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. 1994 May;14(5):3376–3391. doi: 10.1128/mcb.14.5.3376

The DNA-bending protein HMG-1 enhances progesterone receptor binding to its target DNA sequences.

S A Oñate 1, P Prendergast 1, J P Wagner 1, M Nissen 1, R Reeves 1, D E Pettijohn 1, D P Edwards 1
PMCID: PMC358703  PMID: 8164686

Abstract

Steroid hormone receptors are ligand-dependent transcriptional activators that exert their effects by binding as dimers to cis-acting DNA sequences termed hormone response elements. When human progesterone receptor (PR), expressed as a full-length protein in a baculovirus system, was purified to homogeneity, it retained its ability to bind hormonal ligand and to dimerize but exhibited a dramatic loss in DNA binding activity for specific progesterone response elements (PREs). Addition of nuclear extracts from several cellular sources restored DNA binding activity, suggesting that PR requires a ubiquitous accessory protein for efficient interaction with specific DNA sequences. Here we have demonstrated that the high-mobility-group chromatin protein HMG-1, as a highly purified protein, dramatically enhanced binding of purified PR to PREs in gel mobility shift assays. This effect appeared to be highly selective for HMG-1, since a number of other nonspecific proteins failed to enhance PRE binding. Moreover, HMG-1 was effective when added in stoichiometric amounts with receptor, and it was capable of enhancing the DNA binding of both the A and B amino-terminal variants of PR. The presence of HMG-1 measurably increased the binding affinity of purified PR by 10-fold when a synthetic palindromic PRE was the target DNA. The increase in binding affinity for a partial palindromic PRE present in natural target genes was greater than 10-fold. Coimmunoprecipitation assays using anti-PR or anti-HMG-1 antibodies demonstrated that both PR and HMG-1 are present in the enhanced complex with PRE. HMG-1 protein has two conserved DNA binding domains (A and B), which recognize DNA structure rather than specific sequences. The A- or B-box domain expressed and purified from Escherichia coli independently stimulated the binding of PR to PRE, and the B box was able to functionally substitute for HMG-1 in enhancing PR binding. DNA ligase-mediated ring closure assays demonstrated that both the A and B binding domains mediate DNA flexure. It was also demonstrated in competition binding studies that the intact HMG-1 protein binds to tightly curved covalently closed or relaxed DNA sequences in preference to the same sequence in linear form. The finding that enhanced PRE binding was intrinsic to the HMG-1 box, combined with the demonstration that HMG-1 or its DNA binding boxes can flex DNA, suggests that HMG-1 facilitates the binding of PR by inducing a structural change in the target DNA.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abate C., Patel L., Rauscher F. J., 3rd, Curran T. Redox regulation of fos and jun DNA-binding activity in vitro. Science. 1990 Sep 7;249(4973):1157–1161. doi: 10.1126/science.2118682. [DOI] [PubMed] [Google Scholar]
  2. Adachi Y., Mizuno S., Yoshida M. Efficient large-scale purification of non-histone chromosomal proteins HMG1 and HMG2 by using Polybuffer-exchanger PBE94. J Chromatogr. 1990 Aug 24;530(1):39–46. doi: 10.1016/s0378-4347(00)82300-2. [DOI] [PubMed] [Google Scholar]
  3. Bagchi M. K., Tsai S. Y., Tsai M. J., O'Malley B. W. Identification of a functional intermediate in receptor activation in progesterone-dependent cell-free transcription. Nature. 1990 Jun 7;345(6275):547–550. doi: 10.1038/345547a0. [DOI] [PubMed] [Google Scholar]
  4. Bannister A. J., Kouzarides T. Basic peptides enhance protein/DNA interaction in vitro. Nucleic Acids Res. 1992 Jul 11;20(13):3523–3523. doi: 10.1093/nar/20.13.3523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beebe J. S., Darling D. S., Chin W. W. 3,5,3'-triiodothyronine receptor auxiliary protein (TRAP) enhances receptor binding by interactions within the thyroid hormone response element. Mol Endocrinol. 1991 Jan;5(1):85–93. doi: 10.1210/mend-5-1-85. [DOI] [PubMed] [Google Scholar]
