The changing paradigm: estrogen receptor α recognition on DNA and within the dynamic nature of nucleosomes

William M. Scovell; Sachindra R. Joshi; William M. Scovell; Sachindra R. Joshi

doi:10.3934/molsci.2015.2.48

AIMS Molecular Science

2015, Volume 2, Issue 2: 48-63. doi: 10.3934/molsci.2015.2.48

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The changing paradigm: estrogen receptor α recognition on DNA and within the dynamic nature of nucleosomes

William M. Scovell ^{1
,
,},
Sachindra R. Joshi ^1,2

1.
Department of Chemistry, Bowling Green State University, Bowling Green, Ohio 43403, USA;
2.
Department of Biological Sciences, Bowling Green State University, Bowling Green, Ohio 43403, USA

Received: 19 January 2015 Accepted: 25 February 2015 Published: 04 March 2015

Estrogen receptor alpha (ERα) plays a major role in the expression of estrogen-responsive genes. Although its conventional binding characteristics have been considered coincident with & exclusively in the class of steroid hormone receptors,increasing evidence challenges this paradigm. ERα was shown to bind to consensus estrogen response element half-sites (cHERE) in DNA in the presence of the ubiquitous,abundant & conserved architectural protein,high mobility group protein 1 (HMGB1). It also binds to direct repeats with various spacers,in addition to everted repeats. These in vitro binding sites have been shown to be active in vivo,with both the binding affinity and transcriptional activity increased in the presence of HMGB1. Surprisingly,ERα does not bind to the optimally oriented cERE at the dyad in rotationally phased and translationally positioned nucleosomes. However,the presence of HMGB1 restructures the nucleosome to facilitate increased ERα accessibility,resulting in sequence-specific estrogen receptor binding. The finding that HMGB1 interacts with unbound ERα provides a unique avenue for enhanced ERα activity and possibly an increase in the extent of targeting at estrogen-responsive genes. The findings are consistent with ERα 1) targeting a much wider selection of genomic response elements (half-sites and inverted,direct and everted repeats) and 2) exhibiting characteristics of both steroid and non steroid nuclear receptors. Growing evidence already shows a competition occurs at the DNA level between ERα and the non steroid nuclear hormone receptor,thyroid receptor (TR). Collectively,these reports suggest a less restrictive cataloging for estrogen receptor and a broader paradigm for understanding its role in the regulation of estrogen-responsive genes and influence on non steroid hormone receptor activities.

Keywords:

Citation: William M. Scovell, Sachindra R. Joshi. The changing paradigm: estrogen receptor α recognition on DNA and within the dynamic nature of nucleosomes[J]. AIMS Molecular Science, 2015, 2(2): 48-63. doi: 10.3934/molsci.2015.2.48

