Abstract
Bacteriophage T4 gene 45 protein, gp45, serves as the sliding clamp of viral DNA replication and as the activator of T4 late gene transcription. In the latter context, DNA tracking is an essential feature of the unique mechanism of action. T4 late promoters, which consist of a simple TATA box, TATAAATA, are recognized by the small sigma-family gene 55 protein, gp55, which binds to Escherichia coli RNA polymerase core. A direct and RNA polymerase-independent interaction of gp45 with gp55 has been demonstrated in two ways. (i) gp45 tracks along DNA; co-tracking of gp55 requires the previously documented DNA-loading process of gp45, and can be detected by photochemical crosslinking. (ii) The dynamics of DNA tracking by gp45 can be followed by footprinting; the catenated DNA-tracking state of gp45 is short-lived, but is stabilized by gp55. The ability of this topologically linked DNA-tracking transcriptional activator to interact directly with a promoter recognition protein suggests the existence of multiple pathways of promoter location, which are discussed.
Full text
PDF







Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Alberts B. M., Barry J., Bedinger P., Formosa T., Jongeneel C. V., Kreuzer K. N. Studies on DNA replication in the bacteriophage T4 in vitro system. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 2):655–668. doi: 10.1101/sqb.1983.047.01.077. [DOI] [PubMed] [Google Scholar]
- Alberts B. M. Prokaryotic DNA replication mechanisms. Philos Trans R Soc Lond B Biol Sci. 1987 Dec 15;317(1187):395–420. doi: 10.1098/rstb.1987.0068. [DOI] [PubMed] [Google Scholar]
- Bartholomew B., Kassavetis G. A., Braun B. R., Geiduschek E. P. The subunit structure of Saccharomyces cerevisiae transcription factor IIIC probed with a novel photocrosslinking reagent. EMBO J. 1990 Jul;9(7):2197–2205. doi: 10.1002/j.1460-2075.1990.tb07389.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bartholomew B., Tinker R. L., Kassavetis G. A., Geiduschek E. P. Photochemical cross-linking assay for DNA tracking by replication proteins. Methods Enzymol. 1995;262:476–494. doi: 10.1016/0076-6879(95)62039-7. [DOI] [PubMed] [Google Scholar]
- Brody E. N., Kassavetis G. A., Ouhammouch M., Sanders G. M., Tinker R. L., Geiduschek E. P. Old phage, new insights: two recently recognized mechanisms of transcriptional regulation in bacteriophage T4 development. FEMS Microbiol Lett. 1995 Apr 15;128(1):1–8. doi: 10.1111/j.1574-6968.1995.tb07491.x. [DOI] [PubMed] [Google Scholar]
- Capson T. L., Benkovic S. J., Nossal N. G. Protein-DNA cross-linking demonstrates stepwise ATP-dependent assembly of T4 DNA polymerase and its accessory proteins on the primer-template. Cell. 1991 Apr 19;65(2):249–258. doi: 10.1016/0092-8674(91)90159-v. [DOI] [PubMed] [Google Scholar]
- Coppo A., Manzi A., Pulitzer J. F. Host mutant (tabD)-induced inhibition of bacteriophage T4 late transcription. II. Genetic characterization of mutants. J Mol Biol. 1975 Aug 25;96(4):601–624. doi: 10.1016/0022-2836(75)90141-2. [DOI] [PubMed] [Google Scholar]
- Fu T. J., Sanders G. M., O'Donnell M., Geiduschek E. P. Dynamics of DNA-tracking by two sliding-clamp proteins. EMBO J. 1996 Aug 15;15(16):4414–4422. [PMC free article] [PubMed] [Google Scholar]
- Green M. R. Cellular and viral transcriptional activators. Harvey Lect. 1992 1993;88:67–96. [PubMed] [Google Scholar]
