Rationally designed insulator-like elements can block enhancer action in vitro

EMBO Journal

Volumn 22, Issue 18, 2003, Pages 4728-4737

  Bondarenko, Vladimir A ^a,b   Jiang, Yong I ^a   Studitsky, Vasily M ^a,b  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

Enhancers; Initiation; Insulators; RNA polymerase; Transcription

Indexed keywords

DNA; DNA BINDING PROTEIN;

ARTICLE; CHROMATIN; DNA SEQUENCE; DNA STRUCTURE; ENHANCER REGION; EUKARYOTE; GENE CONSTRUCT; GENE EXPRESSION; GENE FUNCTION; IN VITRO STUDY; IN VIVO STUDY; INSULATOR LIKE ELEMENT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN STABILITY; REPRESSOR GENE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

BASE SEQUENCE; CHROMATIN; CLONING, MOLECULAR; DNA, SUPERHELICAL; DRUG DESIGN; ENHANCER ELEMENTS (GENETICS); MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROMOTER REGIONS (GENETICS); RESTRICTION MAPPING; TEMPLATES, GENETIC; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 0141514008     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg468     Document Type: Article

References (67)

1. Bagga, R. and Emerson, B.M. (1997) An HMG I/Y-containing repressor complex and supercoiled DNA topology are critical for long-range enhancer-dependent transcription in vitro. Genes Dev., 11, 629-639.
2. Barkley, M.D., Riggs, A.D., Jobe, A. and Burgeois, S. (1975) Interaction of effecting ligands with lac repressor and repressor-operator complex. Biochemistry, 14, 1700-1712.
3. Barry, J.K. and Matthews, K.S. (1997) Ligand-induced conformational changes in lactose repressor: a fluorescence study of single tryptophan mutants. Biochemistry, 36, 15632-15642.
4. Barton, M.C., Madani, N. and Emerson, B.M. (1997) Distal enhancer regulation by promoter derepression in topologically constrained DNA in vitro. Proc. Natl Acad. Sci. USA, 94, 7257-7262.
5. Bondarenko, V., Liu, Y., Ninfa, A. and Studitsky, V.M. (2002) Action of prokaryotic enhancer over a distance does not require continued presence of promoter-bound sigma54 subunit. Nucleic Acids Res., 30, 636-642.
6. Bonifer, C., Vidal, M., Grosveld, F. and Sippel, A.E. (1990) Tissue specific and position independent expression of the complete gene domain for chicken lysozyme in transgenic mice. EMBO J., 9, 2843-2848.
7. Borowiec, J.A., Zhang, L., Sasse-Dwight, S. and Gralla, J.D. (1987) DNA supercoiling promotes formation of a bent repression loop in lac DNA. J. Mol. Biol., 196, 101-111.
8. Buck, M. and Cannon, W. (1992) Activator-independent formation of a closed complex between sigma 54-holoenzyme and nifH and nifU promoters of Klebsiella pneumoniae. Mol. Microbiol., 6, 1625-1630.
9. Buck, M., Gallegos, M.T., Studholme, D.J., Guo, Y. and Gralla, J.D. (2000) The bacterial enhancer-dependent sigma(54) (sigma(N)) transcription factor. J. Bacteriol., 182, 4129-4136.
10. Cai, H. and Levine, M. (1995) Modulation of enhancer-promoter interactions by insulators in the Drosophila embryo. Nature, 376, 533-536.
11. Cai, H.N. and Shen, P. (2001) Effects of cis arrangement of chromatin insulators on enhancer-blocking activity. Science, 291, 493-495.
12. Camerini-Otero, R.D. and Felsenfeld, G. (1977) Supercoiling energy and nucleosome formation: the role of the arginine-rich histone kernel. Nucleic Acids Res., 4, 1159-1181.