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Abstract

References

[1]	Aranda A,Pascual A (2001) Nuclear hormone receptors and gene expression. Physiol Rev 81: 1269-1304.
[2]	Deroo BJ,Korach KS (2006) Estrogen receptors and human disease. J Clin Invest 116: 561-570. doi: 10.1172/JCI27987
[3]	Klinge CM (2001) Estrogen receptor interaction with estrogen response elements. Nucleic Acids Res 29: 2905-2919. doi: 10.1093/nar/29.14.2905
[4]	Das D,Peterson RC,Scovell WM (2004) High mobility group B proteins facilitate strong estrogen receptor binding to classical and half-site estrogen response elements and relax binding selectivity. Mol Endocrinol 18: 2616-2632. doi: 10.1210/me.2004-0125
[5]	El Marzouk S,Gahattamaneni R,Joshi SR,et al. (2008) The plasticity of estrogen receptor-DNA complexes: binding affinity and specificity of estrogen receptors to estrogen response element half-sites separated by variant spacers. J Steroid Biochem Mol Biol 110: 186-195. doi: 10.1016/j.jsbmb.2008.03.034
[6]	Gruber CJ,Gruber DM,Gruber IM,et al. (2004) Anatomy of the estrogen response element. Trends Endocrinol Metab 15: 73-78. doi: 10.1016/j.tem.2004.01.008
[7]	O'Lone R,Frith MC,Karlsson EK,et al. (2004) Genomic targets of nuclear estrogen receptors. Mol Endocrinol 18: 1859-1875. doi: 10.1210/me.2003-0044
[8]	Klinge CM,Jernigan SC,Mattingly KA,et al. (2004) Estrogen response element-dependent regulation of transcriptional activation of estrogen receptors alpha and beta by coactivators and corepressors. J Mol Endocrinol 33: 387-410. doi: 10.1677/jme.1.01541
[9]	Melvin VS,Edwards DP (1999) Coregulatory proteins in steroid hormone receptor action: the role of chromatin high mobility group proteins HMG-1 and -2. Steroids 64: 576-586. doi: 10.1016/S0039-128X(99)00036-7
[10]	Lonard DM,O'Malley B W (2007) Nuclear receptor coregulators: judges,juries,and executioners of cellular regulation. Mol Cell 27: 691-700. doi: 10.1016/j.molcel.2007.08.012
[11]	Lonard DM,O'Malley BW (2006) The expanding cosmos of nuclear receptor coactivators. Cell 125: 411-414. doi: 10.1016/j.cell.2006.04.021
[12]	Barkhem T,Haldosen LA,Gustafsson JA,et al. (2002) Transcriptional synergism on the pS2 gene promoter between a p160 coactivator and estrogen receptor-alpha depends on the coactivator subtype,the type of estrogen response element,and the promoter context. Mol Endocrinol 16: 2571-2581. doi: 10.1210/me.2002-0051
[13]	Thomas JO,Travers AA (2001) HMG1 and 2,and related 'architectural' DNA-binding proteins. Trends Biochem Sci 26: 167-174. doi: 10.1016/S0968-0004(01)01801-1
[14]	Bustin M (1999) Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol Cell Biol 19: 5237-5246.
[15]	Bianchi ME,Agresti A (2005) HMG proteins: dynamic players in gene regulation and differentiation. Curr Opin Genet Dev 15: 496-506. doi: 10.1016/j.gde.2005.08.007
[16]	Ross ED,Hardwidge PR,Maher LJ,3rd (2001) HMG proteins and DNA flexibility in transcription activation. Mol Cell Biol 21: 6598-6605. doi: 10.1128/MCB.21.19.6598-6605.2001
[17]	Ju BG,Lunyak VV,Perissi V,et al. (2006) A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. Science 312: 1798-1802. doi: 10.1126/science.1127196
[18]	Das D,Scovell WM (2001) The binding interaction of HMG-1 with the TATA-binding protein/TATA complex. J Biol Chem 276: 32597-32605. doi: 10.1074/jbc.M011792200
[19]	Verrier CS,Roodi N,Yee CJ,et al. (1997) High-mobility group (HMG) protein HMG-1 and TATA-binding protein-associated factor TAF(II)30 affect estrogen receptor-mediated transcriptional activation. Mol Endocrinol 11: 1009-1019. doi: 10.1210/mend.11.8.9962
[20]	Ge H,Roeder RG (1994) The high mobility group protein HMG1 can reversibly inhibit class II gene transcription by interaction with the TATA-binding protein. J Biol Chem 269: 17136-17140.
[21]	Onate SA,Prendergast P,Wagner JP,et al. (1994) The DNA-bending protein HMG-1 enhances progesterone receptor binding to its target DNA sequences. Mol Cell Biol 14: 3376-3391.
[22]	Boonyaratanakornkit V,Melvin V,Prendergast P,et al. (1998) High-mobility group chromatin proteins 1 and 2 functionally interact with steroid hormone receptors to enhance their DNA binding in vitro and transcriptional activity in mammalian cells. Mol Cell Biol 18: 4471-4487.
