Xenopus transcription factor IIIA and the 5S nucleosome: Development of a useful in vitro system

Biochemistry and Cell Biology

Volumn 81, Issue 3, 2003, Pages 177-184

  Yang, Zungyoon ^a   Hayes, Jeffrey J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

5S genes; Chromatin; Nucleosomes; Transcription factor IIIA

Indexed keywords

BINDING ENERGY; COMPLEXATION; DNA; GENETIC ENGINEERING; MOLECULAR BIOLOGY; RNA;

TRANSCRIPTION FACTORS;

BIOCHEMISTRY;

DNA; HISTONE; RNA 5S; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR IIIA; UNCLASSIFIED DRUG;

ACETYLATION; CHROMATIN STRUCTURE; CONFERENCE PAPER; DNA BINDING; DNA TRANSCRIPTION; EUKARYOTE; GENE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOSOME; TRANSCRIPTION INITIATION; XENOPUS;

ANIMALS; DNA; HISTONES; MODELS, BIOLOGICAL; NUCLEOSOMES; PROTEIN BINDING; RNA, RIBOSOMAL, 5S; TRANSCRIPTION FACTOR TFIIIA; XENOPUS PROTEINS;

EUKARYOTA; STAPHYLOCOCCUS PHAGE 3A;

EID: 0042888952     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o03-043     Document Type: Conference Paper

References (89)