  6. Bianchi M. E., Falciola L., Ferrari S., Lilley D. M. The DNA binding site of HMG1 protein is composed of two similar segments (HMG boxes), both of which have counterparts in other eukaryotic regulatory proteins. EMBO J. 1992 Mar;11(3):1055–1063. doi: 10.1002/j.1460-2075.1992.tb05144.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Broyles S. S., Pettijohn D. E. Interaction of the Escherichia coli HU protein with DNA. Evidence for formation of nucleosome-like structures with altered DNA helical pitch. J Mol Biol. 1986 Jan 5;187(1):47–60. doi: 10.1016/0022-2836(86)90405-5. [DOI] [PubMed] [Google Scholar]
  8. Bruhn S. L., Pil P. M., Essigmann J. M., Housman D. E., Lippard S. J. Isolation and characterization of human cDNA clones encoding a high mobility group box protein that recognizes structural distortions to DNA caused by binding of the anticancer agent cisplatin. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2307–2311. doi: 10.1073/pnas.89.6.2307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Burnside J., Darling D. S., Chin W. W. A nuclear factor that enhances binding of thyroid hormone receptors to thyroid hormone response elements. J Biol Chem. 1990 Feb 15;265(5):2500–2504. [PubMed] [Google Scholar]
  10. Bustin M., Lehn D. A., Landsman D. Structural features of the HMG chromosomal proteins and their genes. Biochim Biophys Acta. 1990 Jul 30;1049(3):231–243. doi: 10.1016/0167-4781(90)90092-g. [DOI] [PubMed] [Google Scholar]
  11. Cavanaugh A. H., Simons S. S., Jr Glucocorticoid receptor binding to calf thymus DNA. 1. Identification and characterization of a macromolecular factor involved in receptor-steroid complex binding to DNA. Biochemistry. 1990 Jan 30;29(4):989–996. doi: 10.1021/bi00456a022. [DOI] [PubMed] [Google Scholar]
  12. Christensen K., Estes P. A., Oñate S. A., Beck C. A., DeMarzo A., Altmann M., Lieberman B. A., St John J., Nordeen S. K., Edwards D. P. Characterization and functional properties of the A and B forms of human progesterone receptors synthesized in a baculovirus system. Mol Endocrinol. 1991 Nov;5(11):1755–1770. doi: 10.1210/mend-5-11-1755. [DOI] [PubMed] [Google Scholar]
  13. Darling D. S., Beebe J. S., Burnside J., Winslow E. R., Chin W. W. 3,5,3'-triiodothyronine (T3) receptor-auxiliary protein (TRAP) binds DNA and forms heterodimers with the T3 receptor. Mol Endocrinol. 1991 Jan;5(1):73–84. doi: 10.1210/mend-5-1-73. [DOI] [PubMed] [Google Scholar]
  14. DeMarzo A. M., Oñate S. A., Nordeen S. K., Edwards D. P. Effects of the steroid antagonist RU486 on dimerization of the human progesterone receptor. Biochemistry. 1992 Nov 3;31(43):10491–10501. doi: 10.1021/bi00158a012. [DOI] [PubMed] [Google Scholar]
  15. Drouin J., Sun Y. L., Tremblay S., Lavender P., Schmidt T. J., de Léan A., Nemer M. Homodimer formation is rate-limiting for high affinity DNA binding by glucocorticoid receptor. Mol Endocrinol. 1992 Aug;6(8):1299–1309. doi: 10.1210/mend.6.8.1406707. [DOI] [PubMed] [Google Scholar]
  16. Durand B., Saunders M., Leroy P., Leid M., Chambon P. All-trans and 9-cis retinoic acid induction of CRABPII transcription is mediated by RAR-RXR heterodimers bound to DR1 and DR2 repeated motifs. Cell. 1992 Oct 2;71(1):73–85. doi: 10.1016/0092-8674(92)90267-g. [DOI] [PubMed] [Google Scholar]
  17. Edwards D. P., Kühnel B., Estes P. A., Nordeen S. K. Human progesterone receptor binding to mouse mammary tumor virus deoxyribonucleic acid: dependence on hormone and nonreceptor nuclear factor(s). Mol Endocrinol. 1989 Feb;3(2):381–391. doi: 10.1210/mend-3-2-381. [DOI] [PubMed] [Google Scholar]
  18. Einck L., Bustin M. The intracellular distribution and function of the high mobility group chromosomal proteins. Exp Cell Res. 1985 Feb;156(2):295–310. doi: 10.1016/0014-4827(85)90539-7. [DOI] [PubMed] [Google Scholar]