- Herendeen D. R., Kassavetis G. A., Barry J., Alberts B. M., Geiduschek E. P. Enhancement of bacteriophage T4 late transcription by components of the T4 DNA replication apparatus. Science. 1989 Sep 1;245(4921):952–958. doi: 10.1126/science.2672335. [DOI] [PubMed] [Google Scholar]
- Herendeen D. R., Kassavetis G. A., Geiduschek E. P. A transcriptional enhancer whose function imposes a requirement that proteins track along DNA. Science. 1992 May 29;256(5061):1298–1303. doi: 10.1126/science.1598572. [DOI] [PubMed] [Google Scholar]
- Herendeen D. R., Williams K. P., Kassavetis G. A., Geiduschek E. P. An RNA polymerase-binding protein that is required for communication between an enhancer and a promoter. Science. 1990 May 4;248(4955):573–578. doi: 10.1126/science.2185541. [DOI] [PubMed] [Google Scholar]
- Hockensmith J. W., Kubasek W. L., Evertsz E. M., Mesner L. D., von Hippel P. H. Laser cross-linking of proteins to nucleic acids. II. Interactions of the bacteriophage T4 DNA replication polymerase accessory proteins complex with DNA. J Biol Chem. 1993 Jul 25;268(21):15721–15730. [PubMed] [Google Scholar]
- Johanson K. O., Haynes T. E., McHenry C. S. Chemical characterization and purification of the beta subunit of the DNA polymerase III holoenzyme from an overproducing strain. J Biol Chem. 1986 Sep 5;261(25):11460–11465. [PubMed] [Google Scholar]
- Kabata H., Kurosawa O., Arai I., Washizu M., Margarson S. A., Glass R. E., Shimamoto N. Visualization of single molecules of RNA polymerase sliding along DNA. Science. 1993 Dec 3;262(5139):1561–1563. doi: 10.1126/science.8248804. [DOI] [PubMed] [Google Scholar]
- Kelman Z., O'Donnell M. DNA polymerase III holoenzyme: structure and function of a chromosomal replicating machine. Annu Rev Biochem. 1995;64:171–200. doi: 10.1146/annurev.bi.64.070195.001131. [DOI] [PubMed] [Google Scholar]
- Kong X. P., Onrust R., O'Donnell M., Kuriyan J. Three-dimensional structure of the beta subunit of E. coli DNA polymerase III holoenzyme: a sliding DNA clamp. Cell. 1992 May 1;69(3):425–437. doi: 10.1016/0092-8674(92)90445-i. [DOI] [PubMed] [Google Scholar]
- Krishna T. S., Kong X. P., Gary S., Burgers P. M., Kuriyan J. Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell. 1994 Dec 30;79(7):1233–1243. doi: 10.1016/0092-8674(94)90014-0. [DOI] [PubMed] [Google Scholar]
- Kustu S., North A. K., Weiss D. S. Prokaryotic transcriptional enhancers and enhancer-binding proteins. Trends Biochem Sci. 1991 Nov;16(11):397–402. doi: 10.1016/0968-0004(91)90163-p. [DOI] [PubMed] [Google Scholar]
- Maki S., Kornberg A. DNA polymerase III holoenzyme of Escherichia coli. II. A novel complex including the gamma subunit essential for processive synthesis. J Biol Chem. 1988 May 15;263(14):6555–6560. [PubMed] [Google Scholar]
- Maldonado E., Reinberg D. News on initiation and elongation of transcription by RNA polymerase II. Curr Opin Cell Biol. 1995 Jun;7(3):352–361. doi: 10.1016/0955-0674(95)80090-5. [DOI] [PubMed] [Google Scholar]
- Matsuoka S., Yamaguchi M., Matsukage A. D-type cyclin-binding regions of proliferating cell nuclear antigen. J Biol Chem. 1994 Apr 15;269(15):11030–11036. [PubMed] [Google Scholar]
- Morris C. F., Hama-Inaba H., Mace D., Sinha N. K., Alberts B. Purification of the gene 43, 44, 45, and 62 proteins of the bacteriophage T4 DNA replication apparatus. J Biol Chem. 1979 Jul 25;254(14):6787–6796. [PubMed] [Google Scholar]