1. Almouzni, G., Clark, D.J., Mechali, M., and Wolffe, A.P. 1990. Chromatin assembly on replicating DNA in vitro. Nucleic Acids Res. 18: 5767-5774.
2. Almouzni, G., Mechali, M., and Wolffe, A.P. 1991. Transcription complex disruption caused by a transition in chromatin structure. Mol. Cell. Biol. 11: 655-665.
3. Andrews, M.T., and Brown, D.D. 1987. Transient activation of oocyte 5S RNA genes in Xenopus embryos by raising the level of the trans-acting factor TFIIIA. Cell, 51: 445-453.
4. Bauer, W.R., Hayes, J.J., White, J.H., and Wolffe, A.P. 1994. Nucleosome structural changes due to acetylation. J. Mol. Biol. 236: 685-690.
5. Berg, J.M. 1990. "Zinc Finger" domains: Hypothesis and current knowledge. Ann. Rev. Biophys. Chem. 19: 405-421.
6. Berg, J.M., and Merkle, D.L. 1989. On the metal ion specificity of "Zinc Finger" proteins. J. Am. Chem. Soc. 111: 3759-3761.
7. Bieker, J.J., and Roeder, R.G. 1984. Physical properties and DNA-binding stoichiometry of a 5S gene-specific transription factor. J. Biol. Chem. 259: 6158-6164.
8. Bogenhagen, D.F., Wormington, W.M., and Brown, D.D. 1982. Stable Transcription Complexes of Xenopus 5S RNA Genes: A Means to Maintain the Differentiated State. Cell, 28: 413-421.
9. Brown, D.D., and Gurdon, J.B. 1978. Cloned single repeating units of 5S DNA direct accurate transcription of 5S RNA when injected into Xenopus oocytes. Proc. Natl. Acad. Sci. U.S.A. 75: 2849-2853.
10. Brown, D.D., and Littna, E. 1964. RNA synthesis during the development of Xenopus laevis, the South African Clawed Toad. J. Mol. Biol. 8: 669-687.
11. Brown, D.D., and Weber, C.S. 1968. Gene linkage by RNA-DNA hybridization. I. Unique DNA sequences homologous to 4 s RNA, 5 s RNA and ribosomal RNA. J. Mol. Biol. 34: 661-680.
12. Brown, R.S., Sander, C., and Wolffe, A.P. 1985. The Primary Structure of Transcription Factor TFIIIA Has 12 Consecutive Repeats. FEBS Lett. 186: 271-274.
13. Brown, M.L., Schroth, G.P., Gottesfeld, J.M., and Bazett-Jones, D.P. 1996. Protein and DNA requirements for the transcription factor IIIA-induced distortion of the 5 S rRNA gene promoter. J. Mol. Biol. 262: 600-614.
14. Chafin, D.R., Vitolo, J.M., Henricksen, L.A., Bambara, R.A., and Hayes, J.J. 2000. Human DNA ligase I efficiently seals nicks in nucleosomes. EMBO J. 19: 5492-5501.
15. Chipev, C.C., and Wolffe, A.P. 1992. Chromosomal organization of Xenopus laevis oocyte and somatic 5S rRNA genes in vivo. Mol. Cell. Biol. 12: 45-55.
16. Choo, Y., and Klug, A. 1994. Selection of DNA binding sites for zinc fingers using rationally randomized DNA reveals coded interactions. Proc. Natl. Acad. Sci. U.S.A. 91: 11 168-11 172.
17. Churchill, M.E.A., Tullius, T.D., and Klug, A. 1990. Mode of interaction of the zinc finger protein TFIIIA with a 5S RNA gene of Xenopus. Proc. Natl. Acad. Sci. U.S.A. 87: 5528-5532.
18. Ciliberto, G., Raugel, G., Costanzo, F., Dente, L., and Cortese, R. 1983. Common and Interchangeable Elements in the Promoters of Genes Transcribed by RNA Polymerase III. Cell, 32: 725-733.
19. Clemens, K.R., Liao, X., Wolf, V., Wright, P.E., and Gottesfeld, J.M. 1992. Definition of the binding sites of individual Zn-fingers in the transcription factor IIIA-5S RNA gene complex. Proc. Natl. Acad. Sci. U.S.A. 89: 10 822-10 826.
20. Coleman, J.E. 1992. Zinc proteins: enzymes, storage proteins, transcription factors, and replication proteins. Annu. Rev. Biochem. 61: 897-946.
21. Darby, M.K., Andrews, M.T., Brown, D.D. 1988. Transcription complexes that program Xenopus 5S RNA genes are stable in vivo. Proc. Natl. Acad. Sci. U.S.A. 85: 5516-5520.
22. Denis, H., Wegnez, M., and Willem, R. 1972. [Biochemical research on oogenesis. V. Comparison between somatic 5 S RNA and oocyte 5 S RNA in Xenopus laevis]. Biochimie, 54: 1189-1195. [French.]
23. Diakun, G.P., Fairall, L., and Klug, A. 1986. EXAFS Study of the zinc-binding Sites in the Protein Transcription Factor IIIA. Nature (London), 324: 698-699.