  19. Estes P. A., Suba E. J., Lawler-Heavner J., Elashry-Stowers D., Wei L. L., Toft D. O., Sullivan W. P., Horwitz K. B., Edwards D. P. Immunologic analysis of human breast cancer progesterone receptors. 1. Immunoaffinity purification of transformed receptors and production of monoclonal antibodies. Biochemistry. 1987 Sep 22;26(19):6250–6262. doi: 10.1021/bi00393a045. [DOI] [PubMed] [Google Scholar]
  20. Fawell S. E., Lees J. A., White R., Parker M. G. Characterization and colocalization of steroid binding and dimerization activities in the mouse estrogen receptor. Cell. 1990 Mar 23;60(6):953–962. doi: 10.1016/0092-8674(90)90343-d. [DOI] [PubMed] [Google Scholar]
  21. Feavers I. M., Jiricny J., Moncharmont B., Saluz H. P., Jost J. P. Interaction of two nonhistone proteins with the estradiol response element of the avian vitellogenin gene modulates the binding of estradiol-receptor complex. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7453–7457. doi: 10.1073/pnas.84.21.7453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ferrari S., Harley V. R., Pontiggia A., Goodfellow P. N., Lovell-Badge R., Bianchi M. E. SRY, like HMG1, recognizes sharp angles in DNA. EMBO J. 1992 Dec;11(12):4497–4506. doi: 10.1002/j.1460-2075.1992.tb05551.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Flashner Y., Gralla J. D. DNA dynamic flexibility and protein recognition: differential stimulation by bacterial histone-like protein HU. Cell. 1988 Aug 26;54(5):713–721. doi: 10.1016/s0092-8674(88)80016-3. [DOI] [PubMed] [Google Scholar]
  24. Fried M. G. Measurement of protein-DNA interaction parameters by electrophoresis mobility shift assay. Electrophoresis. 1989 May-Jun;10(5-6):366–376. doi: 10.1002/elps.1150100515. [DOI] [PubMed] [Google Scholar]
  25. Giese K., Cox J., Grosschedl R. The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell. 1992 Apr 3;69(1):185–195. doi: 10.1016/0092-8674(92)90129-z. [DOI] [PubMed] [Google Scholar]
  26. Glass C. K., Lipkin S. M., Devary O. V., Rosenfeld M. G. Positive and negative regulation of gene transcription by a retinoic acid-thyroid hormone receptor heterodimer. Cell. 1989 Nov 17;59(4):697–708. doi: 10.1016/0092-8674(89)90016-0. [DOI] [PubMed] [Google Scholar]
  27. Granelli-Piperno A., McHugh P. Characterization of a protein that regulates the DNA-binding activity of NF-AT, the nuclear factor of activated T cells. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11431–11434. doi: 10.1073/pnas.88.24.11431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Grueneberg D. A., Natesan S., Alexandre C., Gilman M. Z. Human and Drosophila homeodomain proteins that enhance the DNA-binding activity of serum response factor. Science. 1992 Aug 21;257(5073):1089–1095. doi: 10.1126/science.257.5073.1089. [DOI] [PubMed] [Google Scholar]
  29. Ha I., Lane W. S., Reinberg D. Cloning of a human gene encoding the general transcription initiation factor IIB. Nature. 1991 Aug 22;352(6337):689–695. doi: 10.1038/352689a0. [DOI] [PubMed] [Google Scholar]
  30. Heyman R. A., Mangelsdorf D. J., Dyck J. A., Stein R. B., Eichele G., Evans R. M., Thaller C. 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell. 1992 Jan 24;68(2):397–406. doi: 10.1016/0092-8674(92)90479-v. [DOI] [PubMed] [Google Scholar]
  31. Hodges-Garcia Y., Hagerman P. J., Pettijohn D. E. DNA ring closure mediated by protein HU. J Biol Chem. 1989 Sep 5;264(25):14621–14623. [PubMed] [Google Scholar]
  32. Ing N. H., Beekman J. M., Tsai S. Y., Tsai M. J., O'Malley B. W. Members of the steroid hormone receptor superfamily interact with TFIIB (S300-II). J Biol Chem. 1992 Sep 5;267(25):17617–17623. [PubMed] [Google Scholar]