[23]	Romine LE,Wood JR,Lamia LA,et al. (1998) The high mobility group protein 1 enhances binding of the estrogen receptor DNA binding domain to the estrogen response element. Mol Endocrinol 12: 664-674. doi: 10.1210/mend.12.5.0111
[24]	Zhang CC,Krieg S,Shapiro DJ (1999) HMG-1 stimulates estrogen response element binding by estrogen receptor from stably transfected HeLa cells. Mol Endocrinol 13: 632-643. doi: 10.1210/mend.13.4.0264
[25]	Jayaraman L,Moorthy NC,Murthy KG,et al. (1998) High mobility group protein-1 (HMG-1) is a unique activator of p53. Genes Dev 12: 462-472. doi: 10.1101/gad.12.4.462
[26]	Zappavigna V,Falciola L,Helmer-Citterich M,et al. (1996) HMG1 interacts with HOX proteins and enhances their DNA binding and transcriptional activation. EMBO J 15: 4981-4991.
[27]	Zwilling S,Konig H,Wirth T (1995) High mobility group protein 2 functionally interacts with the POU domains of octamer transcription factors. EMBO J 14: 1198-1208.
[28]	Butteroni C,De Felici M,Scholer HR,et al. (2000) Phage display screening reveals an association between germline-specific transcription factor Oct-4 and multiple cellular proteins. J Mol Biol 304: 529-540. doi: 10.1006/jmbi.2000.4238
[29]	Brickman JM,Adam M,Ptashne M (1999) Interactions between an HMG-1 protein and members of the Rel family. Proc Natl Acad Sci U S A 96: 10679-10683. doi: 10.1073/pnas.96.19.10679
[30]	Bonaldi T,Langst G,Strohner R,et al. (2002) The DNA chaperone HMGB1 facilitates ACF/CHRAC-dependent nucleosome sliding. EMBO J 21: 6865-6873. doi: 10.1093/emboj/cdf692
[31]	Formosa T (2012) The role of FACT in making and breaking nucleosomes. Biochim Biophys Acta 1819: 247-255. doi: 10.1016/j.bbagrm.2011.07.009
[32]	Metivier R,Penot G,Hubner MR,et al. (2003) Estrogen receptor-alpha directs ordered,cyclical,and combinatorial recruitment of cofactors on a natural target promoter. Cell 115: 751-763. doi: 10.1016/S0092-8674(03)00934-6
[33]	Carroll JS,Brown M (2006) Estrogen receptor target gene: an evolving concept. Mol Endocrinol 20: 1707-1714. doi: 10.1210/me.2005-0334
[34]	Carroll JS,Meyer CA,Song J,et al. (2006) Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38: 1289-1297. doi: 10.1038/ng1901
[35]	Fan HY,He X,Kingston RE,et al. (2003) Distinct strategies to make nucleosomal DNA accessible. Mol Cell 11: 1311-1322. doi: 10.1016/S1097-2765(03)00192-8
[36]	Kinyamu HK,Archer TK (2004) Modifying chromatin to permit steroid hormone receptor-dependent transcription. Biochim Biophys Acta 1677: 30-45. doi: 10.1016/j.bbaexp.2003.09.015
[37]	Becker PB,Horz W (2002) ATP-dependent nucleosome remodeling. Annu Rev Biochem 71: 247-273. doi: 10.1146/annurev.biochem.71.110601.135400
[38]	Joshi SR,Ghattamaneni RB,Scovell WM (2011) Expanding the paradigm for estrogen receptor binding and transcriptional activation. Mol Endocrinol 25: 980-994. doi: 10.1210/me.2010-0302
[39]	Li Q,Bjork U,Wrange O (1999) Assays for interaction of transcription factor with nucleosome. Methods Enzymol 304: 313-332. doi: 10.1016/S0076-6879(99)04019-7
[40]	Joshi SR,Sarpong YC,Peterson RC,et al. (2012) Nucleosome dynamics: HMGB1 relaxes canonical nucleosome structure to facilitate estrogen receptor binding. Nucleic Acids Res 40: 10161-10171. doi: 10.1093/nar/gks815
[41]	Ner SS,Travers AA,Churchill ME (1994) Harnessing the writhe: a role for DNA chaperones in nucleoprotein-complex formation. Trends Biochem Sci 19: 185-187. doi: 10.1016/0968-0004(94)90017-5
[42]	Wolffe AP,Hayes JJ (1999) Chromatin disruption and modification. Nucleic Acids Res 27: 711-720. doi: 10.1093/nar/27.3.711
[43]	Melvin VS,Harrell C,Adelman JS,et al. (2004) The role of the C-terminal extension (CTE) of the estrogen receptor alpha and beta DNA binding domain in DNA binding and interaction with HMGB. J Biol Chem 279: 14763-14771. doi: 10.1074/jbc.M313335200
[44]	Ediger TR,Park SE,Katzenellenbogen BS (2002) Estrogen receptor inducibility of the human Na+/H+ exchanger regulatory factor/ezrin-radixin-moesin binding protein 50 (NHE-RF/EBP50) gene involving multiple half-estrogen response elements. Mol Endocrinol 16: 1828-1839. doi: 10.1210/me.2001-0290
