Impact of chromatin structure on PR signaling: Transition from local to global analysis

Molecular and Cellular Endocrinology

Volumn 357, Issue 1-2, 2012, Pages 30-36

  Grøntved, Lars ^a   Hager, Gordon L ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Chromatin; Dynamics; Nuclear architecture; Progesterone; Receptor; Steroid

Indexed keywords

CELL NUCLEUS DNA; GLUCOCORTICOID RECEPTOR; PROGESTERONE RECEPTOR; STEROID RECEPTOR;

CELL POPULATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONFORMATIONAL TRANSITION; DEVELOPMENTAL STAGE; GENETIC ANALYSIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; RECEPTOR BINDING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS; STRUCTURE ANALYSIS; TISSUE DIFFERENTIATION; TISSUE SPECIFICITY;

ANIMALS; CHROMATIN; GENE EXPRESSION REGULATION; HUMANS; RECEPTORS, PROGESTERONE; RECEPTORS, STEROID; SIGNAL TRANSDUCTION;

EID: 84860343787     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.09.006     Document Type: Review

References (85)

1. Archer T.K., Lefebvre P., Wolford R.G., Hager G.L. Transcription factor loading on the MMTV promoter: a bimodal mechanism for promoter activation. Science 1992, 255:1573-1576.
2. Bain D.L., Heneghan A.F., Connaghan-Jones K.D., Miura M.T. Nuclear receptor structure: implications for function. Annu. Rev. Physiol. 2007, 69:201-220.
3. Bartke T., Vermeulen M., Xhemalce B., Robson S.C., Mann M., Kouzarides T. Nucleosome-interacting proteins regulated by DNA and histone methylation. Cell 2010, 143:470-484.
4. Baumann C.T., Maruvada P., Hager G.L., Yen P.M. Nuclear-cytoplasmic shuttling by thyroid hormone receptors: multiple protein interactions are required for nuclear retention. J. Biol. Chem. 2001, 276:11237-11245.
5. Belikov S., Astrand C., Wrange O. FoxA1 binding directs chromatin structure and the functional response of a glucocorticoid receptor-regulated promoter. Mol. Cell. Biol. 2009, 29:5413-5425.
6. Belmont A.S. Estrogen fueled, nuclear kiss: did it move for you?. Nucleus 2010, 1:440-443.
7. Bernstein B.E., Stamatoyannopoulos J.A., Costello J.F., Ren B., Milosavljevic A., Meissner A., Kellis M., Marra M.A., Beaudet A.L., Ecker J.R., Farnham P.J., Hirst M., Lander E.S., Mikkelsen T.S., Thomson J.A. The NIH roadmap epigenomics mapping consortium. Nat. Biotechnol. 2010, 28:1045-1048.
8. Blomquist P., Li Q., Wrange O. The affinity of nuclear factor 1 for its DNA site is drastically reduced by nucleosome organization irrespective of its rotational or translational position. J. Biol. Chem. 1996, 271:153-159.
9. Bosisio D., Marazzi I., Agresti A., Shimizu N., Bianchi M.E., Natoli G. A hyper-dynamic equilibrium between promoter-bound and nucleoplasmic dimers controls NF-kB-dependent gene activity. EMBO J. 2006, 25:798-810.
10. Botos J., Xian W., Smith D.F., Smith C.L. Progesterone receptor deficient in chromatin binding has an altered cellular state. J. Biol. Chem. 2004, 279:15231-15239.
11. Boyle A.P., Song L., Lee B.K., London D., Keefe D., Birney E., Iyer V.R., Crawford G.E., Furey T.S. High-resolution genome-wide in vivo footprinting of diverse transcription factors in human cells. Genome Res. 2010, 21:456-464.
12. Bresnick E.H., Bustin M., Marsaud V., Richard-Foy H., Hager G.L. The transcriptionally-active MMTV promoter is depleted of histone H1. Nucleic Acids Res. 1992, 20:273-278.
13. Bustin M., Catez F., Lim J.H. The dynamics of histone H1 function in chromatin. Mol. Cell 2005, 17:617-620.
14. Campos E., Reinberg D. Histones: annotating chromatin. Annu. Rev. Genet. 2008, 43:559-599.
