The mechanism of transcriptional activation by the topologically DNA-linked sliding clamp of bacteriophage T4

Journal of Molecular Biology

Volumn 321, Issue 5, 2002, Pages 767-784

  Kolesky, Scott E ^a   Ouhammouch, Mohamed ^a   Peter Geiduschek, E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Co activators; Phage T4; Promoter opening; Replication transcription coupling; Transcriptional activators

Indexed keywords

EPITOPE; GLYCOPROTEIN; GLYCOPROTEIN GP 45; GLYCOPROTEIN GP 55; HOLOENZYME; MEGALIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIOPHAGE T4; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; DNA BINDING; HEAT SENSITIVITY; LOW TEMPERATURE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INTERACTION; TEMPERATURE DEPENDENCE; TRANSCRIPTION INITIATION;

EID: 0036382847     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)00732-5     Document Type: Article

References (69)

1. Kassavetis, G. A., Elliott, T., Rabussay, D. P. & Geiduschek, E. P. (1983). Initiation of transcription at phage T4 late promoters with purified RNA polymerase. Cell, 33, 887-897.
2. Williams, K. P., Herendeen, D. R., Kassavetis, G. A. & Geiduschek, E. P. (1994). Regulation of late gene expression. In Molecular Biology of Bacteriophage T4 (Karam, J. D., ed.), 2nd edit., pp. 161-175, American Society for Microbiology, Washington, DC.
3. Geiduschek, E. P., Fu, T.-J., Kassavetis, G. A., Sanders, G. M. & Tinker-Kulberg, R. L. (1997). Transcriptional activation by a topologically linkable protein: forging a connection between replication and gene activity. In Nucleic Acids and Molecular Biology (Eckstein, F. & Lilley, D. M. J., eds), vol. 11, pp. 135-150, Springer, Heidelberg.
4. Epstein, R. H., Bolle, A., Steinberg, C., Kellenberger, E., Boy de la Tour, E. et al. (1964). Physiological studies of conditional lethal mutants of bacteriophage T4D. Cold Spring Harbor Symp. Quant. Biol. 28, 375-392.
5. Williams, K. P., Müller, R., Rüger, W. & Geiduschek, E. P. (1989). The overproduced bacteriophage T4 gene 33 protein binds RNA polymerase. J. Bacteriol. 171, 3579-3582.
6. Herendeen, D. R., Williams, K. P., Kassavetis, G. A. & Geiduschek, E. P. (1990). An RNA polymerase-binding protein that is required for communication between an enhancer and a promoter. Science, 248, 573-578.
7. Winkelman, J. W., Kassavetis, G. A. & Geiduschek, E. P. (1994). Molecular genetic analysis of a prokaryotic transcriptional coactivator: functional domains of the bacteriophage T4 gene 33 protein. J. Bacteriol. 176, 1164-1171.
8. Adelman, K., Orsini, G., Kolb, A., Graziani, L. & Brody, E. N. (1997). The interaction between the AsiA protein of bacteriophage T4 and the sigma70 subunit of Escherichia coli RNA polymerase. J. Biol. Chem. 272, 27435-27443.
9. Adelman, K., Brody, E. N. & Buckle, M. (1998). Stimulation of bacteriophage T4 middle transcription by the T4 proteins MotA and AsiA occurs at two distinct steps in the transcription cycle. Proc. Natl Acad. Sci. USA, 95, 15247-15252.
10. Colland, F., Orsini, G., Brody, E. N., Buc, H. & Kolb, A. (1998). The bacteriophage T4 AsiA protein: a molecular switch for sigma 70-dependent promoters. Mol. Microbiol. 27, 819-829.
11. Hinton, D. M., March-Amegadzie, R., Gerber, J. S. & Sharma, M. (1996). Characterization of pre-transcription complexes made at a bacteriophage T4 middle promoter: involvement of the T4 MotA activator and the T4 AsiA protein, a sigma 70 binding protein, in the formation of the open complex. J. Mol. Biol. 256, 235-248.
12. Ouhammouch, M., Adelman, K., Harvey, S. R., Orsini, G. & Brody, E. N. (1995). Bacteriophage T4 MotA and AsiA proteins suffice to direct Escherichia coli RNA polymerase to initiate transcription at T4 middle promoters. Proc. Natl Acad. Sci. USA, 92, 1451-1455.
13. Willy, P. J., Kobayashi, R. & Kadonaga, J. T. (2000). A basal transcription factor that activates or represses transcription. Science, 290, 982-984.
