Probasin promoter assembles into a strongly positioned nucleosome that permits androgen receptor binding

Molecular and Cellular Endocrinology

Volumn 268, Issue 1-2, 2007, Pages 10-19

  Maffey, Allison H ^a   Ishibashi, Toyotaka ^a   He, Cheng ^a,b   Wang, Xiaoying ^a,c   White, Adrienne R ^a   Hendy, Stephen C ^d   Nelson, Colleen C ^d   Rennie, Paul S ^d   Ausió, Juan ^a,d  

^a UNIVERSITY OF VICTORIA   (Canada)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^d VANCOUVER GENERAL HOSPITAL   (Canada)

Author keywords

Androgen receptor; Histone acetylation; Nucleosome; Positioning; Probasin

Indexed keywords

ANDROGEN RECEPTOR; DEOXYRIBONUCLEASE I; DNA FRAGMENT; HISTONE; NUCLEOTIDE; OCTAMER TRANSCRIPTION FACTOR; PROBASIN;

ACETYLATION; ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN; CONTROLLED STUDY; DNA BINDING; DNA FOOTPRINTING; DNA RESPONSIVE ELEMENT; DNA SEQUENCE; DNA TRANSCRIPTION; GEL MOBILITY SHIFT ASSAY; HORMONE SENSITIVITY; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ASSEMBLY; RECEPTOR BINDING;

ACETYLATION; ANDROGEN-BINDING PROTEIN; ANIMALS; BASE PAIRING; CHICKENS; DEOXYRIBONUCLEASE I; DNA FOOTPRINTING; HISTONES; MICE; NUCLEOSOMES; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ANDROGEN; RECOMBINANT PROTEINS;

EID: 33947309924     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2007.01.009     Document Type: Article

References (67)