  33. Kahn J. D., Crothers D. M. Protein-induced bending and DNA cyclization. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6343–6347. doi: 10.1073/pnas.89.14.6343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kastner P., Krust A., Turcotte B., Stropp U., Tora L., Gronemeyer H., Chambon P. Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J. 1990 May;9(5):1603–1614. doi: 10.1002/j.1460-2075.1990.tb08280.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. King I. N., de Soyza T., Catanzaro D. F., Lavin T. N. Thyroid hormone receptor-induced bending of specific DNA sequences is modified by an accessory factor. J Biol Chem. 1993 Jan 5;268(1):495–501. [PubMed] [Google Scholar]
  36. Kliewer S. A., Umesono K., Heyman R. A., Mangelsdorf D. J., Dyck J. A., Evans R. M. Retinoid X receptor-COUP-TF interactions modulate retinoic acid signaling. Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1448–1452. doi: 10.1073/pnas.89.4.1448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kliewer S. A., Umesono K., Mangelsdorf D. J., Evans R. M. Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signalling. Nature. 1992 Jan 30;355(6359):446–449. doi: 10.1038/355446a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kliewer S. A., Umesono K., Noonan D. J., Heyman R. A., Evans R. M. Convergence of 9-cis retinoic acid and peroxisome proliferator signalling pathways through heterodimer formation of their receptors. Nature. 1992 Aug 27;358(6389):771–774. doi: 10.1038/358771a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kumar V., Chambon P. The estrogen receptor binds tightly to its responsive element as a ligand-induced homodimer. Cell. 1988 Oct 7;55(1):145–156. doi: 10.1016/0092-8674(88)90017-7. [DOI] [PubMed] [Google Scholar]
  40. Kupfer S. R., Marschke K. B., Wilson E. M., French F. S. Receptor accessory factor enhances specific DNA binding of androgen and glucocorticoid receptors. J Biol Chem. 1993 Aug 15;268(23):17519–17527. [PubMed] [Google Scholar]
  41. Lannigan D. A., Notides A. C. Estrogen receptor selectively binds the "coding strand" of an estrogen responsive element. Proc Natl Acad Sci U S A. 1989 Feb;86(3):863–867. doi: 10.1073/pnas.86.3.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Leid M., Kastner P., Lyons R., Nakshatri H., Saunders M., Zacharewski T., Chen J. Y., Staub A., Garnier J. M., Mader S. Purification, cloning, and RXR identity of the HeLa cell factor with which RAR or TR heterodimerizes to bind target sequences efficiently. Cell. 1992 Jan 24;68(2):377–395. doi: 10.1016/0092-8674(92)90478-u. [DOI] [PubMed] [Google Scholar]
  43. Lenardo M. J., Kuang A., Gifford A., Baltimore D. NF-kappa B protein purification from bovine spleen: nucleotide stimulation and binding site specificity. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8825–8829. doi: 10.1073/pnas.85.23.8825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Lesser D. R., Kurpiewski M. R., Waters T., Connolly B. A., Jen-Jacobson L. Facilitated distortion of the DNA site enhances EcoRI endonuclease-DNA recognition. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7548–7552. doi: 10.1073/pnas.90.16.7548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Liao J., Ozono K., Sone T., McDonnell D. P., Pike J. W. Vitamin D receptor interaction with specific DNA requires a nuclear protein and 1,25-dihydroxyvitamin D3. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9751–9755. doi: 10.1073/pnas.87.24.9751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Makiguchi K., Chida Y., Yoshida M., Shimura K. Mg2+-dependent unwinding of DNA by nonhistone chromosomal protein HMG(1 + 2) from pig thymus as determined by DNA melting temperature analysis. J Biochem. 1984 Feb;95(2):423–429. doi: 10.1093/oxfordjournals.jbchem.a134623. [DOI] [PubMed] [Google Scholar]
  47. Mukherjee R., Chambon P. A single-stranded DNA-binding protein promotes the binding of the purified oestrogen receptor to its responsive element. Nucleic Acids Res. 1990 Oct 11;18(19):5713–5716. doi: 10.1093/nar/18.19.5713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Mukherjee R. Selective binding of the estrogen receptor to one strand of the estrogen responsive element. Nucleic Acids Res. 1993 Jun 11;21(11):2655–2661. doi: 10.1093/nar/21.11.2655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Murray M. B., Towle H. C. Identification of nuclear factors that enhance binding of the thyroid hormone receptor to a thyroid hormone response element. Mol Endocrinol. 1989 Sep;3(9):1434–1442. doi: 10.1210/mend-3-9-1434. [DOI] [PubMed] [Google Scholar]