14. Fry, C. J. & Farnham, P. J. (1999). Context-dependent transcriptional regulation. J. Biol. Chem. 274, 29583-29586.
15. Jones, K. A. & Kadonaga, J. T. (2000). Exploring the transcription-chromatin interface. Genes Dev. 14, 1992-1996.
16. Kuriyan, J. & O'Donnell, M. (1993). Sliding clamps of DNA polymerases. J. Mol. Biol. 234, 915-925.
17. Hingorani, M. M. & O'Donnell, M. (2000). Sliding clamps: a (tail)ored fit. Curr. Biol. 10, R25-R29.
18. Jarvis, T. C., Paul, L. S. & von Hippel, P. H. (1989). Structural and enzymatic studies of the T4 DNA replication system. I. Physical characterization of the polymerase accessory protein complex. J. Biol. Chem. 264, 12709-12716.
19. Capson, T. L., Benkovic, S. J. & Nossal, N. G. (1991). Protein DNA cross-linking demonstrates stepwise ATP-dependent assembly of T4-DNA polymerase and its accessory proteins on the primer-template. Cell, 65, 249-258.
20. Yao, N., Turner, J., Kelman, Z., Stukenberg, P. T., Dean, F., Shechter, D. et al. (1996). Clamp loading, unloading and intrinsic stability of the PCNA, beta and gp45 sliding clamps of human, E. coli and T4 replicases. Genes Cells, 1, 101-113.
21. Stukenberg, P. T., Studwell-Vaughan, P. S. & O'Donnell, M. (1991). Mechanism of the sliding beta-clamp of DNA polymerase III holoenzyme. J. Biol. Chem. 266, 11328-11334.
22. Hingorani, M. M., Bloom, L. B., Goodman, M. F. & O'Donnell, M. (1999). Division of labor-sequential ATP hydrolysis drives assembly of a DNA polymerase sliding clamp around DNA. EMBO J. 18, 5131-5144.
23. Latham, G. J., Dong, F., Pietroni, P., Dozono, J. M., Bacheller, D. J. & von Hippel, P. H. (1999). Opening of a monomer-monomer interface of the trimeric bacteriophage T4-coded GP45 sliding clamp is required for clamp loading onto DNA. Proc. Natl Acad. Sci. USA, 96, 12448-12453.
24. Bertram, J. G., Bloom, L. B., Hingorani, M. M., Beechem, J. M., O'Donnell, M. & Goodman, M. F. (2000). Molecular mechanism and energetics of clamp assembly in Escherichia coli. The role of ATP hydrolysis when gamma complex loads beta on DNA. J. Biol. Chem. 275, 28413-28420.
25. Kong, X. P., Onrust, R., O'Donnell, M. & Kuriyan, J. (1992). Three-dimensional structure of the beta subunit of E. coli DNA polymerase III holoenzyme: a sliding DNA clamp. Cell, 69, 425-437.
26. Krishna, T. S., Kong, X. P., Gary, S., Burgers, P. M. & Kuriyan, J. (1994). Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell, 79, 1233-1243.
27. Moarefi, I., Jeruzalmi, D., Turner, J., O'Donnell, M. & Kuriyan, J. (2000). Crystal structure of the DNA polymerase processivity factor of T4 bacteriophage. J. Mol. Biol. 296, 1215-1223.
28. Shamoo, Y. & Steitz, T. A. (1999). Building a replisome from interacting pieces: sliding clamp complexed to a peptide from DNA polymerase and a polymerase editing complex. Cell, 99, 155-166.
29. Alley, S. C., Abel-Santos, E. & Benkovic, S. J. (2000). Tracking sliding clamp opening and closing during bacteriophage T4 DNA polymerase holoenzyme assembly. Biochemistry, 39, 3076-3090.
30. Trakselis, M. A., Alley, S. C., Abel-Santos, E. & Benkovic, S. J. (2001). Creating a dynamic picture of the sliding clamp during T4 DNA polymerase holoenzyme assembly by using fluorescence resonance energy transfer. Proc. Natl Acad. Sci. USA, 98, 8368-8375.
31. Pietroni, P., Young, M. C., Latham, G. J. & von Hippel, P. H. (2001). Dissection of the ATP-driven reaction cycle of the bacteriophage T4 DNA replication processivity clamp loading system. J. Mol. Biol. 309, 869-891.
32. Alley, S. C., Shier, V. K., Abel-Santos, E., Sexton, D. J., Soumillion, P. & Benkovic, S. J. (1999). Sliding clamp of the bacteriophage T4 polymerase has open and closed subunit interfaces in solution. Biochemistry, 38, 7696-7709.
33. Fu, T.-J., Sanders, G. M., O'Donnell, M. & Geiduschek, E. P. (1996). Dynamics of DNA-tracking by two sliding-clamp proteins. EMBO J. 15, 4414-4422.