1. Angelov D., Lenouvel F., Hans F., Muller C.W., Bouvet P., Bednar J., Moudrianakis E.N., Cadet J., and Dimitrov S. The histone octamer is invisible when NF-kappaB binds to the nucleosome. J. Biol. Chem. 279 (2004) 42374-42382
2. Ausió J. Structure and dynamics of transcriptionally active chromatin. J. Cell Sci. 102 (1992) 1-5
3. Ausió J., and Abbott D.W. The role of histone variability in chromatin stability and folding. In: Zlatanova J., and Leuba S.H. (Eds). New Comprehensive Biochemistry. Chromatin Structure and Dynamics: State-of-the-Art vol. 39 (2004), Elsevier, Amsterdam, The Netherlands 241-290
4. Ausió J., Dong F., and van Holde K.E. Use of selectively trypsinized nucleosome core particles to analyze the role of the histone "tails" in the stabilization of the nucleosome. J. Mol. Biol. 206 (1989) 451-463
5. Ausió J., and Moore S.C. Reconstitution of chromatin complexes from high-performance liquid chromatography-purified histones. Methods 15 (1998) 333-342
6. Beato M., Candau R., Chavez S., Mows C., and Truss M. Interaction of steroid hormone receptors with transcription factors involves chromatin remodelling. J. Steroid Biochem. Mol. Biol. 56 (1996) 47-59
7. Beato M., and Eisfeld K. Transcription factor access to chromatin. Nucl. Acids Res. 25 (1997) 3559-3563
8. Beato M., Herrlich P., and Schutz G. Steroid hormone receptors: many actors in search of a plot. Cell 83 (1995) 851-857
9. Brookes D.E., Zandvliet D., Watt F., Russell P.J., and Molloy P.L. Relative activity and specificity of promoters from prostate-expressed genes. Prostate 35 (1998) 18-26
10. Carascossa S., Gobinet J., Georget V., Lucas A., Badia E., Castet A., White R., Nicolas J.C., Cavailles V., and Jalaguier S. Receptor-interacting protein 140 is a repressor of the androgen receptor activity. Mol. Endocrinol. 20 (2006) 1506-1518
11. Claessens F., Verrijdt G., Schoenmakers E., Haelens A., Peeters B., Verhoeven G., and Rombauts W. Selective DNA binding by the androgen receptor as a mechanism for hormone-specific gene regulation. J. Steroid Biochem. Mol. Biol. 76 (2001) 23-30
12. Clemens K.R., Liao X., Wolf V., Wright P.E., and Gottesfeld J.M. Definition of the binding sites of individual zinc fingers in the transcription factor IIIA-5S RNA gene complex. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 10822-10826
13. De Vos P., Claessens F., Peeters B., Rombauts W., Heyns W., and Verhoeven G. Interaction of androgen and glucocorticoid receptor DNA-binding domains with their response elements. Mol. Cell Endocrinol. 90 (1993) R11-R16
14. Dillon N. Heterochromatin structure and function. Biol. Cell 96 (2004) 631-637
15. Dong F., Hansen J.C., and van Holde K.E. DNA and protein determinants of nucleosome positioning on sea urchin 5S rRNA gene sequences in vitro. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 5724-5728
16. Fragoso G., John S., Roberts M.S., and Hager G.L. Nucleosome positioning on the MMTV LTR results from the frequency-biased occupancy of multiple frames. Genes Dev. 9 (1995) 1933-1947
17. 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. The role of hepatocyte nuclear factor-3 alpha (Forkhead Box A1) and androgen receptor in transcriptional regulation of prostatic genes. Mol. Endocrinol. 17 (2003) 1484-1507
18. Garcia Ramirez M., Rocchini C., and Ausió J. Modulation of chromatin folding by histone acetylation. J. Biol. Chem. 270 (1995) 17923-17928
19. Glass C.K., and Rosenfeld M.G. The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev. 14 (2000) 121-141
20. Greenberg N.M., DeMayo F.J., Sheppard P.C., Barrios R., Lebovitz R., Finegold M., Angelopoulou R., Dodd J.G., Duckworth M.L., Rosen J.M., et al. The rat probasin gene promoter directs hormonally and developmentally regulated expression of a heterologous gene specifically to the prostate in transgenic mice. Mol. Endocrinol. 8 (1994) 230-239
21. Gross D.S., and Garrard W.T. Poising chromatin for transcription. Trends Biochem. Sci. 12 (1987) 293-297
22. Harp J.M., Hanson B.L., Timm D.E., and Bunick G.J. Asymmetries in the nucleosome core particle at 2.5 A resolution. Acta Crystallogr. D: Biol. Crystallogr. 56 Pt 12 (2000) 1513-1534
