The architecture of the heat-inducible Drosophila hsp27 promoter in nuclei

Journal of Molecular Biology

Volumn 256, Issue 2, 1996, Pages 249-263

  Quivy, Jean Pierre ^a   Becker, Peter B ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Chromatin; Genomic footprinting; Heat shock promoter; Positioned nucleosome; Transcription activation

Indexed keywords

1,10 PHENANTHROLINE; HEAT SHOCK PROTEIN; NUCLEASE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; DNA FOOTPRINTING; DNA SEQUENCE; DNA STRUCTURE; DROSOPHILA; EMBRYO; HEAT; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA INTERACTION; TATA BOX; TISSUE CULTURE CELL; TRANSCRIPTION INITIATION;

EID: 0029916961     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0083     Document Type: Article

References (87)

1. Bazett-Jones, D. P., Leblanc, B., Herfort, M. & Moss, T. (1994). Short-range looping by the Xenopus HMG-box transcription factor, xUBF. Science, 264, 1134-1137.
2. Becker, P. B. & Schütz, G. (1988). Genomic footprinting. In Genetic Engineering (Setlow, J. K., ed.), vol. 10, Plenum Press, New York.
3. Becker, P. B., Weih, F. & Schütz, G. (1993). Footprinting of DNA binding proteins in intact cells. Methods Enzymol. 218, 568-587.
4. Becker, P. B., Tsukiyama, T. & Wu, C. (1994). Chromatin assembly extracts from Drosophila embryos. Methods Cell Biol. 44, 207-223.
5. Buttinelli, M., Di Mauro, E. & Negri, R. (1993). Multiple nucleosome positioning with unique rotational setting for the Saccharomyces cerevisiae 5S rRNA gene in vitro and in vivo. Proc. Natl Acad. Sci. USA, 90, 9315-9319.
6. Cartwright, I. L. & Elgin, S. C. R. (1982). Analysis of chromatin structure and DNA sequence organisation: use of the 1,10-phenanthroline-cuprous complex. Nucl. Acids Res. 10, 5835-5852.
7. Cartwright, I. L. & Elgin, S. C. R. (1986). Nucleosomal instability and induction of new upstream protein-DNA associations accompany activation of four small heat shock protein genes in Drosophila melanogaster. Mol. Cell. Biol. 6, 779-791.
8. Churchill, M. E. A., Jones, D. N. M., Glaser, T., Hefner, H., Searles, M. A. & Travers, A. A. (1995). HMG-D is an architecture-specific protein that preferentially binds to DNA containing the dinucleotide TG. EMBO J. 14, 1264-1275.
9. Cohen, R. S. & Meselson, M. (1988). Periodic interactions of heat shock transcriptional elements. Nature, 332, 856-858.
10. Costlow, N. & Lis, J. T. (1984). High-resolution mapping of DNase I-hypersensitive sites of Drosophila heat shock genes in Drosophila melanogaster and Saccharomyces cerevisiae. Mol. Cell. Biol. 4, 1853-1863.
11. Craig, E. A. (1980). Four Drosophila heat shock genes at 67B: characterization of recombinant plasmids. Nucl. Acids Res. 8, 4441-4457.
12. Cullen, K. E., Kladde, M. P. & Seyfred, M. A. (1993). Interaction between transcription regulatory regions of prolactin chromatin. Science, 261, 203-206.
13. Dillon, N. & Grosveld, F. (1993). Transcriptional regulation of multigene loci: multilevel control. Trends Genet. 9, 134-137.
14. Du, W., Thanos, D. & Maniatis, T. (1993). Mechanisms of transcriptional synergism between distinct virus-inducible enhancer elements. Cell, 74, 887-898.
15. Ephrussi, A., Church, G., Tonegawa, S. & Gilbert, W. (1985). B lineage-specific interaction of an immunoglobulin enhancer with cellular factors in vivo. Science, 227, 134-140.
16. Fedor, M. J. & Kornberg, R. D. (1989). Upstream activation sequence-dependent alteration of chromatin structure and transcription activation of the yeast GAL1-GAL10 genes. Mol. Cell. Biol. 9, 1721-1732.
17. Fedor, M. J., Lue, N. F. & Kornberg, R. D. (1988). Statistical positioning of nucleosomes by specific protein-binding to an upstream activating sequence in yeast. J. Mol. Biol. 204, 109-127.
