Androgen regulation of the TMPRSS2 gene and the effect of a SNP in an androgen response element

Molecular Endocrinology

Volumn 27, Issue 12, 2013, Pages 2028-2040

  Clinckemalie, Liesbeth ^a   Spans, Lien ^a   Dubois, Vanessa ^a   Laurent, Michaël ^a   Helsen, Christine ^a   Joniau, Steven ^b   Claessens, Frank ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; DEOXYRIBONUCLEASE I; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR GATA 2;

ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CONTROLLED STUDY; DNA FOOTPRINTING; DNA RESPONSIVE ELEMENT; ENHANCER REGION; GENE; GENE CONTROL; GENE FUSION; HORMONAL REGULATION; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DNA BINDING; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM; TMPRSS2 GENE;

ANDROGENS; ANIMALS; BASE PAIRING; BASE SEQUENCE; BINDING SITES; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; CHROMATIN; COS CELLS; ENHANCER ELEMENTS, GENETIC; GATA2 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; HUMANS; MOLECULAR SEQUENCE DATA; ORGANIC CATION TRANSPORTER 1; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN BINDING; RESPONSE ELEMENTS; SERINE ENDOPEPTIDASES;

EID: 84888343067     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2013-1098     Document Type: Article

References (87)

1. Bugge TH, Antalis TM, Wu Q. Type II transmembrane serine proteases. J Biol Chem. 2009;284:23177-23181.
2. Hooper JD, Scarman AL, Clarke BE, Normyle JF, Antalis TM. Localization of the mosaic transmembrane serine protease corin to heart myocytes. Eur J Biochem. 2000;267:6931-6937.
3. Paoloni-Giacobino A, Chen H, Peitsch MC, Rossier C, Antonarakis SE. Cloning of the TMPRSS2 gene, which encodes a novel serine protease with transmembrane, LDLRA, and SRCR domains and maps to 21q22.3. Genomics. 1997;44:309-320.
4. Afar DE, Vivanco I, Hubert RS, et al. Catalytic cleavage of the androgen-regulated TMPRSS2 protease results in its secretion by prostate and prostate cancer epithelia. Cancer Res. 2001;61:1686-1692.
5. Lin B, Ferguson C, White JT, et al. Prostate-localized and androgenregulated expression of the membrane-bound serine protease TMPRSS2. Cancer Res. 1999;59:4180-4184.
6. Lucas JM, True L, Hawley S, et al. The androgen-regulated type II serine protease TMPRSS2 is differentially expressed and mislocalized in prostate adenocarcinoma. J Pathol. 2008;215:118-125.
7. Jacquinet E, Rao NV, Rao GV, Zhengming W, Albertine KH, Hoidal JR. Cloning and characterization of the cDNA and gene for human epitheliasin. Eur J Biochem. 2001;268:2687-2699.
8. Mosquera JM, Mehra R, Regan MM, et al. Prevalence of TMPRSS2-ERG fusion prostate cancer among men undergoing prostate biopsy in the United States. Clin Cancer Res. 2009;15:4706-4711.
9. Esgueva R, Perner S, LaFargue C, et al. Prevalence of TMPRSS2-ERG and SLC45A3-ERG gene fusions in a large prostatectomy cohort. Mod Pathol. 2010;23:539-546.
10. Clark J, Merson S, Jhavar S, et al. Diversity of TMPRSS2-ERG fusion transcripts in the human prostate. Oncogene. 2007;26: 2667-2673.
11. Tomlins SA, Rhodes DR, Perner S, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science. 2005;310:644-648.
12. Liu H, Shi J, Wilkerson M, Yang XJ, Lin F. Immunohistochemical evaluation of ERG expression in various benign and malignant tissues. Ann Clin Lab Sci. 2013;43:3-9.
13. Petrovics G, Liu A, Shaheduzzaman S, et al. Frequent overexpression of ETS-related gene-1 (ERG1) in prostate cancer transcriptome. Oncogene. 2005;24:3847-3852.
14. Rubin MA, Maher CA, Chinnaiyan AM. Common gene rearrangements in prostate cancer. J Clin Oncol. 2011;29:3659-3668.
15. Kumar-Sinha C, Tomlins SA, Chinnaiyan AM. Recurrent gene fusions in prostate cancer. Nat Rev Cancer. 2008;8:497-511.
16. Oikawa T, Yamada T. Molecular biology of the Ets family of transcription factors. Gene. 2003;303:11-34.
17. Seth A, Watson DK. ETS transcription factors and their emerging roles in human cancer. Eur J Cancer. 2005;41:2462-2478.