15. Chodavarapu R.K., Feng S., Bernatavichute Y.V., Chen P.Y., Stroud H., Yu Y., Hetzel J.A., Kuo F., Kim J., Cokus S.J., Casero D., Bernal M., Huijser P., Clark A.T., Kramer U., Merchant S.S., Zhang X., Jacobsen S.E., Pellegrini M. Relationship between nucleosome positioning and DNA methylation. Nature 2010, 466:388-392.
16. Cordingley M.G., Riegel A.T., Hager G.L. Steroid-dependent interaction of transcription factors with the inducible promoter of mouse mammary tumor virus in vivo. Cell 1987, 48:261-270.
17. Cremer T., Cremer C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2001, 2:292-301.
18. Eeckhoute J., Carroll J.S., Geistlinger T.R., Torres-Arzayus M.I., Brown M. A cell-type-specific transcriptional network required for estrogen regulation of cyclin D1 and cell cycle progression in breast cancer. Genes Dev. 2006, 20:2513-2526.
19. Elbi C., Walker D.A., Romero G., Sullivan W.P., Toft D.O., Hager G.L., DeFranco D.B. Molecular chaperones function as steroid receptor nuclear mobility factors. Proc. Natl. Acad. Sci. USA 2004, 101:2876-2881.
20. Fletcher T.M., Ryu B.-W., Baumann C.T., Warren B.S., Fragoso G., John S., Hager G.L. Structure and dynamic properties of the glucocorticoid receptor-induced chromatin transition at the MMTV promoter. Mol. Cell. Biol. 2000, 20:6466-6475.
21. Fletcher T.M., Xiao N., Mautino G., Baumann C.T., Wolford R.G., Warren B.S., Hager G.L. ATP-dependent mobilization of the glucocorticoid receptor during chromatin remodeling. Mol. Cell. Biol. 2002, 22:3255-3263.
22. Fragoso G., John S., Roberts M.S., Hager G.L. Nucleosome positioning on the MMTV LTR results from the frequency-biased occupancy of multiple frames. Genes Dev. 1995, 9:1933-1947.
23. Fragoso G., Pennie W.D., John S., Hager G.L. The position and length of the steroid-dependent hypersensitive region in the mouse mammary tumor virus long terminal repeat are invariant despite multiple nucleosome B frames. Mol. Cell. Biol. 1998, 18:3633-3644.
24. Freeman B.C., Yamamoto K.R. Disassembly of transcriptional regulatory complexes by molecular chaperones. Science 2002, 296:2232-2235.
25. Fryer C.J., Archer T.K. Chromatin remodeling by the glucocorticoid receptor requires the BRG1 complex. Nature 1998, 393:88-91.
26. Fullwood M.J., Liu M.H., Pan Y.F., Liu J., Xu H., Mohamed Y.B., Orlov Y.L., Velkov S., Ho A., Mei P.H., Chew E.G., Huang P.Y., Welboren W.J., Han Y., Ooi H.S., Ariyaratne P.N., Vega V.B., Luo Y., Tan P.Y., Choy P.Y., Wansa K.D., Zhao B., Lim K.S., Leow S.C., Yow J.S., Joseph R., Li H., Desai K.V., Thomsen J.S., Lee Y.K., Karuturi R.K., Herve T., Bourque G., Stunnenberg H.G., Ruan X., Cacheux-Rataboul V., Sung W.K., Liu E.T., Wei C.L., Cheung E., Ruan Y. An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 2009, 462:58-64.
27. Guelen L., Pagie L., Brasset E., Meuleman W., Faza M.B., Talhout W., Eussen B.H., de Klein A., Wessels L., de Laat W., van Steensel B. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 2008, 453:948-951.
28. Hadjur S., Williams L.M., Ryan N.K., Cobb B.S., Sexton T., Fraser P., Fisher A.G., Merkenschlager M. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 2009, 460:410-413.
29. Hager G.L. Footprints by deep sequencing. Nat. Methods 2010, 6:254-255.
30. Hager G.L., Elbi C., Johnson T.A., Voss T.C., Nagaich A.K., Schiltz R.L., Qiu Y., John S. Chromatin dynamics and the evolution of alternate promoter states. Chromosome Res. 2006, 14:107-116.
31. Hager G.L., McNally J.G., Misteli T. Transcription dynamics. Mol. Cell 2009, 35:741-753.
32. Hakim O., John S., Ling J.Q., Biddie S.C., Hoffman A.R., Hager G.L. Glucocorticoid receptor activation of the Ciz1-Lcn2 locus by long range interactions. J. Biol. Chem. 2009, 284:6048-6052.
