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. 1996 Dec 1;24(23):4733–4740. doi: 10.1093/nar/24.23.4733

A novel activity of HMG domains: promotion of the triple-stranded complex formation between DNA containing (GGA/TCC)11 and d(GGA)11 oligonucleotides.

T Suda 1, Y Mishima 1, K Takayanagi 1, H Asakura 1, S Odani 1, R Kominami 1
PMCID: PMC146295  PMID: 8972860

Abstract

The high mobility group protein (HMG)-box is a DNA-binding domain found in many proteins that bind preferentially to DNA of irregular structures in a sequence-independent manner and can bend the DNA. We show here that GST-fusion proteins of HMG domains from HMG1 and HMG2 promote a triple-stranded complex formation between DNA containing the (GGA/TCC)11 repeat and oligonucleotides of d(GGA)11 probably due to G:G base pairing. The activity is to reduce association time and requirements of Mg2+ and oligonucleotide concentrations. The HMG box of SRY, the protein determining male-sex differentiation, also has the activity, suggesting that it is not restricted to the HMG-box domains derived from HMG1/2 but is common to those from other members of the HMG-box family of proteins. Interestingly, the box-AB and box-B of HMG1 bend DNA containing the repeat, but SRY fails to bend in a circularization assay. The difference suggests that the two activities of association-promotion and DNA bending are distinct. These results suggest that the HMG-box domain has a novel activity of promoting the association between GGA repeats which might be involved in higher-order architecture of chromatin.