18. St John J, Powell K, Conley-Lacomb MK, Chinni SR. TMPRSS2-ERG fusion gene expression in prostate tumor cells and its clinical and biological significance in prostate cancer progression. J Cancer Sci Ther. 2012;4:94-101.
19. FitzGerald LM, Agalliu I, Johnson K, et al. Association of TMPRSS2-ERG gene fusion with clinical characteristics and outcomes: results from a population-based study of prostate cancer. BMC Cancer. 2008;8:230.
20. Gopalan A, Leversha MA, Satagopan JM, et al. TMPRSS2-ERG gene fusion is not associated with outcome in patients treated by prostatectomy. Cancer Res. 2009;69:1400-1406.
21. Attard G, Clark J, Ambroisine L, et al. Duplication of the fusion of TMPRSS2 to ERG sequences identifies fatal human prostate cancer. Oncogene. 2008;27:253-263.
22. Yoshimoto M, Joshua AM, Cunha IW, et al. Absence of TMPRSS2: ERG fusions and PTEN losses in prostate cancer is associated with a favorable outcome. Mod Pathol. 2008;21:1451-1460.
23. Mehra R, Tomlins SA, Yu J, et al. Characterization of TMPRSS2-ETS gene aberrations in androgen-independent metastatic prostate cancer. Cancer Res. 2008;68:3584-3590.
24. Perner S, Svensson MA, Hossain RR, et al. ERG rearrangement metastasis patterns in locally advanced prostate cancer. Urology. 2010;75:762-767.
25. Hu Y, Dobi A, Sreenath T, et al. Delineation of TMPRSS2-ERG splice variants in prostate cancer. Clin Cancer Res. 2008;14:4719-4725.
26. Wang J, Cai Y, Ren C, Ittmann M. Expression of variant TMPRSS2/ ERG fusion messenger RNAs is associated with aggressive prostate cancer. Cancer Res. 2006;66:8347-8351.
27. Wang J, Cai Y, Yu W, Ren C, Spencer DM, Ittmann M. Pleiotropic biological activities of alternatively spliced TMPRSS2/ERG fusion gene transcripts. Cancer Res. 2008;68:8516-8524.
28. Zammarchi F, Boutsalis G, Cartegni L. 5' UTR control of native ERG and of Tmprss2:ERG variants activity in prostate cancer. PLoS One. 2013;8:e49721.
29. Weischenfeldt J, Simon R, Feuerbach L, et al. Integrative genomic analyses reveal an androgen-driven somatic alteration landscape in early-onset prostate cancer. Cancer Cell. 2013;23:159-170.
30. Schaefer G, Mosquera JM, Ramoner R, et al. Distinct ERG rearrangement prevalence in prostate cancer: higher frequency in young age and in low PSA prostate cancer. Prostate Cancer Prostatic Dis. 2013;16(2):132-138.
31. Baca SC, Prandi D, Lawrence MS, et al. Punctuated evolution of prostate cancer genomes. Cell. 2013;153:666-677.
32. Laxman B, Morris DS, Yu J, Siddiqui J, Cao J, Mehra R, Lonigro RJ, Tsodikov A, Wei JT, Tomlins SA, Chinnaiyan AM. A firstgeneration multiplex biomarker analysis of urine for the early detection of prostate cancer. Cancer Res. 2008;68:645-649.
33. Tomlins SA, Aubin SM, Siddiqui J, et al. Urine TMPRSS2:ERG fusion transcript stratifies prostate cancer risk in men with elevated serum PSA. Sci Transl Med. 2011;3:94ra72.
34. Leyten GH, Hessels D, Jannink SA, et al. Prospective multicentre evaluation of PCA3 and TMPRSS2-ERG gene fusions as diagnostic and prognostic urinary biomarkers for prostate cancer [published online November 15, 2012]. Eur Urol. 2012 doi: 10.1016/j.eururo.2012.11.014.
35. Nguyen PN, Violette P, Chan S, et al. A panel of TMPRSS2:ERG fusion transcript markers for urine-based prostate cancer detection with high specificity and sensitivity. Eur Urol. 2011;59:407-414.
36. Hessels D, Smit FP, Verhaegh GW, Witjes JA, Cornel EB, Schalken JA. Detection of TMPRSS2-ERG fusion transcripts and prostate cancer antigen 3 in urinary sediments may improve diagnosis of prostate cancer. Clin Cancer Res. 2007;13:5103-5108.
37. Wang Q, Li W, Liu XS, et al. A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol Cell. 2007;27:380-392.
38. Sahu B, Laakso M, Ovaska K, et al. Dual role of FoxA1 in androgen receptor binding to chromatin, androgen signalling and prostate cancer. EMBO J. 2011;30:3962-3976.
