Mechanism of high-mobility group protein B enhancement of progesterone receptor sequence-specific DNA binding

Nucleic Acids Research

Volumn 36, Issue 11, 2008, Pages 3655-3666

  Roemer, Sarah C ^a   Adelman, James ^a   Churchill, Mair E A ^a   Edwards, Dean P ^b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; DNA; HIGH MOBILITY GROUP B PROTEIN; PROGESTERONE RECEPTOR; THYMINE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN COS1; CONTROLLED STUDY; DNA BINDING; DNA FLANKING REGION; DNA RESPONSIVE ELEMENT; DNA STRUCTURE; GENE SEQUENCE; IN VITRO STUDY; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING;

ADENINE; ANIMALS; BASE SEQUENCE; BINDING SITES; CERCOPITHECUS AETHIOPS; COS CELLS; DNA; HMGB PROTEINS; PEPTIDES; PROTEIN BINDING; RECEPTORS, PROGESTERONE; RESPONSE ELEMENTS; THYMINE;

EID: 46349086564     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn249     Document Type: Article

References (75)

1. Beato,M. and Klug,J. (2000) Steroid hormone receptors: An update. Hum. Reprod. Update, 6, 225-236.
2. Evans,R.M. (1988) The steroid and thyroid hormone receptor superfamily. Science, 240, 889-895.
3. Khorasanizadeh,S. and Rastinejad,F. (2001) Nuclear-receptor interactions on DNA-response elements. Trends Biochem. Sci., 26, 384-390.
4. Mangelsdorf,D.J., Thummel,C., Beato,M., Herrlich,P., Schutz,G., Umesono,K., Blumberg,B, Kastner,P., Mark,M., Charnbon,P. et al. (1995) The nuclear receptor superfamily: The second decade, Cell, 83, 835-839.
5. Gearhart,M.D., Holmbeck,S.M., Evans,R.M., Dyson,H.J. and Wright,P.E. (2003) Monomeric complex of human orphan estrogen related receptor-2 with DNA: A pseudo-dimer interface mediates extended half-site recognition. J. Mol. Biol., 327, 819-832.
6. Lee,M.S., Kliewer,S.A., Provencal,J., Wright,P.E. and Evans,R.M. (1993) Structure of the retinoid X receptor alpha DNA binding domain: A helix required for homodimeric DNA binding. Science, 260, 1117-1121.
7. Meinke,G. and Sigler,P.B. (1999) DNA-binding mechanism of. the monomeric orphan nuclear receptor NGFI-B. Nat. Struct. Biol., 6, 471-477.
8. Rastinejad,F., Perlmann,T., Evans,R.M. and Sigler,P.B. (1995) Structural determinants of nuclear receptor assembly on DNA direct repeats. Nature, 375, 203-211.
9. Rastinejad,F., Wagner,T., Zhao,Q. and Khorasanizadeh,S. (2000) Structure of the RXR-RAR DNA-binding complex on the retinoic acid response element DR1. EMBO J., 19, 1045-1054.
10. Sem,D.S., Casimiro,D.R., Kliewer,S.A., Provencal,J., Evans,R.M. and Wright,P.E. (1997) NMR spectroscopic studies of the DNA-binding domain of the monomer-binding nuclear orphan receptor, human estrogen related receptor-2. The carboxyl-terminal extension to the zinc-finger region is unstructured in the free form of the protein. J. Biol. Chem., 272, 18038-18043.
11. Shaffer,P.L. and Gewirth,D.T. (2002) Structural basis of VDR-DNA interactions on direct lepeat response elements. EMBO J., 21 2242-2252.
12. Solomon,I.H., Hager,J.M., Safi,R., McDonnell,D.P., Redinbo,M.R. and Ortlund,E.A. (2005) Crystal structure of the human LRH-1 DBD-DNA complex reveals Ftz-F1 domain positioning is required for receptor activity. J. Mol. Biol., 354, 1091-1102.