34. Tinker, R. L., Williams, K. P., Kassavetis, G. A. & Geiduschek, E. P. (1994). Transcriptional activation by a DNA-tracking protein: structural consequences of enhancement at the T4 late promoter. Cell, 77, 225-237.
35. Munn, M. M. & Alberts, B. M. (2002). The T4 DNA polymerase accessory proteins form an ATP-dependent complex on a primer-template junction. J. Biol. Chem. 266, 4-20033.
36. Berdis, A. J., Soumillion, P. & Benkovic, S. J. (1996). The carboxyl terminus of the bacteriophage T4 DNA polymerase is required for holoenzyme complex formation. Proc. Natl Acad. Sci. USA, 93, 12822-12827.
37. Sanders, G. M., Kassavetis, G. A. & Geiduschek, E. P. (1997). Dual targets of a transcriptional activator that tracks on DNA. EMBO J. 16, 3124-3132.
38. Wong, K. & Geiduschek, E. P. (1998). Activator-sigma interaction: a hydrophobic segment mediates the interaction of a sigma family promoter recognition protein with a sliding clamp transcription activator. J. Mol. Biol. 284, 195-203.
39. Alley, S. C., Jones, A. D., Soumillion, P. & Benkovic, S. J. (1999). The carboxyl terminus of the bacteriophage T4 DNA polymerase contacts its sliding clamp at the subunit interface. J. Biol. Chem. 274, 24485-24489.
40. Herendeen, D. R., Kassavetis, G. A. & Geiduschek, E. P. (1992). A transcriptional enhancer whose function imposes a requirement that proteins track along DNA. Science, 256, 1298-1303.
41. Tinker, R. L., Kassavetis, G. A. & Geiduschek, E. P. (1994). Detecting the ability of viral, bacterial and eukaryotic replication proteins to track along DNA. EMBO J. 13, 5330-5337.
42. Tinker-Kulberg, R. L., Fu, T. J., Geiduschek, E. P. & Kassavetis, G. A. (1996). A direct interaction between a DNA-tracking protein and a promoter recognition protein: implications for searching DNA sequence. EMBO J. 15, 5032-5039.
43. Malik, S. & Goldfarb, A. (1988). Late sigma factor of bacteriophage T4. Formation and properties of RNA polymerase-promoter complexes. J. Biol. Chem. 263, 1174-1181.
44. Fu, T.-J., Geiduschek, E. P. & Kassavetis, G. A. (1998). Abortive initiation of transcription at a hybrid promoter. An analysis of the sliding clamp activator of bacteriophage T4 late transcription, and a comparison of the sigma70 and T4 gp55 promoter recognition proteins. J. Biol. Chem. 273, 34042-34048.
45. Nossal, N. G. (1994). The bacteriophage T4 DNA replication fork. In Molecular Biology of Bacteriophage T4 (Karam, J. D., ed.), 2nd edit., pp. 43-53, ASM Press, Washington, DC.
46. deHaseth, P. L., Lohman, T. M., Burgess, R. R. & Record, M. T., Jr (1978). Nonspecific interactions of Escherichia coli RNA polymerase with native and denatured DNA: differences in the binding behavior of core and holoenzyme. Biochemistry, 17, 1612-1622.
47. Saecker, R. M., Tsodikov, O. V., McQuade, K. L., Schlax, P. E., Capp, M. W. & Record, M. T. (2002). Kinetic studies and structural models of the association of E. coli sigma 70 RNA polymerase with the phage PR promoter: large scale conformational changes in forming the kinetically-significant intermediates. J. Mol. Biol. 319, 649-671.
48. Buckle, M., Pemberton, I. K., Jacquet, M. A. & Buc, H. (1999). The kinetics of sigma subunit directed promoter recognition by E. coli RNA polymerase. J. Mol. Biol. 285, 955-964.
49. McClure, W. R. (1980). Rate-limiting steps in RNA chain initiation. Proc. Natl Acad. Sci. USA, 77, 5634-5638.
50. Craig, M. L., Tsodikov, O. V., McQuade, K. L., Schlax, P. E., Capp, M. W., Saecker, R. M. & Record, M. T. (1998). DNA footprints of the two kinetically significant intermediates in formation of an RNA polymerase-promoter open complex: evidence that interactions with start site and downstream DNA induce sequential conformational changes in poly-merase and DNA. J. Mol. Biol. 283, 741-756.