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Selected References

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

  1. 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]
  2. Baxevanis A. D., Landsman D. The HMG-1 box protein family: classification and functional relationships. Nucleic Acids Res. 1995 May 11;23(9):1604–1613. doi: 10.1093/nar/23.9.1604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beal P. A., Dervan P. B. Second structural motif for recognition of DNA by oligonucleotide-directed triple-helix formation. Science. 1991 Mar 15;251(4999):1360–1363. doi: 10.1126/science.2003222. [DOI] [PubMed] [Google Scholar]
  4. Beckman J. S., Weber J. L. Survey of human and rat microsatellites. Genomics. 1992 Apr;12(4):627–631. doi: 10.1016/0888-7543(92)90285-z. [DOI] [PubMed] [Google Scholar]
  5. Bianchi M. E., Beltrame M., Paonessa G. Specific recognition of cruciform DNA by nuclear protein HMG1. Science. 1989 Feb 24;243(4894 Pt 1):1056–1059. doi: 10.1126/science.2922595. [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. Blackburn E. H. Structure and function of telomeres. Nature. 1991 Apr 18;350(6319):569–573. doi: 10.1038/350569a0. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Camerini-Otero R. D., Hsieh P. Parallel DNA triplexes, homologous recombination, and other homology-dependent DNA interactions. Cell. 1993 Apr 23;73(2):217–223. doi: 10.1016/0092-8674(93)90224-e. [DOI] [PubMed] [Google Scholar]
  10. Chase J. W., Williams K. R. Single-stranded DNA binding proteins required for DNA replication. Annu Rev Biochem. 1986;55:103–136. doi: 10.1146/annurev.bi.55.070186.000535. [DOI] [PubMed] [Google Scholar]
  11. Churchill M. E., Jones D. N., Glaser T., Hefner H., Searles M. A., Travers A. A. HMG-D is an architecture-specific protein that preferentially binds to DNA containing the dinucleotide TG. EMBO J. 1995 Mar 15;14(6):1264–1275. doi: 10.1002/j.1460-2075.1995.tb07110.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Falciola L., Murchie A. I., Lilley D. M., Bianchi M. Mutational analysis of the DNA binding domain A of chromosomal protein HMG1. Nucleic Acids Res. 1994 Feb 11;22(3):285–292. doi: 10.1093/nar/22.3.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Gaillard C., Strauss F. Association of poly(CA).poly(TG) DNA fragments into four-stranded complexes bound by HMG1 and 2. Science. 1994 Apr 15;264(5157):433–436. doi: 10.1126/science.8153633. [DOI] [PubMed] [Google Scholar]
  15. Ge H., Roeder R. G. The high mobility group protein HMG1 can reversibly inhibit class II gene transcription by interaction with the TATA-binding protein. J Biol Chem. 1994 Jun 24;269(25):17136–17140. [PubMed] [Google Scholar]
  16. 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]
  17. Grosschedl R., Giese K., Pagel J. HMG domain proteins: architectural elements in the assembly of nucleoprotein structures. Trends Genet. 1994 Mar;10(3):94–100. doi: 10.1016/0168-9525(94)90232-1. [DOI] [PubMed] [Google Scholar]
  18. Gubbay J., Collignon J., Koopman P., Capel B., Economou A., Münsterberg A., Vivian N., Goodfellow P., Lovell-Badge R. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature. 1990 Jul 19;346(6281):245–250. doi: 10.1038/346245a0. [DOI] [PubMed] [Google Scholar]
  19. Haqq C. M., King C. Y., Ukiyama E., Falsafi S., Haqq T. N., Donahoe P. K., Weiss M. A. Molecular basis of mammalian sexual determination: activation of Müllerian inhibiting substance gene expression by SRY. Science. 1994 Dec 2;266(5190):1494–1500. doi: 10.1126/science.7985018. [DOI] [PubMed] [Google Scholar]
  20. Hearne C. M., Ghosh S., Todd J. A. Microsatellites for linkage analysis of genetic traits. Trends Genet. 1992 Aug;8(8):288–294. doi: 10.1016/0168-9525(92)90256-4. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Hoffman-Liebermann B., Liebermann D., Troutt A., Kedes L. H., Cohen S. N. Human homologs of TU transposon sequences: polypurine/polypyrimidine sequence elements that can alter DNA conformation in vitro and in vivo. Mol Cell Biol. 1986 Nov;6(11):3632–3642. doi: 10.1128/mcb.6.11.3632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Htun H., Dahlberg J. E. Single strands, triple strands, and kinks in H-DNA. Science. 1988 Sep 30;241(4874):1791–1796. doi: 10.1126/science.3175620. [DOI] [PubMed] [Google Scholar]
  24. Jantzen H. M., Chow A. M., King D. S., Tjian R. Multiple domains of the RNA polymerase I activator hUBF interact with the TATA-binding protein complex hSL1 to mediate transcription. Genes Dev. 1992 Oct;6(10):1950–1963. doi: 10.1101/gad.6.10.1950. [DOI] [PubMed] [Google Scholar]
  25. Johnston B. H. The S1-sensitive form of d(C-T)n.d(A-G)n: chemical evidence for a three-stranded structure in plasmids. Science. 1988 Sep 30;241(4874):1800–1804. doi: 10.1126/science.2845572. [DOI] [PubMed] [Google Scholar]