13. Wilson,T.E., Paulsen,R.E., Padgett,K.A. and Milbrandt,J, (1992) Participation of non-zinc finger residues in DNA binding by two nuclear orphan receptors. Science, 256, 107-110.
14. Zechel,C., Shen,X. Q., Chambon,P. and Gronemeyer,H. (1994) Dimerization interfaces formed between the DNA binding domains determine the cooperative binding of RXR/RAR and RXR/TR heterodimers to DR5 and DR4 elements. EMBO J., 13, 1414-1424.
15. Zhao,Q., Chasse,S.A., Devarakonda,S., Sierk,M.L., Ahvazi,B. and Rastinejad,F. (2000) Structural basis of RXR-DNA interactions. J. Mol. Biol., 296, 509-520.
16. Zhao,Q., Khorasanizadeh,S., Miyoshi,Y., Lazar,M.A. and Rastinejad,F. (1998) Structural elements of an orphan nuclear receptor-DNA complex: Mol Cell, 1, 849-861.
17. Wilson,T.E., Fahrner,T.J. and Milbrandt,J. (1993) The orphan receptors NGFI-B and-steroidogenic factor 1 establish monomer binding as a third paradigm of nuclear receptor-DNA interaction. Mol. Cell. Biol., 13, 5794-5804.
18. Hsieh,J.C., Jurutka,P.W., Selznick,S.M., Reeder,M.C. Haussler,C.A., Whitfield,G.K. and Haussler,M.R. (1995) The T-box near the zinc fingers or the human vitamin receptor is required for heterodimeric DNA blinding and transactivation, Biochem. Biophys. Res. Commun., 215, 1-7.
19. Hsieh,J.C., Whitfield,G.K., Oza,A.K., Dang,H.T., Price,J.N., Galligan,M.A., Jurutka,P.W., Thompson,P.D., Haussler,C.A. and Haussler,M.R. (1999) Characterization of unique DNA-binding and transcriptional-activation functions in the carboxyl-terminal extension of the zinc finger region in the human vitamin D receptor. Biochemistry, 38, 16347-16358.
20. Quack,M., Szafranski,K., Rouvinen,J. and Carlberg,C. (1998) The role of the T-box for the function of the vitamin D receptor on different types of response elements. Nucleic Acids Res., 26, 5372-5378.
21. Giguere,V., Tini,M., Flock,G., Ong,E., Evans,R.M. and Otulakowski,G. (1994) Isoform-specific amino-terminal domains dictate DNA-binding properties of ROR alpha, a novel family of orphan hormone nuclear receptors. Genes Dev., 8, 538-553.
22. Yan,Z.H., Medvedev,A., Hirose,T., Gotoh,H. and Jetten,A.M. (1997) Characterization of the response element and DNA binding properties of the nuclear orphan receptor germ cell nuclear factor/retinoid receptor-related testis-associated receptor. J. Biol. Chem., 272, 10565-10572.
23. Roemer,S.C., Donham,D.C., Sherman,L., Pon,V.H., Edwards,D.P. and Churchill,M.E. (2006) Structure of the progesterone receptor-deoxyribonucleic acid complex: Novel interactions required for binding to half-site response elements. Mol. Endocrinol., 20 3042-3052.
24. Mclvin,V.S., Harrell,C., Adelman,J.S., Kraus,W.L., Churchill,M. and Edwards,D.P. (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.
25. Melvin,V.S., Roemer,S.C., Churchill,M.E. and Edwards,D.P. (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.
26. Kim,M.Y., Woo,E.M., Chong,Y.T., Homenko,D.R. and Kraus,W.L. (2006) Acetylation of estrogen receptor alpha by p300 at lysines 266 and 268 enhances the deoxyribonucleic acid binding and transactivation activities of the receptor. Mol. Endocrinol., 20, 1479-1493.
