatic stellate cells and binding partner of the protein inhibitor of activated STAT1. Biochem. J., 359, 485-496.
49. Sung,Y.Y. and Cheung,E. (2013) Androgen receptor co-regulatory networks in castration-resistant prostate cancer. Endocr. Relat. Cancer, 21, R1-R11.
50. Linja,M.J., Porkka,K.P., Kang,Z., Savinainen,K.J., Jänne,O.A., Tammela,T.L., Vessella,R.L., Palvimo,J.J. and Visakorpi,T. (2004) Expression of androgen receptor coregulators in prostate cancer. Clin. Cancer Res., 10, 1032-1040.
51. Heemers,H.V., Regan,K.M., Schmidt,L.J., Anderson,S.K., Ballman,K.V. and Tindall,D.J. (2009) Androgen modulation of coregulator expression in prostate cancer cells. Mol. Endocrinol., 23, 572-583.
52. Ciro,M., Prosperini,E., Quarto,M., Grazini,U., Walfridsson,J., McBlane,F., Nucifero,P., Pacchiana,G., Capra,M., Christensen,J. et al. (2009) ATAD2 is a novel cofactor for MYC, overexpressed and amplified in aggressive tumors. Cancer Res., 69, 8491-8498.
53. Lanz,R.B., Bulynko,Y., Malovannaya,A., Labhart,P., Wang,L., Li,W., Qin,J., Harper,M. and O'Malley,B.W. (2010) Global characterization of transcriptional impact of the SRC-3 coregulator. Mol. Endocrinol., 24, 859-872.
54. Norris,J.D., Chang,C.Y., Wittmann,B.M., Kunder,R.S., Cui,H., Fan,D., Joseph,J.D. and McDonnell,D.P. (2009) The homeodomain protein HOXB13 regulates the cellular response to androgens. Mol. Cell, 36, 405-416.
55. Sutinen,P., Rahkama,V., Rytinki,M. and Palvimo,J.J. (2014) Nuclear mobility and activity of FOXA1 with androgen receptor are regulated by SUMOylation. Mol. Endocrinol., 28, 1719-1728.