39. Yu J, Mani RS, Cao Q, et al. An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell. 2010;17:443-454.
40. Massie CE, Lynch A, Ramos-Montoya A, et al. The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J. 2011;30:2719-2733.
41. Sharma NL, Massie CE, Ramos-Montoya A, et al. The androgen receptor induces a distinct transcriptional program in castrationresistant prostate cancer in man. Cancer Cell. 2013;23:35-47.
42. Andreu-Vieyra C, Lai J, Berman BP, et al. Dynamic nucleosomedepleted regions at androgen receptor enhancers in the absence of ligand in prostate cancer cells. Mol Cell Biol. 2011;31:4648-4662.
43. Green S, Issemann I, Sheer E. A versatile in vivo and in vitro eukaryotic expression vector for protein engineering. Nucleic Acids Res. 1988;16:369.
44. Verrijdt G, Schauwaers K, Haelens A, Rombauts W, Claessens F. Functional interplay between two response elements with distinct binding characteristics dictates androgen specificity of the mouse sex-limited protein enhancer. J Biol Chem. 2002;277:35191-35201.
45. Moehren U, Denayer S, Podvinec M, Verrijdt G, Claessens F. Identification of androgen-selective androgen-response elements in the human aquaporin-5 and Rad9 genes. Biochem J. 2008;411:679-686.
46. http://www.chem.agilent.com/Library/usermanuals/Public/ 200518.pdf. Accessed April 1, 2013.
47. Haelens A, Verrijdt G, Callewaert L, Peeters B, Rombauts W, Claessens F. Androgen-receptor-specific DNA binding to an element in the first exon of the human secretory component gene. Biochem J. 2001;353:611-620.
48. Thomas-Chollier M, Sand O, Turatsinze JV, et al. RSAT: regulatory sequence analysis tools. Nucleic Acids Res. 2008;36:W119-W127.
49. http://rsat.ulb.ac.be/rsat/. Accessed April 1, 2013.
50. Denayer S, Helsen C, Thorrez L, Haelens A, Claessens F. The rules of DNA recognition by the androgen receptor. Mol Endocrinol. 2010;24:898-913.
51. Schoenmakers E, Alen P, Verrijdt G, et al. DifferentialDNAbinding by the androgen and glucocorticoid receptors involves the second Zn-finger and a C-terminal extension of the DNA-binding domains. Biochem J. 1999;341(Pt. 3):515-521.
52. Schauwaers K, De Gendt K, Saunders PT, et al. Loss of androgen receptor binding to selective androgen response elements causes a reproductive phenotype in a knockin mouse model. Proc Natl Acad Sci USA. 2007;104:4961-4966.
53. Sambrook J, Russell DW. Isolation of DNA fragments from polyacrylamide gels by the crush and soak method. CSH Protoc. 2006; 2006(1).
54. Fu Q, Manolagas SC, O'Brien CA. Parathyroid hormone controls receptor activator of NF-κB ligand gene expression via a distant transcriptional enhancer. Mol Cell Biol. 2006;26:6453-6468.
55. Swaminathan S, Sharan SK. Bacterial artificial chromosome engineering. Methods Mol Biol. 2004;256:89-106.
56. Zella LA, Meyer MB, Nerenz RD, Lee SM, Martowicz ML, Pike JW. Multifunctional enhancers regulate mouse and human vitamin D receptor gene transcription. Mol Endocrinol. 2010;24:128-147.
57. Warming S, Costantino N, Court DL, Jenkins NA, Copeland NG. Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res. 2005;33:e36.
58. Portales-Casamar E, Thongjuea S, Kwon AT, et al. JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res. 2010;38:D105-D110.
59. Matys V, Kel-Margoulis OV, Fricke E, et al. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res. 2006;34:D108-D110.
60. Claessens F, Verrijdt G, Schoenmakers E, et al. SelectiveDNAbinding by the androgen receptor as a mechanism for hormone-specific gene regulation. J Steroid Biochem Mol Biol. 2001;76:23-30.
61. Zaret KS, Carroll JS. Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 2011;25:2227-2241.
62. Kim S, Broströmer E, Xing D, et al. Probing allostery through DNA. Science. 2013;339:816-819.
63. Masuda K, Werner T, Maheshwari S, et al. Androgen receptor binding sites identified by a GREF_GATA model. J Mol Biol. 2005; 353:763-771.