27. Murphy,F.V.T. and Churchill,M.E. (2000) Nonsequence-specific DNA recognition: A structural perspective. Struct. Fold Des., 8, R83-R89.
28. Murphy,F.V.T., Sweet,R.M. and Churchill,M.E. (1999) The structure of a chromosomal high mobility group prptein-DNA complex reveals sequence-neutral mechanisms important for non-sequence-specific DNA recognition. EMBO J., 18, 6610-6618.
29. Stros,M., Cherny,D. and Jovin,T.M. (2000) HMG1 protein stimulates DNA end joining by promoting association of DNA molecules via their ends. Eur. J. Biochem., 267, 4088-4097.
30. Thomas,J.O. and Travers,A.A. (2001) HMG1 and 2, and 4 related 'architectural' DNA-binding proteins. Trends Biochem. Sci., 26 167-174.
31. Travers,A. (2000) Recognition of distorted DNA structures by HMG domains. Curr. Opin. Struct. Biol., 10, 102-109.
32. Krynetski,E.Y., Krynetskaia,N.F., Bianchi,M.E. and Evans,W.E. (2003) A nuclear protein complex containing high mobility group proteins B1 and B2, heat shock cognate protein 70, ERp60, and glyceraldehyde-3-phosphate dehydrogenase is involved in the cytotoxic response to DNA modified by incorporation of anticancer nucleoside analogues. Cancer Res., 63, 100-106.
33. Nagatani,G., Nomoto,M., Takano,H., Ise,T., Kato,K., Imamura,T., Izumi,H., Makishima,K. and Kohno, (2001) Transcriptional activation of the human HMG1 gene in cisplatin-resistant human cancer cells. Cancer Res., 61, 1592-1597.
34. Okuhara,K., Ohta,K., Seo,H., Shioda,M., Yamada,T., Tanaka,Y., Dohmae,N., Seyama,Y., Shibata,T. and Murofushi,H. (1999) A DNA unwinding factor involved in DNA replication in cell-free extracts of Xenopus eggs. Curr. Biol., 9, 341-350.
35. Ellwood,K.B., Yen,Y.M., Johnson,R.C. and Carey,M. (2000) Mechanism for specificity by HMG-1 in enhanceosome assembly. Mol. Cell. Biol., 20, 4359-4370.
36. Mitsouras,K., Wong,B., Arayata,C., Johnson,R.C. and Carey,M. (2002) The DNA architectural protein HMGB1 displays two distinct modes of action that promote enhanceosome assembly. Mol. Cell. Biol., 22, 4390-4401.
37. Bonaldi,T., Langst,G., Strohner,R., Becker,P.B. and Bianchi,M.E. (2002) The DNA chaperone HMGB1 facilitates ACFJ/CHRAC-dependent nucleosome sliding. EMBO J., 21, 6865-6873.
38. Boonyaratanakornkit,V., Melvin,V., Prendergast,P., Altmann,M., Ronfani,L., Bianchi,M.E., Taraseviciene,L., Nordeen,S.K., Allegretto,E.A. and Edwards,D.P. (1998) High-mobility group chromatin proteitis 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.
39. Das,D., Peterson,R.C. and Scovell,W.M. (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.
40. Romine,L.E., Wood,J.R., Lamia,L.A., Prendergast,P., Edwards,D.P. and Nardulli,A.M. (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.
41. Verrier,C.S., Roodi,N., Yee,C.J., Bailey,L.R., Jensen,R.A., Bustin,M. and Parl,F.F. (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.
42. Verrijdt,G., Haelens,A., Schoenmakers,E., Rombauts,W. and Claessens,F. (2002) Comparative analysis of the influence of the high-mobility group box 1 protein on DNA binding and transcriptional activation by the androgen, glucocorticoid, progesterone and mineralocorticoid receptors. Biochem. J., 361, 97-103.