  50. Nakajima N., Horikoshi M., Roeder R. G. Factors involved in specific transcription by mammalian RNA polymerase II: purification, genetic specificity, and TATA box-promoter interactions of TFIID. Mol Cell Biol. 1988 Oct;8(10):4028–4040. doi: 10.1128/mcb.8.10.4028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Nardulli A. M., Greene G. L., Shapiro D. J. Human estrogen receptor bound to an estrogen response element bends DNA. Mol Endocrinol. 1993 Mar;7(3):331–340. doi: 10.1210/mend.7.3.8483477. [DOI] [PubMed] [Google Scholar]
  52. Nardulli A. M., Shapiro D. J. Binding of the estrogen receptor DNA-binding domain to the estrogen response element induces DNA bending. Mol Cell Biol. 1992 May;12(5):2037–2042. doi: 10.1128/mcb.12.5.2037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Okamoto K., Isohashi F., Ueda K., Kokufu I., Sakamoto Y. Purification and characterization of an adenosine triphosphate-stimulated factor that enhances the nuclear binding of activated glucocorticoid-receptor complex from rat liver. Endocrinology. 1988 Dec;123(6):2752–2761. doi: 10.1210/endo-123-6-2752. [DOI] [PubMed] [Google Scholar]
  54. Oñate S. A., Estes P. A., Welch W. J., Nordeen S. K., Edwards D. P. Evidence that heat shock protein-70 associated with progesterone receptors is not involved in receptor-DNA binding. Mol Endocrinol. 1991 Dec;5(12):1993–2004. doi: 10.1210/mend-5-12-1993. [DOI] [PubMed] [Google Scholar]
  55. Paull T. T., Haykinson M. J., Johnson R. C. The nonspecific DNA-binding and -bending proteins HMG1 and HMG2 promote the assembly of complex nucleoprotein structures. Genes Dev. 1993 Aug;7(8):1521–1534. doi: 10.1101/gad.7.8.1521. [DOI] [PubMed] [Google Scholar]
  56. Pettijohn D. E. Histone-like proteins and bacterial chromosome structure. J Biol Chem. 1988 Sep 15;263(26):12793–12796. [PubMed] [Google Scholar]
  57. Pil P. M., Chow C. S., Lippard S. J. High-mobility-group 1 protein mediates DNA bending as determined by ring closures. Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9465–9469. doi: 10.1073/pnas.90.20.9465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Pil P. M., Lippard S. J. Specific binding of chromosomal protein HMG1 to DNA damaged by the anticancer drug cisplatin. Science. 1992 Apr 10;256(5054):234–237. doi: 10.1126/science.1566071. [DOI] [PubMed] [Google Scholar]
  59. Rodriguez R., Weigel N. L., O'Malley B. W., Schrader W. T. Dimerization of the chicken progesterone receptor in vitro can occur in the absence of hormone and DNA. Mol Endocrinol. 1990 Dec;4(12):1782–1790. doi: 10.1210/mend-4-12-1782. [DOI] [PubMed] [Google Scholar]
  60. Ross T. K., Moss V. E., Prahl J. M., DeLuca H. F. A nuclear protein essential for binding of rat 1,25-dihydroxyvitamin D3 receptor to its response elements. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):256–260. doi: 10.1073/pnas.89.1.256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Smith D. F., Toft D. O. Steroid receptors and their associated proteins. Mol Endocrinol. 1993 Jan;7(1):4–11. doi: 10.1210/mend.7.1.8446107. [DOI] [PubMed] [Google Scholar]
  62. Sone T., Ozono K., Pike J. W. A 55-kilodalton accessory factor facilitates vitamin D receptor DNA binding. Mol Endocrinol. 1991 Nov;5(11):1578–1586. doi: 10.1210/mend-5-11-1578. [DOI] [PubMed] [Google Scholar]