24. Engelke, D.R., Ng, S.-Y., Shastry, B.S., and Roeder, R.G. 1980. Specific Interaction of a Purified Transcription Factor with an Internal Control Region of 5S RNA Genes. Cell, 19: 717-728.
25. Fairall, L., Schwabe, J.W., Chapman, L., Finch, J.T., and Rhodes, D. 1993. The crystal structure of a two zinc-finger peptide reveals an extension to the rules for zinc-finger/DNA recognition. Nature (London), 366: 483-487.
26. Fedoroff, N.V. 1979. Deletion Mutants of Xenopus laevis 5S Ribosomal DNA. Cell, 16:551-563.
27. Felts, S.J., Weil, P.A., and Chalkley, R. 1990. Transcription factor requirements for in vitro formation of transcriptionally competent 5S rRNA gene chromatin. Mol. Cell. Biol. 10: 2390-2401.
28. Ford, P.J., and Southern, E.M. 1973. Different sequences for 5S RNA in kidney cells and ovaries of Xenopus laevis. Nat. New Biol. 241: 7-12.
29. Ginsberg, A.M., King, B.O., and Roeder, R.G. 1984. Xenopus 5S Gene Transcription Factor, TFIIIA: Characterization of a cDNA Clone and Measurement of RNA Levels Throughout Development. Cell, 39: 479-489.
30. Gottesfeld, J.M. 1987. DNA sequence-directed nucleosome reconstitution on 5S RNA genes of Xenopus laevis. Mol. Cell. Biol. 7: 1612-1622.
31. Gottesfeld, J.M., and Bloomer, L.S. 1980. Nonrandom alignment of nucleosomes on 5S RNA genes of X. laevis. Cell, 21: 751-760.
32. Hanas, J.S., Hazuda, D.J., Bogenhagen, D.F., Wu, F.Y.H., and Wu, C.-W. 1983. Xenopus transcription factor A requires zinc for binding to the 5S RNA gene. J. Biol. Chem. 258: 14 120-14 125.
33. Hayes, J.J., and Clemens, K.R. 1992. Location of contacts between individual zinc fingers of Xenopus laevis transcription factor IIIA and the internal control region of a 5S RNA gene. Biochemistry 31: 11 600-11 605.
34. Hayes, J.J., and Tullius, T.D. 1992. The structure of the TFIIIA/5S DNA complex. J. Mol. Biol. 227: 407-417.
35. Hayes, J.J., and Wolffe, A.P. 1992. Histones H2A/H2B inhibit the interaction of transcription factor IIIA with the Xenopus borealis somatic 5S RNA gene in a nucleosome. Proc. Natl. Acad. Sci. U.S.A. 89: 1229-1233.
36. Hayes, J.J., Tullius, T.D., and Wolffe, A.P. 1989. A protein-protein interaction is essential for stable complex formation on a 5 S RNA gene. J. Biol. Chem. 264: 6009-6012.
37. Hayes, J.J., Tullius, T.D., and Wolffe, A.P. 1990. The structure of DNA in a nucleosome. Proc. Natl. Acad. Sci. U.S.A. 87: 7405-7409.
38. Hayes, J.J., Clark, D.J., and Wolffe, A.P. 1991. Histone contributions to the structure of DNA in the nucleosome. Proc. Natl. Acad. Sci. U.S.A. 88: 6829-6833.
39. Houbaviy, H.B., Usheva, A., Shenk, T., and Burley, S.K. 1996. Cocrystal structure of YY1 bound to the adeno-associated virus P5 initiator. Proc. Natl. Acad. Sci. U.S.A. 93: 13 577-13 582.
40. Howe, L., Itoh, T., Katagiri, C., and Ausio, J. 1998a. Histone H1 binding does not inhibit transcription of nucleosomal Xenopus laevis somatic 5S rRNA templates. Biochemistry, 37: 7077-7082.
41. Howe, L., Ranalli, T.A., Allis, C.D., and Ausio, J. 1998b. Transcriptionally active Xenopus laevis somatic 5 S ribosomal RNA genes are packaged with hyperacetylated histone H4, whereas transcriptionally silent oocyte genes are not. J. Biol. Chem. 273: 20 693-20 696.
42. Knochel, W., Poting, A., Koster, M., El Baradi, T., Nietfeld, W., and Bouwmeester, T. 1989. Evolutionary Conserved Modules Associated With zinc Fingers in Xenopus laevis. Proc. Natl. Acad. Sci. U.S.A. 86: 6097-6100.
43. Korn, L.J., and Brown, D.D. 1978. Nucleotide sequence of Xenopus borealis oocyte 5S DNA: comparison of sequences that flank several related eucaryotic genes. Cell, 15: 1145-1156.
44. Lassar, A.B., Martin, P.L., and Roeder, R.G. 1983. Transcription of class III genes: formation of preinitiation complexes. Science (Washington, D.C.), 222: 740-748.