33. Hakim O., Sung M.H., Hager G.L. 3D shortcuts to gene regulation. Curr. Opin. Cell Biol. 2010, 22:305-313.
34. Hakim O., Sung M.H., Voss T.C., John S., Splinter E., Sabo P.J., Thurman R.E., Stamatoyannopoulos J.A., de Laat W., Hager G.L. Diverse gene reprogramming events occur in the same spatial clusters of distal regulatory elements. Genome Res. 2011, 21:697-706.
35. Hepperger C., Mannes A., Merz J., Peters J., Dietzel S. Three-dimensional positioning of genes in mouse cell nuclei. Chromosoma 2008, 117:535-551.
36. Hesselberth J.R., Zhang Z., Sabo P.J., Chen X., Sandstrom R., Reynolds A.P., Thurman R.E., Neph S., Kuehn M.S., Noble W.S., Fields S., Stamatoyannopoulos J.A. Global mapping of protein-DNA interactions in vivo by digital genomic footprinting. Nat. Methods 2009, 6:283-289.
37. Htun H., Holth L.T., Walker D., Davie J.R., Hager G.L. Direct visualization of ligand occupied and unoccupied human estrogen receptor alpha reveals a role for ligand in the nuclear distribution of the receptor. Mol. Biol. Cell 1999, 10:471-486.
38. Hu Q., Kwon Y.S., Nunez E., Cardamone M.D., Hutt K.R., Ohgi K.A., Garcia-Bassets I., Rose D.W., Glass C.K., Rosenfeld M.G., Fu X.D. Enhancing nuclear receptor-induced transcription requires nuclear motor and LSD1-dependent gene networking in interchromatin granules. Proc. Natl. Acad. Sci. USA 2008, 105:19199-19204.
39. Hurtado A., Holmes K.A., Ross-Innes C.S., Schmidt D., Carroll J.S. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat. Genet. 2010, 43:27-33.
40. Jiang C., Pugh B.F. Nucleosome positioning and gene regulation: advances through genomics. Nat. Rev. Genet. 2009, 10:161-172.
41. John S., Sabo P.J., Johnson T.A., Sung M.H., Biddie S.C., Lightman S.L., Voss T.C., Davis S.R., Meltzer P.S., Stamatoyannopoulos J.A., Hager G.L. Interaction of the glucocorticoid receptor with the global chromatin landscape. Mol. Cell 2008, 29:611-624.
42. John S., Sabo P.J., Thurman R.E., Sung M.H., Biddie S.C., Johnson T.A., Hager G.L., Stamatoyannopoulos J.A. Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat. Genet. 2011, 43:264-268.
43. Kagey M.H., Newman J.J., Bilodeau S., Zhan Y., Orlando D.A., van Berkum N.L., Ebmeier C.C., Goossens J., Rahl P.B., Levine S.S., Taatjes D.J., Dekker J., Young R.A. Mediator and cohesin connect gene expression and chromatin architecture. Nature 2010, 467:430-435.
44. Kocanova S., Kerr E.A., Rafique S., Boyle S., Katz E., Caze-Subra S., Bickmore W.A., Bystricky K. Activation of estrogen-responsive genes does not require their nuclear co-localization. PLoS Genet. 2010, 6:e1000922.
45. Koop R., Di C.L., Beato M. Histone H1 enhances synergistic activation of the MMTV promoter in chromatin. EMBO J. 2003, 22:588-599.
46. Lanzuolo C., Roure V., Dekker J., Bantignies F., Orlando V. Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Nat. Cell Biol. 2007, 9:1167-1174.
47. Lee H.-L., Archer T.K. Nucleosome mediated disruption of transcription factor: chromatin initiation complexes at the mouse mammary tumour virus long terminal repeat in vivo. Mol. Cell Biol. 1994, 14:32-41.
48. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell 2007, 128:707-719.
49. Li Q., Wrange O. Accessibility of a glucocorticoid response element in a nucleosome depends on its rotational positioning. Mol. Cell Biol. 1995, 15:4375-4384.
50. Lieberman-Aiden E., van Berkum N.L., Williams L., Imakaev M., Ragoczy T., Telling A., Amit I., Lajoie B.R., Sabo P.J., Dorschner M.O., Sandstrom R., Bernstein B., Bender M.A., Groudine M., Gnirke A., Stamatoyannopoulos J., Mirny L.A., Lander E.S., Dekker J. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326:289-293.