  26. Kohwi-Shigematsu T., Kohwi Y. Poly(dG)-poly(dC) sequences, under torsional stress, induce an altered DNA conformation upon neighboring DNA sequences. Cell. 1985 Nov;43(1):199–206. doi: 10.1016/0092-8674(85)90024-8. [DOI] [PubMed] [Google Scholar]
  27. Laudet V., Stehelin D., Clevers H. Ancestry and diversity of the HMG box superfamily. Nucleic Acids Res. 1993 May 25;21(10):2493–2501. doi: 10.1093/nar/21.10.2493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Locker D., Decoville M., Maurizot J. C., Bianchi M. E., Leng M. Interaction between cisplatin-modified DNA and the HMG boxes of HMG 1: DNase I footprinting and circular dichroism. J Mol Biol. 1995 Feb 17;246(2):243–247. doi: 10.1006/jmbi.1994.0079. [DOI] [PubMed] [Google Scholar]
  29. Mishima Y., Suda T., Kominami R. Formation of a triple-stranded DNA between d(GGA:TCC) repeats and d(GGA) repeat oligonucleotides. J Biochem. 1996 Apr;119(4):805–810. doi: 10.1093/oxfordjournals.jbchem.a021311. [DOI] [PubMed] [Google Scholar]
  30. Muraiso T., Nomoto S., Yamazaki H., Mishima Y., Kominami R. A single-stranded DNA binding protein from mouse tumor cells specifically recognizes the C-rich strand of the (AGG:CCT)n repeats that can alter DNA conformation. Nucleic Acids Res. 1992 Dec 25;20(24):6631–6635. doi: 10.1093/nar/20.24.6631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Oñate S. A., Prendergast P., Wagner J. P., Nissen M., Reeves R., Pettijohn D. E., Edwards D. P. The DNA-bending protein HMG-1 enhances progesterone receptor binding to its target DNA sequences. Mol Cell Biol. 1994 May;14(5):3376–3391. doi: 10.1128/mcb.14.5.3376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. 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]
  35. Rao B. J., Chiu S. K., Radding C. M. Homologous recognition and triplex formation promoted by RecA protein between duplex oligonucleotides and single-stranded DNA. J Mol Biol. 1993 Jan 20;229(2):328–343. doi: 10.1006/jmbi.1993.1038. [DOI] [PubMed] [Google Scholar]
  36. Read C. M., Cary P. D., Preston N. S., Lnenicek-Allen M., Crane-Robinson C. The DNA sequence specificity of HMG boxes lies in the minor wing of the structure. EMBO J. 1994 Dec 1;13(23):5639–5646. doi: 10.1002/j.1460-2075.1994.tb06902.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  38. Sen D., Gilbert W. Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis. Nature. 1988 Jul 28;334(6180):364–366. doi: 10.1038/334364a0. [DOI] [PubMed] [Google Scholar]
  39. Shykind B. M., Kim J., Sharp P. A. Activation of the TFIID-TFIIA complex with HMG-2. Genes Dev. 1995 Jun 1;9(11):1354–1365. doi: 10.1101/gad.9.11.1354. [DOI] [PubMed] [Google Scholar]
  40. Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
  41. Stros M., Stokrová J., Thomas J. O. DNA looping by the HMG-box domains of HMG1 and modulation of DNA binding by the acidic C-terminal domain. Nucleic Acids Res. 1994 Mar 25;22(6):1044–1051. doi: 10.1093/nar/22.6.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Suda T., Mishima Y., Asakura H., Kominami R. Formation of a parallel-stranded DNA homoduplex by d(GGA) repeat oligonucleotides. Nucleic Acids Res. 1995 Sep 25;23(18):3771–3777. doi: 10.1093/nar/23.18.3771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sundquist W. I., Klug A. Telomeric DNA dimerizes by formation of guanine tetrads between hairpin loops. Nature. 1989 Dec 14;342(6251):825–829. doi: 10.1038/342825a0. [DOI] [PubMed] [Google Scholar]
  44. Teo S. H., Grasser K. D., Thomas J. O. Differences in the DNA-binding properties of the HMG-box domains of HMG1 and the sex-determining factor SRY. Eur J Biochem. 1995 Jun 15;230(3):943–950. doi: 10.1111/j.1432-1033.1995.tb20640.x. [DOI] [PubMed] [Google Scholar]
  45. Travers A. A., Ner S. S., Churchill M. E. DNA chaperones: a solution to a persistence problem? Cell. 1994 Apr 22;77(2):167–169. doi: 10.1016/0092-8674(94)90306-9. [DOI] [PubMed] [Google Scholar]
  46. Williamson J. R., Raghuraman M. K., Cech T. R. Monovalent cation-induced structure of telomeric DNA: the G-quartet model. Cell. 1989 Dec 1;59(5):871–880. doi: 10.1016/0092-8674(89)90610-7. [DOI] [PubMed] [Google Scholar]
  47. Yotov W. V., St-Arnaud R. Nucleotide sequence of a mouse cDNA encoding the nonhistone chromosomal high mobility group protein-1 (HMG1). Nucleic Acids Res. 1992 Jul 11;20(13):3516–3516. doi: 10.1093/nar/20.13.3516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Zwilling S., König H., Wirth T. High mobility group protein 2 functionally interacts with the POU domains of octamer transcription factors. EMBO J. 1995 Mar 15;14(6):1198–1208. doi: 10.1002/j.1460-2075.1995.tb07103.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. van de Wetering M., Oosterwegel M., Dooijes D., Clevers H. Identification and cloning of TCF-1, a T lymphocyte-specific transcription factor containing a sequence-specific HMG box. EMBO J. 1991 Jan;10(1):123–132. doi: 10.1002/j.1460-2075.1991.tb07928.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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