45. Lee, M.S., Gippert, G.P., Soman, K.V., Case, D.A., and Wright, P.E. 1989. Three-dimensional solution structure of a single zinc finger DNA-binding domain. Science, 245: 635-637.
46. Lee, D.Y., Hayes, J.J., Pruss, D., and Wolffe, A.P. 1993. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell, 72: 73-84.
47. Miller, J., McLachlan, A.D., and Klug, A. 1985. Repetitive zinc-Binding Domains in the Protein Transcription Factor IIIA from Xenopus Oocytes. EMBO J. 4: 1609-1614.
48. Morse, R.H. 1989. Nucleosomes inhibit both transcriptional initiation and elongation by RNA polymerase III in vitro. EMBO J. 8: 2343-2351.
49. Nardelli, J., Gibson, T.J., Vesque, C., and Charnay, P. 1991. Base-sequence discrimination by zinc-finger DNA binding domains. Nature (London), 349: 175-178.
50. Nickol, J., and Rau, D.C. 1992. Zinc induces a bend within the transcription factor IIIA-binding region of the 5 S RNA gene. J. Mol. Biol. 228: 1115-1123.
51. Nolte, R.T., Conlin, R.M., Harrison, S.C., and Brown, R.S. 1998. Differing roles for zinc fingers in DNA recognition: structure of a six-finger transcription factor IIIA complex. Proc. Natl. Acad. Sci. U.S.A. 95: 2938-2943.
52. Parker, C.S., and Roeder, R.G. 1977. Selective and accurate transcription of the Xenopus laevis 5S RNA genes in isolated chromatin by purified RNA polymerase III. Proc. Natl. Acad. Sci. U.S.A. 74: 44-48.
53. Parraga, G., Horvath, S.J., Eisen, A., Taylor, W.E., Hood, L., Young, E.T., and Klevit, R.E. 1988. Zinc-dependent structure of a single-finger domain of yeast ADR1. Science (Washington, D.C.), 241: 1489-1492.
54. Pavletich, N.P., and Pabo, C.O. 1991. Zinc finger-DNA recognition: Crystal structure of a Zif268-DNA complex at 2.1 Å. Science (Washington, D.C.), 252: 809-817.
55. Pavletich, N.P., and Pabo, C.O. 1993. Crystal structure of a five-finger GLI-DNA complex: new perspectives on zinc fingers. Science (Washington, D.C.), 261: 1701-1707.
56. Peterson, R.C., Doering, J.L., and Brown, D.D. 1980. Characterization of two Xenopus somatic 5S DNAs and one minor oocyte-specific 5S DNA. Cell, 20: 131-141.
57. Pieler, T., Hamm, J., and Roeder, R.G. 1987. The 5S Gene internal control region is composed of three distinct sequence elements, organized as two functional domains with variable spacing. Cell, 48: 91-100.
58. Polach, K.J., and Widom, J. 1995. Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J. Mol. Biol. 254: 130-149.
59. Polach, K.J., Lowary, P.T., and Widom, J. 2000. Effects of core histone tail domains on the equilibrium constants for dynamic DNA site accessibility in nucleosomes. J. Mol. Biol. 298: 211-223.
60. Rhodes, D. 1985. Structural analysis of a triple complex between the histone octamer, a Xenopus gene for 5S RNA and transcription factor IIIA. EMBO J. 4: 3473-3482.
61. Rhodes, D., and Klug, A. 1986. An underlying repeat in some transcriptional control sequences corresponding to half a double helical turn of DNA. Cell, 46: 123-132.
62. Sakonju, S., and Brown, D.D. 1981. The binding of a transcription factor to deletion mutants of a 5S ribosomal RNA gene. Cell, 23: 665-669.
63. Sakonju, S., and Brown, D.D. 1982. Contact points between a positive transcription factor and the Xenopus 5S RNA gene. Cell, 31: 395-405.
64. Sakonju, S., Bogenhagen, D.F., and Brown, D.D. 1980. A control region in the center of the 5S RNA gene directs specific initiation of transcription: I. The 5′ border of the region. Cell, 19: 13-25.
65. Schlissel, M.S., and Brown, D.D. 1984. The transcriptional regulation of Xenopus 5S RNA genes in chromatin: the roles of active stable transcription complexes and histone H1. Cell, 37: 903-913.
66. Schroth, G.P., Cook, G.R., Bradbury, E.M., and Gottesfeld, J.M. 1989. Transcription factor IIIA induced bending of the Xenopus somatic 5S gene promoter. Nature (London), 340: 487-488.