- Munn M. M., Alberts B. M. The T4 DNA polymerase accessory proteins form an ATP-dependent complex on a primer-template junction. J Biol Chem. 1991 Oct 25;266(30):20024–20033. [PubMed] [Google Scholar]
- Muskhelishvili G., Travers A. A., Heumann H., Kahmann R. FIS and RNA polymerase holoenzyme form a specific nucleoprotein complex at a stable RNA promoter. EMBO J. 1995 Apr 3;14(7):1446–1452. doi: 10.1002/j.1460-2075.1995.tb07131.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Naktinis V., Turner J., O'Donnell M. A molecular switch in a replication machine defined by an internal competition for protein rings. Cell. 1996 Jan 12;84(1):137–145. doi: 10.1016/s0092-8674(00)81000-4. [DOI] [PubMed] [Google Scholar]
- Reddy M. K., Weitzel S. E., Daube S. S., Jarvis T. C., von Hippel P. H. Using macromolecular crowding agents to identify weak interactions within DNA replication complexes. Methods Enzymol. 1995;262:466–476. doi: 10.1016/0076-6879(95)62038-9. [DOI] [PubMed] [Google Scholar]
- Reddy M. K., Weitzel S. E., von Hippel P. H. Assembly of a functional replication complex without ATP hydrolysis: a direct interaction of bacteriophage T4 gp45 with T4 DNA polymerase. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3211–3215. doi: 10.1073/pnas.90.8.3211. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roberts S. G., Green M. R. Activator-induced conformational change in general transcription factor TFIIB. Nature. 1994 Oct 20;371(6499):717–720. doi: 10.1038/371717a0. [DOI] [PubMed] [Google Scholar]
- Ruusala T., Crothers D. M. Sliding and intermolecular transfer of the lac repressor: kinetic perturbation of a reaction intermediate by a distant DNA sequence. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):4903–4907. doi: 10.1073/pnas.89.11.4903. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sanders G. M., Kassavetis G. A., Geiduschek E. P. Use of a macromolecular crowding agent to dissect interactions and define functions in transcriptional activation by a DNA-tracking protein: bacteriophage T4 gene 45 protein and late transcription. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7703–7707. doi: 10.1073/pnas.91.16.7703. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sauer F., Hansen S. K., Tjian R. Multiple TAFIIs directing synergistic activation of transcription. Science. 1995 Dec 15;270(5243):1783–1788. doi: 10.1126/science.270.5243.1783. [DOI] [PubMed] [Google Scholar]
- Singer P., Wu C. W. Promoter search by Escherichia coli RNA polymerase on a circular DNA template. J Biol Chem. 1987 Oct 15;262(29):14178–14189. [PubMed] [Google Scholar]
- Smith M. L., Chen I. T., Zhan Q., Bae I., Chen C. Y., Gilmer T. M., Kastan M. B., O'Connor P. M., Fornace A. J., Jr Interaction of the p53-regulated protein Gadd45 with proliferating cell nuclear antigen. Science. 1994 Nov 25;266(5189):1376–1380. doi: 10.1126/science.7973727. [DOI] [PubMed] [Google Scholar]
- Struhl K. Yeast transcription factors. Curr Opin Cell Biol. 1993 Jun;5(3):513–520. doi: 10.1016/0955-0674(93)90018-l. [DOI] [PubMed] [Google Scholar]
- Stukenberg P. T., Studwell-Vaughan P. S., O'Donnell M. Mechanism of the sliding beta-clamp of DNA polymerase III holoenzyme. J Biol Chem. 1991 Jun 15;266(17):11328–11334. [PubMed] [Google Scholar]