18. Fernandes, M., Xiao, H. & Lis, J. T. (1994). Fine structure analyses of the Drosophila and Saccharomyces heat shock factor-heat shock element interactions. Nucl. Acids Res. 22, 167-173.
19. Fragoso, G., John, S., Roberts, M. S. & Hager, G. L. (1995). Nucleosome positioning on the MMTV LTR results from the frequency-biased occupancy of multiple frames. Genes Dev. 9, 1933-1947.
20. Giese, K., Cox, J. & Grosschedl, R. (1992). The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoproteins structures. Cell, 69, 185-195.
21. Gilmour, D. S., Thomas, G. H. & Elgin, S. C. R. (1989). Drosophila nuclear proteins bind to regions of alternating C and T residues in gene promoters. Science, 245, 1487-1490.
22. Godde, J. S. & Widom, J. (1992). Chromatin structure of Schizosaccharomyces pombe (A nucleosome repeat length that is shorter than the chromatosomal DNA length). J. Mol. Biol. 226, 1009-1025.
23. Gralla, J. D. (1989). Bacterial gene regulation from distant DNA sites. Cell, 57, 193-195.
24. Granok, H., Leibovitch, B. A., Shaffer, C. D. & Elgin, S. C. R. (1995). Ga-ga over GAGA factor. Curr. Biol. 5, 238-241.
25. Grosschedl, R. (1995). Higher-order nucleoprotein complexes in transcription: analogies with site-specific recombination. Curr. Opin. Cell. Biol. 7, 362-370.
26. Hayes, J. J., Clark, D. J. & Wolffe, A. P. (1991). Histone contributions to the structure of DNA in the nucleosome. Proc. Natl Acad. Sci. USA, 88, 6829-6833.
27. Hecht, A., Laroche, T., Strahl-Bolsinger, S., Gasser, S. M. & Grunstein, M. (1995). Histone H3 and H4 N-termini interact with SIR3 and Sir4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell, 80, 583-592.
28. Hoffmann, E. & Corces, V. (1986). Sequences involved in temperature and ecdysterone-induced transcription are located in separate regions of a Drosophila melanogaster heat shock gene. Mol. Cell. Biol. 6, 663-673.
29. Hoffmann, E. P., Gerring, S. L. & Corces, V. G. (1987). The ovarian, ecdysterone, and heat-shock-responsive promoters of the Drosophila hsp27 gene react very differently to perturbations of DNA sequence. Mol. Cell. Biol. 7, 973-981.
30. Jackson, J. R. & Benyajati, C. (1992). DNA-histone interactions are sufficient to position a single nucleosome juxtaposing Drosophila Adh adult enhancer and distal promoter. Nucl. Acids Res. 21, 957-967.
31. Kerrigan, L. A. & Kadonaga, J. T. (1992). Periodic binding of individual core histones to DNA: inadvertant purification of the core histone H2B as a putative enhancer-binding factor. Nucl. Acids Res. 20, 6673-6680.
32. Klug, A. (1993). Opening the gateway. Nature, 365, 486-487.
33. Lis, J. T. & Wu, C. (1994). Transcriptional regulation of heat shock genes. In Transcription: Mechanisms and Regulation (Conaway, R. V. & Conaway, J. W., eds), pp. 459-475, Raven Press, New York.
34. n repeats is critical for the formation of the DNase I hypersensitive sites in the Drosophila hsp26 gene. J. Mol. Biol. 225, 985-998.
35. n repeats and heat shock elements have distinct roles in chromatin structure and transcriptional activation of the Drosophila hsp26 gene. Mol. Cell. Biol. 13, 2802-2814.
36. Lu, Q., Wallrath, L. L. & Elgin, S. C. R. (1994). Nucleosome positioning and gene regulation. J. Cell. Biochem. 55, 83-92.
37. Lutter, L. C. (1978). Kinetic analysis of deoxyribonuclease I cleavages in the nucleosome core: evidence for a DNA superhelix. J. Mol. Biol. 124, 391-420.
38. Mason, P. J., Hall, L. M. C. & Gausz, J. (1984). The expression of heat shock genes during normal development in Drosophila melanogaster. Mol. Gen. Genet. 194, 73-78.
39. McPherson, C. E., Shim, E., Friedman, D. S. & Zaret, K. S. (1993). An active tissue-specific enhancer and bound transcription factors existing in a precisely positioned nucleosomal array. Cell, 75, 387-398.