64. Perez-Stable CM, Pozas A, Roos BA. A role for GATA transcription factors in the androgen regulation of the prostate-specific antigen gene enhancer. Mol Cell Endocrinol. 2000;167:43-53.
65. Bhardwaj A, Song HW, Beildeck M, et al. DNA demethylationdependent AR recruitment and GATA factors drive Rhox5 homeobox gene transcription in the epididymis. Mol Endocrinol. 2012; 26:538-549.
66. Carey MF, Peterson CL, Smale ST. Experimental strategies for the identification of DNA-binding proteins. Cold Spring Harb Protoc. 2012;2012:18-33.
67. Celis L, Claessens F, Peeters B, Heyns W, Verhoeven G, Rombauts W. Proteins interacting with an androgen-responsive unit in the C3(1) gene intron. Mol Cell Endocrinol. 1993;94:165-172.
68. Claessens F, Celis L, De Vos P, et al. Intronic androgen response elements of prostatic binding protein genes. Biochem Biophys Res Commun. 1993;191:688-694.
69. De Vos P, Claessens F, Winderickx J, et al. Interaction of androgen response elements with the DNA-binding domain of the rat androgen receptor expressed in Escherichia coli. J Biol Chem. 1991;266: 3439-3443.
70. Lareyre JJ, Reid K, Nelson C, et al. Characterization of an androgen-specific response region within the 5' flanking region of the murine epididymal retinoic acid binding protein gene. Biol Reprod. 2000;63:1881-1892.
71. Maffey AH, Ishibashi T, He C, et al. Probasin promoter assembles into a strongly positioned nucleosome that permits androgen receptor binding. Mol Cell Endocrinol. 2007;268:10-19.
72. Rundlett SE, Miesfeld RL. Quantitative differences in androgen and glucocorticoid receptor DNA binding properties contribute to receptor-selective transcriptional regulation. Mol Cell Endocrinol. 1995;109:1-10.
73. Burgos-Trinidad M, Youngblood GL, Maroto MR, Scheller A, Robins DM, Payne AH. Repression of cAMP-induced expression of the mouse P450 17 α-hydroxylase/C17-20 lyase gene (Cyp17) by androgens. Mol Endocrinol. 1997;11:87-96.
74. Kallio PJ, Palvimo JJ, Mehto M, Jänne OA. Analysis of androgen receptor-DNA interactions with receptor proteins produced in insect cells. J Biol Chem. 1994;269:11514-11522.
75. Scheller A, Hughes E, Golden KL, Robins DM. Multiple receptor domains interact to permit, or restrict, androgen-specific gene activation. J Biol Chem. 1998;273:24216-24222.
76. Scheller A, Scheinman RI, Thompson E, Scarlett CO, Robins DM. Contextual dependence of steroid receptor function on an androgenresponsive enhancer. Mol Cell Endocrinol. 1996;121:75-86.
77. Kasowski M, Grubert F, Heffelfinger C, et al. Variation in transcription factor binding among humans. Science. 2010;328:232-235.
78. Rockman MV, Wray GA. Abundant raw material for cis-regulatory evolution in humans. Mol Biol Evol. 2002;19:1991-2004.
79. Eeles RA, Kote-Jarai Z, Al Olama AA, et al. Identification of seven new prostate cancer susceptibility loci through a genome-wide association study. Nat Genet. 2009;41:1116-1121.
80. Lichtenstein P, Holm NV, Verkasalo PK, et al. Environmental and heritable factors in the causation of cancer-analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med. 2000; 343:78-85.
81. Schaid DJ. The complex genetic epidemiology of prostate cancer. Hum Mol Genet. 2004;13(Spec. No.):R103-R121.
82. Haffner MC, Aryee MJ, Toubaji A, et al. Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements. Nat Genet. 2010;42:668-675.
83. Lin C, Yang L, Tanasa B, et al. Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer. Cell. 2009;139:1069-1083.
84. Mani RS, Tomlins SA, Callahan K, et al. Induced chromosomal proximity and gene fusions in prostate cancer. Science. 2009;326: 1230.
85. http://genome.ucsc.edu/cgi-bin/hgGateway. Accessed April 1, 2013.
86. Maxam AM, Gilbert W. Sequencing end-labeled DNA with basespecific chemical cleavages. Methods Enzymol. 1980;65:499-560.
87. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004;14:1188-1190.