23. Hayes J.J., and Wolffe A.P. Preferential and asymmetric interaction of linker histones with 5S DNA in the nucleosome. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 6415-6419
24. Hediger F., and Gasser S.M. Heterochromatin protein 1: don't judge the book by its cover!. Curr. Opin. Genet. Dev. 16 (2006) 143-150
25. Heinlein C.A., and Chang C. Androgen receptor (AR) coregulators: an overview. Endocr. Rev. 23 (2002) 175-200
26. Howe L., and Ausió J. Nucleosome translational position, not histone acetylation, determines TFIIIA binding to nucleosomal Xenopus laevis 5S rRNA genes. Mol. Cell Biol. 18 (1998) 1156-1162
27. Howe L., Iskandar M., and Ausió J. Folding of chromatin in the presence of heterogeneous histone H1 binding to nucleosomes. J. Biol. Chem. 273 (1998) 11625-11629
28. Hsiao P.W., Deroo B.J., and Archer T.K. Chromatin remodeling and tissue-selective responses of nuclear hormone receptors. Biochem. Cell Biol. 80 (2002) 343-351
29. Jenuwein T., and Allis C.D. Translating the histone code. Science 293 (2001) 1074-1080
30. Jia L., Shen H.C., Wantroba M., Khalid O., Liang G., Wang Q., Gentzschein E., Pinski J.K., Stanczyk F.Z., Jones P.A., and Coetzee G.A. Locus-wide chromatin remodeling and enhanced androgen receptor-mediated transcription in recurrent prostate tumor cells. Mol. Cell Biol. 26 (2006) 7331-7341
31. Kang Z., Janne O.A., and Palvimo J.J. Coregulator recruitment and histone modifications in transcriptional regulation by the androgen receptor. Mol. Endocrinol. 18 (2004) 2633-2648
32. Kasper S., and Matusik R.J. Rat probasin: structure and function of an outlier lipocalin. Biochim. Biophys. Acta 1482 (2000) 249-258
33. Kasper S., Rennie P.S., Bruchovsky N., Sheppard P.C., Cheng H., Lin L., Shiu R.P., Snoek R., and Matusik R.J. Cooperative binding of androgen receptors to two DNA sequences is required for androgen induction of the probasin gene. J. Biol. Chem. 269 (1994) 31763-31769
34. Khorasanizadeh S., and Rastinejad F. Nuclear-receptor interactions on DNA-response elements. Trends Biochem. Sci. 26 (2001) 384-390
35. Lambert J.R., and Nordeen S.K. Steroid-selective initiation of chromatin remodeling and transcriptional activation of the mouse mammary tumor virus promoter is controlled by the site of promoter integration. J. Biol. Chem. 273 (1998) 32708-32714
36. Li Q., and Wrange O. Translational positioning of a nucleosomal glucocorticoid response element modulates glucocorticoid receptor affinity. Genes Dev. 7 (1993) 2471-2482
37. Link K.A., Burd C.J., Williams E., Marshall T., Rosson G., Henry E., Weissman B., and Knudsen K.E. BAF57 governs androgen receptor action and androgen-dependent proliferation through SWI/SNF. Mol. Cell Biol. 25 (2005) 2200-2215
38. List H.J., Lozano C., Lu J., Danielsen M., Wellstein A., and Riegel A.T. Comparison of chromatin remodeling and transcriptional activation of the mouse mammary tumor virus promoter by the androgen and glucocorticoid receptor. Exp. Cell Res. 250 (1999) 414-422
39. List H.J., Smith C.L., Martinez E., Harris V.K., Danielsen M., and Riegel A.T. Effects of antiandrogens on chromatin remodeling and transcription of the integrated mouse mammary tumor virus promoter. Exp. Cell Res. 260 (2000) 160-165
40. Lomberk G., Bensi D., Fernandez-Zapico M.E., and Urrutia R. Evidence for the existence of an HP1-mediated subcode within the histone code. Nat. Cell Biol. 8 (2006) 407-415
41. Luisi B.F., Xu W.X., Otwinowski Z., Freedman L.P., Yamamoto K.R., and Sigler P.B. Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA. Nature 352 (1991) 497-505
42. Marshall T.W., Link K.A., Petre-Draviam C.E., and Knudsen K.E. Differential requirement of SWI/SNF for androgen receptor activity. J. Biol. Chem. 278 (2003) 30605-30613
43. Matuo Y., Adams P.S., Nishi N., Yasumitsu H., Crabb J.W., Matusik R.J., and McKeehan W.L. The androgen-dependent rat prostate protein, probasin, is a heparin-binding protein that co-purifies with heparin-binding growth factor-1. In Vitro Cell Dev. Biol. 25 (1989) 581-584
44. Matuo Y., Nishi N., Muguruma Y., Yoshitake Y., Kurata N., and Wada F. Localization of prostatic basic protein ("probasin") in the rat prostates by use of monoclonal antibody. Biochem. Biophys. Res. Commun. 130 (1985) 293-300