51. Luger K., Mader A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8å resolution (see comments). Nature 1997, 389:251-260.
52. Lupien M., Eeckhoute J., Meyer C.A., Wang Q., Zhang Y., Li W., Carroll J.S., Liu X.S., Brown M. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 2008, 132:958-970.
53. McNally J.G., Mueller W.G., Walker D., Wolford R.G., Hager G.L. The glucocorticoid receptor: rapid exchange with regulatory sites in living cells. Science 2000, 287:1262-1265.
54. Metivier R., Penot G., Hubner M.R., Reid G., Brand H., Kos M., Gannon F. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 2003, 115:751-763.
55. Nagaich A.K., Walker D.A., Wolford R.G., Hager G.L. Rapid periodic binding and displacement of the glucocorticoid receptor during chromatin remodeling. Mol. Cell 2004, 14:163-174.
56. Negre N., Brown C.D., Ma L., Bristow C.A., Miller S.W., Wagner U., Kheradpour P., Eaton M.L., Loriaux P., Sealfon R., Li Z., Ishii H., Spokony R.F., Chen J., Hwang L., Cheng C., Auburn R.P., Davis M.B., Domanus M., Shah P.K., Morrison C.A., Zieba J., Suchy S., Senderowicz L., Victorsen A., Bild N.A., Grundstad A.J., Hanley D., MacAlpine D.M., Mannervik M., Venken K., Bellen H., White R., Gerstein M., Russell S., Grossman R.L., Ren B., Posakony J.W., Kellis M., White K.P. A cis-regulatory map of the Drosophila genome. Nature 2011, 471:527-531.
57. Osborne C.S., Chakalova L., Brown K.E., Carter D., Horton A., Debrand E., Goyenechea B., Mitchell J.A., Lopes S., Reik W., Fraser P. Active genes dynamically colocalize to shared sites of ongoing transcription. Nat. Genet. 2004, 36:1065-1071.
58. Perlmann T., Wrange O. Specific glucocorticoid receptor binding to DNA reconstituted in a nucleosome. EMBO J. 1988, 7:3073-3079.
59. Pina B., Brüggemeier U., Beato M. Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter. Cell 1990, 60:719-731.
60. Prufer K., Racz A., Lin G.C., Barsony J. Dimerization with retinoid X receptors promotes nuclear localization and subnuclear targeting of vitamin D receptors. J. Biol. Chem. 2000, 275:41114-41123.
61. Rayasam G.V., Elbi C., Walker D.A., Wolford R.G., Fletcher T.M., Edwards D.P., Hager G.L. Ligand specific dynamics of the progesterone receptor in living cells and during chromatin remodeling in vitro. Mol. Cell. Biol. 2005, 25:2406-2418.
62. Richard-Foy H., Hager G.L. Sequence specific positioning of nucleosomes over the steroid-inducible MMTV promoter. EMBO J. 1987, 6:2321-2328.
63. Rishi V., Bhattacharya P., Chatterjee R., Rozenberg J., Zhao J., Glass K., Fitzgerald P., Vinson C. CpG methylation of half-CRE sequences creates C/EBPalpha binding sites that activate some tissue-specific genes. Proc. Natl. Acad. Sci. USA 2010, 107:20311-20316.
64. Schubeler D. Epigenomics: methylation matters. Nature 2009, 462:296-297.
65. Serandour A.A., Avner S., Percevault F., Demay F., Bizot M., Lucchetti-Miganeh C., Barloy-Hubler F., Brown M., Lupien M., Metivier R., Salbert G., Eeckhoute J. Epigenetic switch involved in activation of pioneer factor FOXA1-dependent enhancers. Genome Res. 2011, 21:555-565.
66. Sharp Z.D., Mancini M.G., Hinojos C.A., Dai F., Berno V., Szafran A.T., Smith K.P., Lele T.T., Ingber D.E., Mancini M.A. Estrogen-receptor-alpha exchange and chromatin dynamics are ligand- and domain-dependent. J. Cell Sci. 2006, 119:4101-4116.
67. Siersbaek R., Nielsen R., John S., Sung M.H., Baek S., Loft A., Hager G.L., Mandrup S. Adipogenic development is associated with extensive early remodeling of the chromatin landscape and establishment of transcription factor 'hotspots'. EMBO J. 2011, 30:1459-1472.