40. Mirkovitch, J. & Darnell, J. E. J. (1991). Rapid in vivo footprinting technique identifies proteins bound to the TTR gene in the mouse liver. Genes Dev. 5, 83-93.
41. Mueller, P. R. & Wold, B. (1989). In vivo footprinting of a muscle-specific enhancer by ligation-mediated PCR. Science, 246, 780-810.
42. Mueller, P. R., Garrity, P. A. & Wold, B. (1993). Ligation mediated PCR for genomic sequencing and footprinting. In Current Protocols in Molecular Biology (Ausubel, I. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K., eds), vol. 2, Current Protocols, New York.
43. Natesan, S. & Gilman, M. Z. (1993). DNA bending and orientation-dependent function of YY1 in the c-fos promoter. Genes Dev. 7, 2497-2509.
44. Noll, M. & Kornberg, R. D. (1977). Action of micrococcal nuclease on chromatin and the location of histone H1. J. Mol. Biol. 1109, 393-404.
45. O'Brien, T. & Lis, J. T. (1993). Rapid changes in Drosophila transcription after an instantaneous heat shock. Mol. Cell. Biol. 13, 3456-3463.
46. Orlando, V. & Paro, R. (1995). Chromatin multiprotein complexes involved in the maintainance of transcription patterns. Curr. Opin. Genet. Dev. 5, 174-179.
47. Papavassiliou, A. G. (1994). 1,10-Phenanthroline-copper ion nuclease footprinting of DNA-protein complexes in situ following mobility shift electrophoresis assays. In Methods in Molecular Biology (Kneale, G. G., ed.), vol. 5, pp. 43-78, Humana Press, New Jersey.
48. Paranjape, S. M., Kamakaka, R. T. & Kadonaga, J. T. (1994). Role of chromatin structure in the regulation of transcription by RNA polymerase II. Annu. Rev. Biochem. 63, 265-297.
49. Paull, T. T., Haykinson, M. J. & Johnson, R. C. (1993). The non-specific DNA-binding and -bending proteins HMG1 and HMG2 promote the assembly of complex nucleoprotein structures. Genes Dev. 7, 1521-1534.
50. Perisic, O., Xiao, H. & Lis, J. T. (1989). Stable binding of Drosophila heat shock factor to head-to-head and tail-to-tail repeats of a conserved 5 bp recognition unit. Cell, 59, 797-806.
51. Pfeifer, G. P. & Riggs, A. D. (1991). Chromatin differences between active and inactive X chromosomes revealed by genomic footprinting of permeabilizd cells using DNase I and ligation-mediated PCR. Genes Dev. 5, 1102-1113.
52. Pfeifer, G. P., Steigerwald, S. D., Mueller, P. R., Wold, B. & Riggs, A. D. (1989). Genomic sequencing and methylation analysis by ligation mediated PCR. Science, 246, 810-813.
53. Ptashne, M. (1986). Gene regulation by proteins acting nearby and at a distance. Nature, 322, 697-701.
54. Quivy, J.-P. & Becker, P. B. (1993). An improved protocol for genomic sequencing and footprinting by ligation-mediated PCR. Nucl. Acids Res. 21, 2779-2781.
55. Quivy, J.-P. & Becker, P. B. (1994). Direct dideoxy sequencing of genomic DNA by ligation-mediated PCR. BioTechniques, 16, 238-241.
56. Rasmussen, E. B. & Lis, J. T. (1993). In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc. Natl Acad. Sci. USA, 90, 7923-7927.
57. Riddihough, G. & Pelham, H. (1986). Activation of the Drosophila hsp27 promoter by heat shock and by ecdysone involves independent and remote regulatory elements. EMBO J. 5, 1653-1658.
58. Riddihough, G. & Pelham, H. R. B. (1987). An ecdysone response element in the Drosophila hsp27 promoter. EMBO J. 6, 3729-3734.
59. Roth, S. Y., Shimizu, M., Johnson, L., Grunstein, M. & Simpson, R. T. (1992). Stable nucleosome positioning and complete repression by the yeast alpha 2 repressor are disrupted by amino-terminal mutations in histone H4. Genes Dev. 6, 411-425.
60. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
61. Sandaltzopoulos, R., Mitchelmore, C., Bonte, E., Wall, G. & Becker, P. B. (1995). Dual regulation of the Drosophila hsp26 promoter in vitro. Nucl. Acids Res. 23, 2479-2487.