43. Zhang,C.C., Krieg,S. and Shapiro,D.J. (1999) HMG-1 stimulates estrogen response element binding by estrogen receptor from stably transfected HeLa cells. Mol. Endocrinol., 13, 632-643.
44. Calogero,S., Grassi,F., Aguzzi,A., Voigtlander,T., Ferrier,P., Ferrari,S. and Bianchi,M.E. (1999) The lack of chromosomal protein Hmg1 does not disrupt cell growth but causes lethal hypoglycaemia in newborn mice. Nat. Genet., 22, 276-280.
45. Agresti,A., Scaffidi,P., Riva,A., Caiolfa,V.R. and Bianchi,M.E. (2005) GR and HMGB1 interact only within chromatin and influence each other's residence time. Mol. Cell, 18, 109-121.
46. Zappavigna,V., Falciola,L., Helmer-Citterich,M., Mavilio,F. and Bianchi,M.E. (1996) HMG1 interacts with HOX proteins and enhances their DNA binding and transcriptional activation. EMBO J., 15, 4981-4991.
47. Butteroni,C., De Felici,M., Scholer,H.R. and Pesce,M. (2000) Phage display screening reveals an association between germline-specific transcription factor Oct-4 and multiple cellular proteins. J. Mol. Biol., 304, 529-540.
48. Zwilling,S., Konig,H. and Wirth,T. (1995) High mobility group protein 2 functionally interacts with the POU domains of octamer transcription factors. EMBO J., 14, 1198-1208.
49. Agresti,A., Lupo,R., Bianchi,M.E. and Muller,S. (2003) HMGB1 interacts differentially with members of the Rel family of transcription factors. Biochem. Biophys. Res. Commun., 302, 421-426.-
50. McKinney,K. and Prives,C. (2002) Efficient specific DNA binding by p53 requires both its central and C-terminal domains as revealed by studies with high-mobility group 1 protein. Mol. Cell. Biol., 22, 6797-6808.
51. Jayaraman,L., Moorthy,N.C., Murthy,K.G., Manley,J.L., Bustin,M. and Prives,C. (1998) High mobility group protein-1 (HMG-1) is a unique activator of p53. Genes Dev., 12, 462-472.
52. Stros,M., Ozaki,T., Bacikova,A., Kageyama,H. and Nakagawara,A. (2001) HMGB1 and HMGB2 cell-specifically down-regulate the p53- and p73-dependent sequence-specific transactivation from the human Bax gene promoter. J. Biol. Chem., 277, 7157-17164.
53. Naghavi,M.H., Nowak,P., Andersson,J., Sonnerborg,A., Yang,H., Tracey,K.J. and Vahlne,A. (2003) Intracellular high mobility group B1 Protein (HMGB1) represses HIV-1 LTR-directed tran- scription in a promoter- and cell-specific manner. Virology, 314, 179-189.
54. Allgood,V.E., Zhang,Y., O'Malley,B.W. and Weigel,N.L. (1997) Analysis of chicken progesterone receptor function and phosphorylation using an adenovirus-mediated procedure for HIGH-efficiency DNA transfer. Biochemistry, 36, 224-232.
55. Pollock,R. and Treisman,R. (1990) A sensitive method for the determination of protein-DNA binding specificities. Nucleic Acids Res., 18, 6197-6204.
56. Maxam,A.M. and Gilbert,W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol., 65, 499-560.
57. Hertz,G.Z. and Stormo,G.D. (1999) Identifying DNA and protein patterns with statistically significant alignments of multiple sequences. Bioinformatics, 15, 563-577.
58. Crooks,G.E., Hon,G., Chandonia,J.M. and Brenner,S.E. (2004) WebLogo: A sequence logo generator. Genome Res., 14, 1188-1190.
59. Churchill,M.E., Changela,A., Dow,L.K. and Krieg,A.J. (1999) Interactions of high mobility group box proteins with DNA and chromatin. Methods Enzymol., 304, 99-133.