68. Simonis M., Kooren J., de Laat W. An evaluation of 3C-based methods to capture DNA interactions. Nat. Methods 2007, 4:895-901.
69. Splinter E., Heath H., Kooren J., Palstra R.J., Klous P., Grosveld F., Galjart N., de Laat W. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev. 2006, 20:2349-2354.
70. Stavreva D.A., Muller W.G., Hager G.L., Smith C.L., McNally J.G. Rapid glucocorticoid receptor exchange at a promoter is coupled to transcription and regulated by chaperones and proteasomes. Mol. Cell. Biol. 2004, 24:2682-2697.
71. Stearns T. Green fluorescent protein. The green revolution. Curr. Biol. 1995, 5:262-264.
72. Steger D.J., Grant G.R., Schupp M., Tomaru T., Lefterova M.I., Schug J., Manduchi E., Stoeckert C.J., Lazar M.A. Propagation of adipogenic signals through an epigenomic transition state. Genes Dev. 2010, 24:1035-1044.
73. Subtil-Rodriguez A., Millan-Arino L., Quiles I., Ballare C., Beato M., Jordan A. Progesterone induction of the 11beta-hydroxysteroid dehydrogenase type 2 promoter in breast cancer cells involves coordinated recruitment of STAT5A and progesterone receptor to a distal enhancer and polymerase tracking. Mol. Cell. Biol. 2008, 28:3830-3849.
74. Sun L.H., Pfendner E.G., Senior M.B., Frankel F.R. Progesterone, glucocorticoid and estradiol receptors in MCF-7 cells bind to chromatin. Mol. Cell. Endocrinol. 1983, 30:267-278.
75. Talbert P.B., Henikoff S. Histone variants - ancient wrap artists of the epigenome. Nat. Rev. Mol. Cell Biol. 2010, 11:264-275.
76. Tomura A., Goto K., Morinaga H., Nomura M., Okabe T., Yanase T., Takayanagi R., Nawata H. The subnuclear three-dimensional image analysis of androgen receptor fused to green fluorescence protein. J. Biol. Chem. 2001, 276:28395-28401.
77. Venditti P., Di Croce L., Kauer M., Blank T., Becker P.B., Beato M. Assembly of MMTV promoter minichromosomes with positioned nucleosomes precludes NF1 access but not restriction enzyme cleavage. Nucleic Acids Res. 1998, 26:3657-3666.
78. Vicent G.P., Ballare C., Nacht A.S., Clausell J., Subtil-Rodriguez A., Quiles I., Jordan A., Beato M. Induction of progesterone target genes requires activation of Erk and Msk kinases and phosphorylation of histone H3. Mol. Cell 2006, 24:367-381.
79. Vicent G.P., Nacht A.S., Smith C.L., Peterson C.L., Dimitrov S., Beato M. DNA instructed displacement of histones H2A and H2B at an inducible promoter. Mol. Cell 2004, 16:439-452.
80. Vicent G.P., Zaurin R., Nacht A.S., Font-Mateu J., Le Dily F., Beato M. Nuclear factor 1 synergizes with progesterone receptor on the mouse mammary tumor virus promoter wrapped around a histone H3/H4 tetramer by facilitating access to the central hormone-responsive elements. J. Biol. Chem. 2010, 285:2622-2631.
81. Vicent G.P., Zaurin R., Nacht A.S., Li A., Font-Mateu J., Le Dily F., Vermeulen M., Mann M., Beato M. Two chromatin remodeling activities cooperate during activation of hormone responsive promoters. PLoS Genet. 2009, 5:e1000567.
82. Voss T.C., John S., Hager G.L. Single cell analysis of glucocorticoid receptor action reveals that stochastic post-chromatin association mechanisms regulate ligand-specific transcription. Mol. Endocrinol. 2006, 20:2641-2655.
83. Voss T.C., Schiltz R.L., Sung M.H., Johnson T.A., John S., Hager G.L. Combinatorial probabilistic chromatin interactions produce transcriptional heterogeneity. J. Cell Sci. 2009, 122:345-356.
84. Wang Q., Li W., Liu X.S., Carroll J.S., Janne O.A., Keeton E.K., Chinnaiyan A.M., Pienta K.J., Brown M. A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol. Cell 2007, 27:380-392.
85. Wu J.I., Lessard J., Crabtree G.R. Understanding the words of chromatin regulation. Cell 2009, 136:200-206.