62. Schild, C., Claret, F., Wahli, W. & Wolffe, A. P. (1993). A nucleosome-dependent static loop potentiates estrogen-regulated transcription from the Xenopus vitellogenin B1 promoter in vitro. EMBO J. 12, 423-433.
63. Segall, A. M., Goodman, S. D. & Nash, H. A. (1994). Architectural elements in nucleoprotein complexes: interchangeability of specific and nonspecific DNA binding proteins. EMBO J. 13, 4536-4548.
64. Sigman, D. S. (1990). Chemical nucleases. Biochemistry, 29, 9097-9105.
65. Simon, J. A. & Lis, J. T. (1987). A germline transformation analysis reveals flexibility in the organisation of heat shock consensus elements. Nucl. Acids Res. 15, 2971-2988.
66. Simpson, R. T. (1978). Structure of the chromatosome, a chromatin core particle containing 160 base pairs of DNA and all the histones. Biochemistry, 17, 5524-5521.
67. Soeller, W. C., Oh, C. E. & Kornberg, T. B. (1993). Isolation of cDNAs encoding the Drosophila GAGA transcription factor. Mol. Cell. Biol. 13, 7961-7970.
68. Thanos, D. & Maniatis, T. (1992). The high mobility group protein HMG I/Y is required for NFκB-dependent virus induction of the human INF-β gene. Cell, 71, 777-789.
69. Thoma, F. (1992). Nucleosome positioning. Biochim. Biophys. Acta, 1130, 1-19.
70. Thoma, F., Koller, T. & Klug, A. (1979). Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J. Cell Biol. 83, 403-427.
71. Thomas, G. H. & Elgin, S. C. R. (1988). Protein/DNA architecture of the DNase I hypersensitive region of the Drosophila hsp26 promoter. EMBO J. 7, 2191-2201.
72. Todd, R. D. & Garrard, W. T. (1979). Overall pathway of mononucleosome production. J. Biol. Chem. 254, 3074-3083.
73. Truss, M., Bartsch, J., Schelbert, A., Hachi, R. J. G. & Beato, M. (1995). Hormone induces binding of receptors and transcription factors to a rearranged nucleosome on the MMTV promoter in vivo. EMBO J. 14, 1737-1751.
74. Van der Vliet, P. C. & Verrijzer, C. P. (1993). Bending of DNA by transcription factors. BioEssays, 15, 25-32.
75. Van Holde, K. E. (1988). Chromatin (Rich, A., ed.), Springer, Berlin.
76. Verdin, E., Paras, P., Jr & Van Lint, C. (1993). Chromatin disruption in the promoter of human immunodefiency virus type 1 during transcriptional activation. EMBO J. 12, 3249-3259.
77. Verrijzer, C. P., Yokomori, K., Chen, J. & Tjian, R. (1994). Drosophila TAFII150: similarity to yeast gene TSM-1 and specific binding to core promoter DNA. Science, 264, 933-941.
78. Wallrath, L. L., Quinn, L., Granok, H. & Elgin, S. C. R. (1994). Architectural variations of inducible eukaryotic promoters: preset and remodeling chromatin structures. BioEssays, 6, 165-170.
79. Weintraub, H. (1985). Assembly and propagation of repressed and derepressed chromosomal states. Cell, 42, 705-711.
80. Weisbrod, S. (1982). Active chromatin. Nature, 297, 289-295.
81. Weischet, W. O. & Van Holde, K. E. (1980). Nuclease digestion promotes structural rearrangements in H1 depleted chromatin. Nucl. Acids Res. 8, 3743-3755.
82. Wolffe, A. P. (1994a). Architectural transcription factors. Science, 264, 1100-1101.
83. Wolffe, A. P. (1994b). Transcription: in tune with the histones. Cell, 77, 1-4.
84. Wyman, C., Grotlopp, E., Bustamante, C. & Nelson, H. C. (1995). Determination of heat shock transcription factor 2 stoichiometry at looped DNA complexes using scanning force microscopy. EMBO J. 14, 117-123.
85. Xiao, H., Perisic, O. & Lis, J. T. (1991). Cooperative binding of Drosophila Heat shock factor to arrays of a conserved 5 bp unit. Cell, 64, 585-593.
86. Zawel, L., Kumar, K. P. & Reinberg, D. (1995). Recycling of the general transcription factors during RNA polymerase II transcription. Genes Dev. 9, 1479-1490.
87. Zhang L. & Gralla, J. D. (1989). In situ nucleoprotein structure at the SV40 major late promoter: melted and wrapped DNA flank the start site. Genes Dev. 3, 1814-1822.