13. Chen, J., Alberti, S. and Matthews, K.S. (1994) Wild-type operator binding and altered cooperativity for inducer binding of lac repressor dimer mutant R3. J. Biol. Chem., 269, 12482-12487.
14. Chirico, G. and Langowski, J. (1996) Brownian dynamics simulations of supercoiled DNA with bent sequences. Biophys. J., 71, 955-971.
15. Choy, H.E. and Adhya, S. (1992) Control of gal transcription through DNA looping: inhibition of the initial transcribing complex. Proc. Natl Acad. Sci. USA, 89, 11264-11268.
16. Chung, J.H., Whiteley, M. and Felsenfeld, G. (1993) A 5′ element of the chicken β-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell, 74, 505-514.
17. Dorsett, D. (1993) Distance-independent inactivation of an enhancer by the suppressor of Hairy-wing DNA-binding protein of Drosophila. Genetics, 134, 1135-1144.
18. Eismann, E.R. and Muller-Hill, B. (1990) lac repressor forms stable loops in vitro with supercoiled wild-type lac DNA containing all three natural lac operators. J. Mol. Biol., 213, 763-775.
19. Flashner, Y. and Gralla, J.D. (1988) Dual mechanism of repression at a distance in the lac operon. Proc. Natl Acad. Sci. USA, 85, 8968-8972.
20. Gerasimova, T.I. and Corces, V.G. (1998) Polycomb and trithorax group proteins mediate the function of a chromatin insulator. Cell, 92, 511-521.
21. Gerasimova, T.I. and Corces, V.G. (2001) Chromatin insulators and boundaries: effects on transcription and nuclear organization. Annu. Rev. Genet., 35, 193-208.
22. Gerasimova, T.I., Byrd, K. and Corces, V.G. (2000) A chromatin insulator determines the nuclear localization of DNA. Mol. Cell, 6, 1025-1035.
23. Geyer, P.K. (1997) The role of insulator elements in defining domains of gene expression. Curr. Opin. Genet. Dev., 7, 242-248.
24. Geyer, P.K. and Corces, V.G. (1992) DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes Dev., 6, 1865-1873.
25. Geyer, P.K. and Clark, I. (2002) Protecting against promiscuity: the regulatory role of insulators. Cell Mol. Life Sci., 59, 2112-2127.
26. Golovnin, A., Gause, M., Georgieva, S., Gracheva, E. and Georgiev, P. (1999) The su(Hw) insulator can disrupt enhancer-promoter interactions when located more than 20 kilobases away from the Drosophila achaete-scute complex. Mol. Cell. Biol., 19, 3443-3456.
27. Havas, K., Flaus, A., Phelan, M., Kingston, R., Wade, P.A., Lilley, D.M. and Owen-Hughes, T. (2000) Generation of superhelical torsion by ATP-dependent chromatin remodeling activities. Cell, 103, 1133-1142.
28. Hsieh, W.T., Whitson, P.A., Matthews, K.S. and Wells, R.D. (1987) Influence of sequence and distance between two operators on interaction with the lac repressor. J. Biol. Chem., 262, 14583-14591.
29. Huang, J., Schlick, T. and Vologodskii, A. (2001) Dynamics of site juxtaposition in supercoiled DNA. Proc. Natl Acad. Sci. USA, 98, 968-973.
30. Hunt, T.P. and Magasanik, B. (1985) Transcription of glnA by purified Escherichia coli components: core RNA polymerase and the products of glnF, glnG and glnL. Proc. Natl Acad. Sci. USA, 82, 8453-8457.
31. Ishii, K., Arib, G., Lin, C., Van Houwe, G. and Laemmli, U.K. (2002) Chromatin boundaries in budding yeast: the nuclear pore connection. Cell, 109, 551-562.
32. Kellum, R. and Schedl, P. (1991) A position-effect assay for boundaries of higher order chromosomal domains. Cell, 64, 941-950.