67. Schroth, G.P., Gottesfeld, J.M., and Bradbury, E.M. 1991. TFIIIA induced DNA bending: effect of low ionic strength electrophoresis buffer conditions. Nucleic Acids Res. 19: 511-516.
68. Segall, J., Matsui, R.G., and Roeder, R.G. 1980. Multiple factors are required for the accurate transcription of purified genes by RNA polymerase III. J. Biol. Chem. 255: 11 986-11 991.
69. Sera, T., and Wolffe, A.P. 1998. Role of histone H1 as an architectural determinant of chromatin structure and as a specific repressor of transcription on Xenopus oocyte 5S rRNA genes. Mol. Cell. Biol. 18: 3668-3680.
70. Setzer, D.R., and Brown, D.D. 1985. Formation and stability of the 5S RNA transcription Complex. J. Biol. Chem. 260: 2483-2492.
71. Shastry, B.S., Ng, S.-Y., and Roeder, R.G. 1982. Multiple factors involved in the transcription of class III genes in Xenopus laevis. J. Biol. Chem. 257: 12 979-12 986.
72. Shimamura, A., Tremethick, D., and Worcel, A. 1988. Characterization of the repressed 5S DNA minichromosomes assembled in vitro with a high-speed supernatant of Xenopus laevis oocytes. Mol. Cell. Biol. 8: 4257-4269.
73. Simpson, R.T. 1986. Nucleosome positioning in vivo and in vitro. Bioessays, 4: 172-176.
74. Smith, D.R., Jackson, I.J., and Brown, D.D. 1984. Domains of the positive transcription factor specific for the Xenopus 5S RNA gene. Cell, 37: 645-652.
75. Taylor, W., Jackson, I.J., Siegel, N., Kumar, A., and Brown, D. 1986. The developmental expression of the gene for TFIIIA in Xenopus laevis. Nucleic Acids Res. 14: 6185-6195.
76. Thiriet, C., and Hayes, J.J. 1998. Functionally relevant histone-DNA interactions extend beyond the classically defined nucleosome core region. J. Biol. Chem. 273: 21 352-21 358.
77. Tremethick, D., Zucker, K., and Worcel, A. 1990. The transcription complex of the 5 S RNA gene, but not transcription factor IIIA alone, prevents nucleosomal repression of transcription. J. Biol. Chem. 265: 5014-5023.
78. Vitolo, J.M., Thiriet, C., and Hayes, J.J. 2000. The H3-H4 N-terminal tail domains are the primary mediators of transcription factor IIIA access to 5S DNA within a nucleosome. Mol. Cell. Biol. 20: 2167-2175.
79. Vrana, K.E., Churchill, M.E., Tullius, T.D., and Brown, D.D. 1988. Mapping functional regions of transcription factor TFIIIA. Mol. Cell. Biol. 8: 1684-1696.
80. Wegnez, M., Monier, R., and Denis, H. 1972. FEBS Lett. 25: 13-17.
81. Wolfe, S.A., Nekludova, L., and Pabo, C.O. 2000. DNA recognition by Cys2His2 zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 29: 183-212.
82. Wolffe, A.P. 1988. Transcription fraction TFIIIC can regulate differential Xenopus 5S RNA gene transcription in vitro. EMBO J. 7: 1071-1079.
83. Wolffe, A.P., and Brown, D.D. 1986. DNA replication in vitro erases a Xenopus 5S RNA gene transcription complex. Cell, 47: 217-227.
84. Wolffe, A.P., and Brown, D.D. 1988. Developmental regulation of two 5S ribosomal RNA genes. Science, 241: 1626-1632.
85. Wolffe, A.P., and Morse, R.H. 1990. The transcription complex of the Xenopus somatic 5 S RNA gene. A functional analysis of protein-DNA interactions outside of the internal control region. J. Biol. Chem. 265: 4592-4599.
86. Wolffe, A.P., Jordan, E., and Brown, D.D. 1986. A bacteriophage RNA polymerase transcribes through a Xenopus 5S RNA gene transcription complex without disrupting it. Cell, 44: 381-389.
87. Wormington, W.M., Bogenhagen, D.F., Jordan, E., and Brown, D.D. 1981. A Quantitative Assay for Xenopus 5S RNA Gene Transcription in Vitro. Cell, 24: 809-817.
88. Wu, H., Yang, W.P., and Barbas, C.F., 3rd. 1995. Building zinc fingers by selection: toward a therapeutic application. Proc. Natl. Acad. Sci. U.S.A. 92: 344-348.
89. Wuttke, D.S., Foster, M.P., Case, D.A., Gottesfeld, J.M., and Wright, P.E. 1997. Solution structure of the first three zinc fingers of TFIIIA bound to the cognate DNA sequence: determinants of affinity and sequence specificity. J. Mol. Biol. 273: 183-206.