  63. Spiro C., Richards J. P., Chandrasekaran S., Brennan R. G., McMurray C. T. Secondary structure creates mismatched base pairs required for high-affinity binding of cAMP response element-binding protein to the human enkephalin enhancer. Proc Natl Acad Sci U S A. 1993 May 15;90(10):4606–4610. doi: 10.1073/pnas.90.10.4606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Taylor W. H., Hagerman P. J. Application of the method of phage T4 DNA ligase-catalyzed ring-closure to the study of DNA structure. II. NaCl-dependence of DNA flexibility and helical repeat. J Mol Biol. 1990 Mar 20;212(2):363–376. doi: 10.1016/0022-2836(90)90131-5. [DOI] [PubMed] [Google Scholar]
  65. Thanos D., Maniatis T. The high mobility group protein HMG I(Y) is required for NF-kappa B-dependent virus induction of the human IFN-beta gene. Cell. 1992 Nov 27;71(5):777–789. doi: 10.1016/0092-8674(92)90554-p. [DOI] [PubMed] [Google Scholar]
  66. Toledano M. B., Leonard W. J. Modulation of transcription factor NF-kappa B binding activity by oxidation-reduction in vitro. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4328–4332. doi: 10.1073/pnas.88.10.4328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Travers A. A. DNA conformation and protein binding. Annu Rev Biochem. 1989;58:427–452. doi: 10.1146/annurev.bi.58.070189.002235. [DOI] [PubMed] [Google Scholar]
  68. Truss M., Beato M. Steroid hormone receptors: interaction with deoxyribonucleic acid and transcription factors. Endocr Rev. 1993 Aug;14(4):459–479. doi: 10.1210/edrv-14-4-459. [DOI] [PubMed] [Google Scholar]
  69. Umesono K., Murakami K. K., Thompson C. C., Evans R. M. Direct repeats as selective response elements for the thyroid hormone, retinoic acid, and vitamin D3 receptors. Cell. 1991 Jun 28;65(7):1255–1266. doi: 10.1016/0092-8674(91)90020-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Wagner S., Green M. R. HTLV-I Tax protein stimulation of DNA binding of bZIP proteins by enhancing dimerization. Science. 1993 Oct 15;262(5132):395–399. doi: 10.1126/science.8211160. [DOI] [PubMed] [Google Scholar]
  71. Wahlström G. M., Sjöberg M., Andersson M., Nordström K., Vennström B. Binding characteristics of the thyroid hormone receptor homo- and heterodimers to consensus AGGTCA repeat motifs. Mol Endocrinol. 1992 Jul;6(7):1013–1022. doi: 10.1210/mend.6.7.1324417. [DOI] [PubMed] [Google Scholar]
  72. Weir H. M., Kraulis P. J., Hill C. S., Raine A. R., Laue E. D., Thomas J. O. Structure of the HMG box motif in the B-domain of HMG1. EMBO J. 1993 Apr;12(4):1311–1319. doi: 10.1002/j.1460-2075.1993.tb05776.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Xanthoudakis S., Miao G., Wang F., Pan Y. C., Curran T. Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO J. 1992 Sep;11(9):3323–3335. doi: 10.1002/j.1460-2075.1992.tb05411.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Yang N., Schüle R., Mangelsdorf D. J., Evans R. M. Characterization of DNA binding and retinoic acid binding properties of retinoic acid receptor. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3559–3563. doi: 10.1073/pnas.88.9.3559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Yoshida M., Shimura K. Unwinding of DNA by nonhistone chromosomal protein HMG(1 + 2) from pig thymus as determined with endonuclease. J Biochem. 1984 Jan;95(1):117–124. doi: 10.1093/oxfordjournals.jbchem.a134573. [DOI] [PubMed] [Google Scholar]
  76. Yu V. C., Delsert C., Andersen B., Holloway J. M., Devary O. V., När A. M., Kim S. Y., Boutin J. M., Glass C. K., Rosenfeld M. G. RXR beta: a coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements. Cell. 1991 Dec 20;67(6):1251–1266. doi: 10.1016/0092-8674(91)90301-e. [DOI] [PubMed] [Google Scholar]
  77. Zhang X. K., Hoffmann B., Tran P. B., Graupner G., Pfahl M. Retinoid X receptor is an auxiliary protein for thyroid hormone and retinoic acid receptors. Nature. 1992 Jan 30;355(6359):441–446. doi: 10.1038/355441a0. [DOI] [PubMed] [Google Scholar]
  78. Zhang X. Y., Asiedu C. K., Supakar P. C., Ehrlich M. Increasing the activity of affinity-purified DNA-binding proteins by adding high concentrations of nonspecific proteins. Anal Biochem. 1992 Mar;201(2):366–374. doi: 10.1016/0003-2697(92)90353-9. [DOI] [PubMed] [Google Scholar]

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