- Su W., Porter S., Kustu S., Echols H. DNA-looping and enhancer activity: association between DNA-bound NtrC activator and RNA polymerase at the bacterial glnA promoter. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5504–5508. doi: 10.1073/pnas.87.14.5504. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Surby M. A., Reich N. O. Contribution of facilitated diffusion and processive catalysis to enzyme efficiency: implications for the EcoRI restriction-modification system. Biochemistry. 1996 Feb 20;35(7):2201–2208. doi: 10.1021/bi951883n. [DOI] [PubMed] [Google Scholar]
- Tinker R. L., Kassavetis G. A., Geiduschek E. P. Detecting the ability of viral, bacterial and eukaryotic replication proteins to track along DNA. EMBO J. 1994 Nov 15;13(22):5330–5337. doi: 10.1002/j.1460-2075.1994.tb06867.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tinker R. L., Sanders G. M., Severinov K., Kassavetis G. A., Geiduschek E. P. The COOH-terminal domain of the RNA polymerase alpha subunit in transcriptional enhancement and deactivation at the bacteriophage T4 late promoter. J Biol Chem. 1995 Jun 30;270(26):15899–15907. doi: 10.1074/jbc.270.26.15899. [DOI] [PubMed] [Google Scholar]
- Tinker R. L., Williams K. P., Kassavetis G. A., Geiduschek E. P. Transcriptional activation by a DNA-tracking protein: structural consequences of enhancement at the T4 late promoter. Cell. 1994 Apr 22;77(2):225–237. doi: 10.1016/0092-8674(94)90315-8. [DOI] [PubMed] [Google Scholar]
- Waga S., Hannon G. J., Beach D., Stillman B. The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature. 1994 Jun 16;369(6481):574–578. doi: 10.1038/369574a0. [DOI] [PubMed] [Google Scholar]
- Waga S., Stillman B. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature. 1994 May 19;369(6477):207–212. doi: 10.1038/369207a0. [DOI] [PubMed] [Google Scholar]
- Wedel A., Weiss D. S., Popham D., Dröge P., Kustu S. A bacterial enhancer functions to tether a transcriptional activator near a promoter. Science. 1990 Apr 27;248(4954):486–490. doi: 10.1126/science.1970441. [DOI] [PubMed] [Google Scholar]
- Williams K. P., Müller R., Rüger W., Geiduschek E. P. Overproduced bacteriophage T4 gene 33 protein binds RNA polymerase. J Bacteriol. 1989 Jun;171(6):3579–3582. doi: 10.1128/jb.171.6.3579-3582.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Winkelman J. W., Kassavetis G. A., Geiduschek E. P. Molecular genetic analysis of a prokaryotic transcriptional coactivator: functional domains of the bacteriophage T4 gene 33 protein. J Bacteriol. 1994 Feb;176(4):1164–1171. doi: 10.1128/jb.176.4.1164-1171.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xiong Y., Zhang H., Beach D. D type cyclins associate with multiple protein kinases and the DNA replication and repair factor PCNA. Cell. 1992 Oct 30;71(3):505–514. doi: 10.1016/0092-8674(92)90518-h. [DOI] [PubMed] [Google Scholar]
- Yao N., Turner J., Kelman Z., Stukenberg P. T., Dean F., Shechter D., Pan Z. Q., Hurwitz J., O'Donnell M. Clamp loading, unloading and intrinsic stability of the PCNA, beta and gp45 sliding clamps of human, E. coli and T4 replicases. Genes Cells. 1996 Jan;1(1):101–113. doi: 10.1046/j.1365-2443.1996.07007.x. [DOI] [PubMed] [Google Scholar]
- von Hippel P. H., Berg O. G. Facilitated target location in biological systems. J Biol Chem. 1989 Jan 15;264(2):675–678. [PubMed] [Google Scholar]
- von Hippel P. H. Protein-DNA recognition: new perspectives and underlying themes. Science. 1994 Feb 11;263(5148):769–770. doi: 10.1126/science.8303292. [DOI] [PubMed] [Google Scholar]