33. Kellum, R. and Schedl, P. (1992) A group of scs elements function as domain boundaries in an enhancer-blocking assay. Mol. Cell. Biol., 12, 2424-2431.
34. Kramer, H., Niemoller, M., Amouyal, M., Revet, B., von Wilcken-Bergmann, B. and Muller-Hill, B. (1987) lac repressor forms loops with linear DNA carrying two suitably spaced lac operators. EMBO J., 6, 1481-1491.
35. Kramer, H., Amouyal, M., Nordheim, A. and Muller-Hill, B. (1988) DNA supercoiling changes the spacing requirement of two lac operators for DNA loop formation with lac repressor. EMBO J., 7, 547-556.
36. Kramer, P.R., Bat, O. and Sinden, R.R. (1999) Measurement of localized DNA supercoiling and topological domain size in eukaryotic cells. Methods Enzymol., 304, 639-650.
37. Krebs, J.E. and Dunaway, M. (1998) The scs and scs' insulator elements impart a cis requirement on enhancer-promoter interactions. Mol. Cell, 1, 301-308.
38. Kuhn, E.J., Viering, M.M., Rhodes, K.M. and Geyer, P.K. (2003) A test of insulator interactions in Drosophila. EMBO J., 22, 2463-2471.
39. Law, S.M., Bellomy, G.R., Schlax, P.J. and Record, M.T., Jr (1993) In vivo thermodynamic analysis of repression with and without looping in lac constructs. Estimates of free and local lac repressor concentrations and of physical properties of a region of supercoiled plasmid DNA in vivo. J. Mol. Biol., 230, 161-173.
40. Lewis, M., Chang, G., Horton, N.C., Kercher, M.A., Pace, H.C., Schumacher, M.A., Brennan, R.G. and Lu, P. (1996) Crystal structure of the lactose operon repressor and its complexes with DNA and inducer. Science, 271, 1247-1254.
41. Liu, L.F. and Wang, J.C. (1987) Supercoiling of the DNA template during transcription. Proc. Natl Acad. Sci. USA, 84, 7024-7027.
42. Liu, Y., Bondarenko, V., Ninfa, A. and Studitsky, V.M. (2001) DNA supercoiling allows enhancer action over a large distance. Proc. Natl Acad. Sci. USA, 98, 14883-14888.
43. Melnikova, L., Gause, M. and Georgiev, P. (2002) The gypsy insulators flanking yellow enhancers do not form a separate transcriptional domain in Drosophila melanogaster: the enhancers can activate an isolated yellow promoter. Genetics, 160, 1549-1560.
44. Muravyova, E., Golovnin, A., Gracheva, E., Parshikov, A., Belenkaya, T., Pirrotta, V. and Georgiev, P. (2001) Loss of insulator activity by paired Su(Hw) chromatin insulators. Science, 291, 495-498.
45. Mutskov, V.J., Farrell, C.M., Wade, P.A., Wolffe, A.P. and Felsenfeld, G. (2002) The barrier function of an insulator couples high histone acetylation levels with specific protection of promoter DNA from methylation. Genes Dev., 16, 1540-1554.
46. Oehler, S., Eismann, E.R., Kramer, H. and Muller-Hill, B, (1990) The three operators of the lac operon cooperate in repression. EMBO J., 9, 973-979.
47. O'Gorman, R.B., Rosenberg, J.M., Kallai, O.B., Dickerson, R.E., Itakura, K., Riggs, A.D. and Matthews, K.S. (1980) Equilibrium binding of inducer to lac repressor.operator DNA complex. J. Biol. Chem., 255, 10107-10114.
48. Popham, D.L., Szeto, D., Keener, J. and Kustu, S. (1989) Function of a bacterial activator protein that binds to transcriptional enhancers. Science, 243, 629-635.
49. Porter, S.C., North, A.K., Wedel, A.B. and Kustu, S. (1993) Oligomerization of NTRC at the glnA enhancer is required for transcriptional activation. Genes Dev., 7, 2258-2273.