[45]	Vasudevan N,Ogawa S,Pfaff D (2002) Estrogen and thyroid hormone receptor interactions: physiological flexibility by molecular specificity. Physiol Rev 82: 923-944. doi: 10.1152/physrev.00014.2002
[46]	Zhu YS,Yen PM,Chin WW,et al. (1996) Estrogen and thyroid hormone interaction on regulation of gene expression. Proc Natl Acad Sci U S A 93: 12587-12592. doi: 10.1073/pnas.93.22.12587
[47]	Kingston RE,Narlikar GJ (1999) ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes Dev 13: 2339-2352. doi: 10.1101/gad.13.18.2339
[48]	Vignali M,Hassan AH,Neely KE,et al. (2000) ATP-dependent chromatin-remodeling complexes. Mol Cell Biol 20: 1899-1910. doi: 10.1128/MCB.20.6.1899-1910.2000
[49]	Narlikar GJ,Sundaramoorthy R,Owen-Hughes T (2013) Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154: 490-503. doi: 10.1016/j.cell.2013.07.011
[50]	Xue Y,Wong J,Moreno GT,et al. (1998) NURD,a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell 2: 851-861. doi: 10.1016/S1097-2765(00)80299-3
[51]	Schnitzler G,Sif S,Kingston RE (1998) Human SWI/SNF interconverts a nucleosome between its base state and a stable remodeled state. Cell 94: 17-27. doi: 10.1016/S0092-8674(00)81217-9
[52]	Lorch Y,Cairns BR,Zhang M,et al. (1998) Activated RSC-nucleosome complex and persistently altered form of the nucleosome. Cell 94: 29-34. doi: 10.1016/S0092-8674(00)81218-0
[53]	Narlikar GJ,Phelan ML,Kingston RE (2001) Generation and interconversion of multiple distinct nucleosomal states as a mechanism for catalyzing chromatin fluidity. Mol Cell 8: 1219-1230. doi: 10.1016/S1097-2765(01)00412-9
[54]	Cote J,Peterson CL,Workman JL (1998) Perturbation of nucleosome core structure by the SWI/SNF complex persists after its detachment,enhancing subsequent transcription factor binding. Proc Natl Acad Sci U S A 95: 4947-4952. doi: 10.1073/pnas.95.9.4947
[55]	Bazett-Jones DP,Cote J,Landel CC,et al. (1999) The SWI/SNF complex creates loop domains in DNA and polynucleosome arrays and can disrupt DNA-histone contacts within these domains. Mol Cell Biol 19: 1470-1478.
[56]	Nardulli AM,Grobner C,Cotter D (1995) Estrogen receptor-induced DNA bending: orientation of the bend and replacement of an estrogen response element with an intrinsic DNA bending sequence. Mol Endocrinol 9: 1064-1076.
[57]	Nardulli AM,Greene GL,Shapiro DJ (1993) Human estrogen receptor bound to an estrogen response element bends DNA. Mol Endocrinol 7: 331-340.
[58]	Cary PD,Moss T,Bradbury EM (1978) High-resolution proton-magnetic-resonance studies of chromatin core particles. Eur J Biochem 89: 475-482. doi: 10.1111/j.1432-1033.1978.tb12551.x
[59]	Perutz MF (1978) Hemoglobin structure and respiratory transport. Sci Am 239: 92-125.
[60]	Melvin VS,Roemer SC,Churchill ME,et al. (2002) The C-terminal extension (CTE) of the nuclear hormone receptor DNA binding domain determines interactions and functional response to the HMGB-1/-2 co-regulatory proteins. J Biol Chem 277: 25115-25124. doi: 10.1074/jbc.M110400200
[61]	Li Q,Wrange O (1993) Translational positioning of a nucleosomal glucocorticoid response element modulates glucocorticoid receptor affinity. Genes Dev 7: 2471-2482. doi: 10.1101/gad.7.12a.2471
[62]	Fletcher TM,Xiao N,Mautino G,et al. (2002) ATP-dependent mobilization of the glucocorticoid receptor during chromatin remodeling. Mol Cell Biol 22: 3255-3263. doi: 10.1128/MCB.22.10.3255-3263.2002
[63]	Walker P,Germond JE,Brown-Luedi M,et al. (1984) Sequence homologies in the region preceding the transcription initiation site of the liver estrogen-responsive vitellogenin and apo-VLDLII genes. Nucleic Acids Res 12: 8611-8626. doi: 10.1093/nar/12.22.8611
[64]	Reese JC,Katzenellenbogen BS (1991) Differential DNA-binding abilities of estrogen receptor occupied with two classes of antiestrogens: studies using human estrogen receptor overexpressed in mammalian cells. Nucleic Acids Res 19: 6595-6602. doi: 10.1093/nar/19.23.6595

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