45. Nelson C.C., Hendy S.C., Shukin R.J., Cheng H., Bruchovsky N., Koop B.F., and Rennie P.S. Determinants of DNA sequence specificity of the androgen, progesterone, and glucocorticoid receptors: evidence for differential steroid receptor response elements. Mol. Endocrinol. 13 (1999) 2090-2107
46. Norton V.G., Imai B.S., Yau P., and Bradbury E.M. Histone acetylation reduces nucleosome core particle linking number change. Cell 57 (1989) 449-457
47. Panetta G., Buttinelli M., Flaus A., Richmond T.J., and Rhodes D. Differential nucleosome positioning on Xenopus oocyte and somatic 5 S RNA genes determines both TFIIIA and H1 binding: a mechanism for selective H1 repression. J. Mol. Biol. 282 (1998) 683-697
48. Pennings S., Allan J., and Davey C.S. DNA methylation, nucleosome formation and positioning. Brief Funct. Genomic Proteomic 3 (2005) 351-361
49. Perlmann T., and Wrange O. Specific glucocorticoid receptor binding to DNA reconstituted in a nucleosome. EMBO J. 7 (1988) 3073-3079
50. Pervaiz S., and Brew K. Homology and structure-function correlations between alpha 1-acid glycoprotein and serum retinol-binding protein and its relatives. FASEB J. 1 (1987) 209-214
51. Reid K.J., Hendy S.C., Saito J., Sorensen P., and Nelson C.C. Two classes of androgen receptor elements mediate cooperativity through allosteric interactions. J. Biol. Chem. 276 (2001) 2943-2952
52. Richard-Foy H., and Hager G.L. Sequence-specific positioning of nucleosomes over the steroid-inducible MMTV promoter. EMBO J. 6 (1987) 2321-2328
53. Robyr D., and Wolffe P. Hormone action and chromatin remodelling. Cell Mol. Life Sci. 54 (1998) 113-124
54. Schild C., Claret F.X., Wahli W., and Wolffe A.P. A nucleosome-dependent static loop potentiates estrogen-regulated transcription from the Xenopus vitellogenin B1 promoter in vitro. EMBO J. 12 (1993) 423-433
55. Schoenmakers E., Verrijdt G., Peeters B., Verhoeven G., Rombauts W., and Claessens F. Differences in DNA binding characteristics of the androgen and glucocorticoid receptors can determine hormone-specific responses. J. Biol. Chem. 275 (2000) 12290-12297
56. Shaffer P.L., Jivan A., Dollins D.E., Claessens F., and Gewirth D.T. Structural basis of androgen receptor binding to selective androgen response elements. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 4758-4763
57. Spence A.M., Sheppard P.C., Davie J.R., Matuo Y., Nishi N., McKeehan W.L., Dodd J.G., and Matusik R.J. Regulation of a bifunctional mRNA results in synthesis of secreted and nuclear probasin. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 7843-7847
58. Spencer V.A., and Davie J.R. Role of covalent modifications of histones in regulating gene expression. Gene 240 (1999) 1-12
59. Strahl B.D., and Allis C.D. The language of covalent histone modifications. Nature 403 (2000) 41-45
60. Tatchell K., and Van Holde K.E. Reconstitution of chromatin core particles. Biochemistry 16 (1977) 5295-5303
61. Truss M., Bartsch J., Schelbert A., Hache R.J., and Beato M. Hormone induces binding of receptors and transcription factors to a rearranged nucleosome on the MMTV promoter in vivo. EMBO J. 14 (1995) 1737-1751
62. Turner B.M. Histone acetylation as an epigenetic determinant of long-term transcriptional competence. Cell Mol. Life Sci. 54 (1998) 21-31
63. Turner B.M. Reading signals on the nucleosome with a new nomenclature for modified histones. Nat. Struct. Mol. Biol. 12 (2005) 110-112
64. Wang X., Moore S.C., Laszckzak M., and Ausió J. Acetylation increases the alpha-helical content of the histone tails of the nucleosome. J. Biol. Chem. 275 (2000) 35013-35020
65. Yeung L.H., Read J.T., Sorenson P., Nelson C.C., Jia W., and Rennie P.S. Identification and characterization of a prostate-specific androgen-independent protein-binding site in the probasin promoter. Biochem. J. 371 (2003) 843-855
66. Yu D., Jia W.W., Gleave M.E., Nelson C.C., and Rennie P.S. Prostate-tumor targeting of gene expression by lentiviral vectors containing elements of the probasin promoter. Prostate 59 (2004) 370-382
67. Zhang J., Thomas T.Z., Kasper S., and Matusik R.J. A small composite probasin promoter confers high levels of prostate-specific gene expression through regulation by androgens and glucocorticoids in vitro and in vivo. Endocrinology 141 (2000) 4698-4710