50. Recillas-Targa, F., Pikaart, M.J., Burgess-Beusse, B., Bell, A.C., Litt, M.D., West, A.G., Gaszner, M. and Felsenfeld, G. (2002) Position-effect protection and enhancer blocking by the chicken β-globin insulator are separable activities. Proc. Natl Acad. Sci. USA, 99, 6883-6888.
51. Rippe, K., Guthold, M., von Hippel, P.H. and Bustamante, C. (1997) Transcriptional activation via DNA-looping: visualization of intermediates in the activation pathway of E. coli RNA polymerase × sigma 54 holoenzyme by scanning force microscopy. J. Mol. Biol., 270, 125-138.
52. Sasse-Dwight, S. and Gralla, J.D. (1988) Probing the Escherichia coli glnALG upstream activation mechanism in vivo. Proc. Natl Acad. Sci. USA, 85, 8934-8938.
53. Schedl, P. and Grosveld, F. (1995) Domains and boundaries. In Elgin, S.C. (ed.), Chromatin Structure and Gene Expression. Oxford University Press, Oxford, UK, pp. 172-196.
54. Schmitz, A. and Galas, D.J. (1979) The interaction of RNA polymerase and lac repressor with the lac control region. Nucleic Acids Res., 6, 111-137.
55. Scott, K.S. and Geyer, P.K. (1995) Effects of the su(Hw) insulator protein on the expression of the divergently transcribed Drosophila yolk protein genes. EMBO J., 14, 6258-6267.
56. Simons, A., Tils, D., von Wilcken-Bergmann, B. and Muller-Hill, B. (1984) Possible ideal lac operator: Escherichia coli lac operator-like sequences from eukaryotic genomes lack the central G X C pair. Proc. Natl Acad. Sci. USA, 81, 1624-1628.
57. Sinden, R.R., Carlson, J.O. and Pettijohn, D.E. (1980) Torsional tension in the DNA double helix measured with trimethylpsoralen in living E. coli cells: analogous measurements in insect and human cells. Cell, 21, 773-783.
58. Straney, S.B. and Crothers, D.M. (1987) Lac repressor is a transient gene-activating protein. Cell, 51, 699-707.
59. Su, W., Porter, S., Kustu, S. and Echols, H. (1990) DNA-looping and enhancer activity: association between DNA-bound NtrC activator and RNA polymerase at the bacterial glnA promoter. Proc. Natl Acad. Sci. USA, 87, 5504-5508.
60. Vologodskii, A. and Cozzarelli, N.R. (1996) Effect of supercoiling on the juxtaposition and relative orientation of DNA sites. Biophys. J., 70, 2548-2556.
61. Wedel, A. and Kustu, S. (1995) The bacterial enhancer-binding protein NTRC is a molecular machine: ATP hydrolysis is coupled to transcriptional activation. Genes Dev., 9, 2042-2052.
62. Wei, W. and Brennan, M.D. (2000) Polarity of transcriptional enhancement revealed by an insulator element. Proc. Natl Acad. Sci. USA, 97, 14518-14523.
63. Wei, W. and Brennan, M.D. (2001) The gypsy insulator can act as a promoter-specific transcriptional stimulator. Mol. Cell. Biol., 21, 7714-7720.
64. West, A.G., Gaszner, M. and Felsenfeld, G. (2002) Insulators: many functions, many mechanisms. Genes Dev., 16, 271-288.
65. Whitson, P.A., Hsieh, W.T., Wells, R.D. and Matthews, K.S. (1987) Influence of supercoiling and sequence context on operator DNA binding with lac repressor. J. Biol. Chem., 262, 14592-14599.
66. Wu, H.Y., Shyy, S.H., Wang, J.C. and Liu, L.F. (1988) Transcription generates positively and negatively supercoiled domains in the template. Cell, 53, 433-440.
67. Wyman, C., Rombel, I., North, A.K., Bustamante, C. and Kustu, S. (1997) Unusual oligomerization required for activity of NtrC, a bacterial enhancer-binding protein. Science, 275, 1658-1661.