60. Boonyaratanakornkit,V., Scott,M.P., Ribon,V., Sherman,L., Anderson,S.M., Maller,J.L., Miller,W.T. and Edwards,D.P. (2001) Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-Src family tyrosine kinases. Mol. Cell, 8, 269-280.
61. Jones,D.N., Searles,M.A., Shaw,G.L., Churchill,M.E., Ner,S.S., Keeler,J., Travers,A.A. and Neuhaus,D. (1994) The solution structure and dynamics of the DNA-binding domain of HMG-D from Drosophila melanogaster. Structure, 2, 609-627.
62. Weir,H.M., Kraulis,P.J., Hill,C.S., Raine,A.R., Laue,E.D. and Thomas,J.O. (1993) Structure of the HMG box motif in the B-domain of HMG1. EMBO J., 12, 1311-1319.
63. Teo,S.H., Grasser,K.D. and Thomas,J.O. (1995) Differences in the DNA-binding properties of the HMG-box domains of HMG1 and the sex-determining factor SRY. Eur. J. Biochem., 230, 943-950.
64. Muller,S., Bianchi,M.E. and Knapp,S. (2001) Thermodynamics of HMGB1 interaction with duplex DNA. Biochemistry, 40, 10254-10261.
65. Klass,J., Murphy,F.V.T., Fouts,S., Serenil,M., Changela,A., Siple,J. and Churchill,M.E. (2003) The role of intercalating residues in chromosomal high-mobility-group protein DNA binding, bending and specificity. Nucleic Acids Res., 31, 2852-2864.
66. Stros,M. and Muselikova,E. (2000) A role of basic residues and the putative intercalating phenylalanine of the HMG-1 box B in DNA supercoiling and binding to four-way DNA junctions. J. Biol. Chem. 275, 35699-35707.
67. Shirakawa,H., Tanigawa,T., Sugiyama,S., Kobayashi,M., Terashima,T., Yoshida,K., Arai,T. and Yoshida,M. (1997) Nuclear accumulation of HMG2 protein is mediated by basic regions interspaced with a long DNA-binding sequence, and retention within the nucleus requires the acidic carboxyl terminus. Biochemistry, 36, 5992-5999.
68. Brown,J.W. and Anderson,J.A. (1986) The binding of the chromosomal protein HMG-2a to DNA regions of reduced stabilities. J. Biol. Chem. 261, 1349-1354.
69. Paull,T.T., Haykinson,M.J. and Johnson,R.C. (1993) The nonspecific DNA-binding and -bending proteins HMG1 and HMG2 promote the assembly of complex nucleoprotein structures. Genes Dev., 7, 1521-1534.
70. Churchill,M.E., Jones,D.N., Glaser,T., Hefner,H., Searles,M.A. and Travers,A.A. (1995) HMG-D is an architecture-specific protein that preferentially binds to DNA containing the dinucleotide T.G. EMBO J. 14, 1264-1275.
71. Thomas,J.O. (2001) HMG1 and 2: Architectural DNA-binding proteins. Biochem. Soc. Trans., 29, 395-401.
72. Taudte,S., Xin,H. and Kallenbach,N.R. (2000) Alanine mutagenesis of high-mobility-group-protein-1 box B (HMG1-B). Biochem. J., 347 (Pt 3), 807-814.
73. Langst,G. and Becker,P.B. (2004) Nucleosome remodeling: One mechanism, many phenomena? Biochimica et biophysica acta, 1677, 58-63.
74. Das,D. and Scovell,W.M. (2001) The binding interaction of HMG-1 with the TATA-binding protein/TATA complex. J. Biol. Chem., 276, 32597-32605.
75. Guermah,M., Palhan,V.B., Tackett,A.J., Chait,B.T. and Roeder,R.G. (2006) Synergistic functions of SII and p300 in productive activator-dependent transcription of chromatin templates. Cell, 125, 275-286.