51. Spassky, A., Kirkegaard, K. & Buc, H. (1985). Changes in the DNA structure of the lac UV5 promoter during formation of an open complex with Escherichia coli RNA polymerase. Biochemistry, 24, 2723-2731.
52. Tsodikov, O. V., Craig, M. L., Saecker, R. M. & Record, M. T. (1998). Quantitative analysis of multiple-hit footprinting studies to characterize DNA conformational changes in protein-DNA complexes: application to DNA opening by E sigma(70) RNA polymerase. J. Mol. Biol. 283, 757-769.
53. Cowing, D. W., Mecsas, J., Record, M. T., Jr & Gross, C. A. (1989). Intermediates in the formation of the open complex by RNA polymerase holoenzyme containing the sigma factor sigma 32 at the groE promoter. J. Mol. Biol. 210, 521-530.
54. 70), promoters, and the kinetics of the steps of transcription initiation. In Escherichia coli and Salmonella (Neidhardt, F. C., ed.), 2nd edit., pp. 792-820, ASM Press, Washington, DC.
55. Gribskov, M. & Burgess, R. (1986). Sigma factors from E. coli, B. subtilis, phage SPO1, and phage T4 are homologous proteins. Nucl. Acids Res. 14, 6745-6763.
56. Lonetto, M., Gribskov, M. & Gross, C. A. (1992). The sigma 70 family: sequence conservation and evolutionary relationships. J. Bacteriol. 174, 3843-3849.
57. Sanders, G. M., Kassavetis, G. A. & Geiduschek, E. P. (1995). Rules governing the efficiency and polarity of loading a tracking clamp protein onto DNA: determinants of enhancement in bacteriophage T4 late transcription. EMBO J. 14, 3966-3976.
58. Alley, S. C., Trakselis, M. A., Mayer, M. U., Ishmael, F. T., Jones, A. D. & Benkovic, S. J. (2001). Building a replisome solution structure by elucidation of protein-protein interactions in the bacteriophage T4 DNA polymerase holoenzyme. J. Biol. Chem. 276, 39340-39349.
59. Shao, W. P., Kearns, D. R. & Sanders, G. M. (1997). Secondary structure of T4 gene 33 protein: Fourier transform infrared and circular dichroic spectroscopic studies. Int. J. Biol. Macromol. 20, 115-121.
60. Li, X. Y. & McClure, W. R. (1998). Characterization of the closed complex intermediate formed during transcription initiation by Escherichia coli RNA polymerase. J. Biol. Chem. 273, 23549-23557.
61. Brodolin, K. & Buckle, M. (2001). Differential melting of the transcription start site associated with changes in RNA polymerase-promoter contacts in initiating transcription complexes. J. Mol. Biol. 307, 25-30.
62. Burns, H. D., Belyaeva, T. A., Busby, S. J. W. & Minchin, S. D. (1996). Temperature-dependence of open-complex formation at two Escherichia coli promoters with extended - 10 sequences. Biochem. J. 317, 305-311.
63. Severinov, K. & Darst, S. A. (1997). A mutant RNA polymerase that forms unusual open promoter complexes. Proc. Natl Acad. Sci. USA, 94, 13481-13486.
64. Kolesky, S., Ouhammouch, M., Brody, E. N. & Geiduschek, E. P. (1999). Sigma competition: the contest between bacteriophage T4 middle and late transcription. J. Mol. Biol. 291, 267-281.
65. Williams, K. P., Kassavetis, G. A. & Geiduschek, E. P. (1987). Interactions of the bacteriophage T4 gene 55 product with Escherichia coli RNA polymerase. Competition with Escherichia coli sigma 70 and release from late T4 transcription complexes following initiation. J. Biol. Chem. 262, 12365-12371.
66. Leonetti, J. P., Wong, K. & Geiduschek, E. P. (1998). Core-sigma interaction: probing the interaction of the bacteriophage T4 gene 55 promoter recognition protein with E. coli RNA polymerase core. EMBO J. 17, 1467-1475.
67. Borukhov, S. & Goldfarb, A. (1993). Recombinant Escherichia coli RNA polymerase: purification of individually overexpressed subunits and in vitro assembly. Protein Expr. Purif. 4, 503-511.
68. Williams, K. P., Kassavetis, G. W., Esch, F. S. & Geiduschek, E. P. (1987). Identification of the gene encoding an RNA polymerase-binding protein of bacteriophage T4. J. Virol. 61, 597-599.
69. Elliott, T. & Geiduschek, E. P. (1984). Defining a bacteriophage T4 late promoter: absence of a "-35" region. Cell, 36, 211-219.