Characterization of structural features important for T7 RNAP elongation complex stability reveals competing complex conformations and a role for the non-template strand in RNA displacement

Journal of Molecular Biology

Volumn 290, Issue 2, 1999, Pages 411-431

  Gopal, Vijaya ^a   Brieba, Luis G ^a   Guajardo, Richard ^a   McAllister, William T ^b   Sousa, Rui ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b SUNY DOWNSTATE MEDICAL CENTER   (United States)

Author keywords

Elongation complex; Processivity; RNA:DNA hybrid; T7 RNA polymerase; Transcription

Indexed keywords

RNA POLYMERASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIOPHAGE T7; DISSOCIATION; ENZYME MODIFICATION; ENZYME STRUCTURE; MOLECULAR INTERACTION; MOLECULAR STABILITY; PRIORITY JOURNAL; RNA BINDING;

UNIDENTIFIED BACTERIOPHAGE;

EID: 0033538419     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2836     Document Type: Article

References (67)

1. Baker T. A., Kornberg A. Transcriptional activation of replication from the E. coli chromosomal origin: an RNA-DNA hybrid near oriC. Cell. 55:1988;113-123.
2. Bonner G., Lafer E. M., Sousa R. The thumb subdomain of T7 RNAP functions to stabilize the ternary complex during processive transcription. J. Biol. Chem. 42:1994;25129-25136.
3. Carpousis A. J., Stefano J. E., Gralla J. D. 5′ nucleotide heterogeneity and altered initiation of transcription at mutant lac promoters. J. Mol. Biol. 157:1982;619-633.
4. Cazenave C., Uhlnebeck O. C. RNA template-directed RNA synthesis by T7 RNA polymerase. Proc. Natl Acad. Sci. USA. 91:1994;6972-6976.
5. Choder M., Aloni Y. RNA polymerase II allows unwinding and rewinding of the DNA and thus maintains a constant length of the transcription bubble. J. Biol. Chem. 263:1988;12994-13002.
6. Darst S. A., Edwards A. M., Kubalek E. W., Kornberg R. D. Three-dimensional structure of Escherichia coli RNA polymerase holoenzyme determined by electronic crystallography. Nature. 340:1989;730-732.
7. Darst S. A., Kubalek E. W., Edwards A. M., Kornberg R. D. Three-dimensional structure of yeast RNA polymerase II at 16 Å resolution. Cell. 66:1991;121-128.
8. Daube S. S., von Hippel P. H. RNA displacement pathways during transcription from synthetic RNA-DNA bubble duplexes. Biochemistry. 33:1994;340-347.
9. Diaz G. A., Rong M., McAllister W. T., Durbin R. K. The stability of abortively cycling T7 RNA polymerase complexes depends upon template conformation. Biochemistry. 35:1996;10837-10843.
10. Donner G., Patra D., Lafer E. M., Soussa R. Mutations in T7 RNA polymerase which support the proposal for a common polymerase active site structure. EMBO J. 11:1992;3767-3775.
11. Drolet M., Phoenix P., Menzel R., Masse E., Liu L. F., Crouch R. J. Overexpression of RNase H partially complements the growth defect of an Escherichia coli DtopA mutant: R-loop formation is a major problem in the absence of topoisomerase I. Proc. Natl Acad. Sci. USA. 92:1995;3526-3530.
12. Erie D. A., Hajiseyedjavadi O., Young M. C., von Hippel P. H. Multiple RNA polymerase conformations and GreA: control of the fidelity of transcription. Science. 262:1993;867-873.
13. Fuller C. W., Richardson C. C. Initiation of DNA replication at the primary origin of bacteriophage T7 by purified proteins. J. Biol. Chem. 260:1985;3185-3196.
14. Gaal T., Bartlett M., Ross W., Turnbough C. L. Jr, Gourse R. NTP concentration as a regulator of transcription initiation: control of rRNA synthesis in bacteria. Science. 278:1997;2092-2097.
15. Grabczyk E., Fishman M. C. A long purine-pyrimidine homopolymer acts as a transcriptional diode. J. Biol. Chem. 270:1995;1791-1797.
16. Gross L., Chen W., McAllister W. T. Characterization of bacteriophage T7 RNA polymerase by linker insertion mutagenesis. J. Mol. Biol. 228:1992;488-505.
17. Guajardo R., Lopez P. J., Dreyfus M., Sousa R. NTP concentration effects during initial transcription by T7 RNA polymerase indicate that translocation occurs by passive sliding and reveal that divergent promoters have distinct NTP concentration requirements for productive initiation. J. Mol. Biol. 281:1998;777-792.
18. Hartvig L., Christiansen J. Intrinsic termination of T7 RNA polymerase mediated by either RNA or DNA. EMBO J. 15:1996;4767-4774.
19. Hayashi M. A DNA-RNA complex as an intermediate of in vitro genetic transcription. Proc. Natl Acad. Sci. USA. 54:1965;1736-1743.
20. He B., Rong M., Durbin R. K., McAllister W. T. A mutant T7 RNA polymerase that is defective in RNA binding and blocked in the early stages of transcription. J. Mol. Biol. 265:1997;275-288.
21. He B., Kukarin A., Temiakov D., Chin-Bow S. T., Lyakhov D. L., Rong M., Durbin R. K., McAllister W. T. Characterization of an unusual, sequence-specific termination signal for T7 RNA polymerase. J. Biol. Chem. 273:1998;18802-18811.
22. Huang Y., Padilla R., Eckstein F., Sousa R. The Mechanism of ribose 2′-group discrimination by an RNA polymerase. Biochemistry. 36:1997a;8231-8242.
23. ++and dNMP incorporation into transcripts. Biochemistry. 36:1997b;13718-13728.
24. Hung S. C., Gottesman M. E. The NUN protein of bacteriophage HK022 inhibits translocation of Escherichia coli RNA polymerase without abolishing its catalytic activities. Genes Dev. 11:1997;2670-2678.
25. Ikeda R. A., Richardson C. C. Interactions of the RNA polymerase of bacteriophage T7 with its promoter during binding and initiation of transcription. Proc. Natl Acad. Sci. USA. 83:1986;3614-3618.
26. Ikeda R. A., Richardson C. C. Enzymatic properties of a proteolytically nicked RNA polymerase of bacteriophage T7. J. Biol. Chem. 262:1987;3790-3799.
27. Jeng S. T., Gardner J. F., Gumport R. I. Transcription termination by bacteriophage T7 RNA polymerase at Rho-independent terminators. J. Biol. Chem. 265:1990;3823-3830.
28. Jia Y., Patel S. S. Kinetic mechanism of transcription initiation by bacteriophage T7 RNA polymerase. Biochemistry. 36:1997;4223-4232.
29. Kane C. M. Renaturase and ribonuclease H: a novel mechanism that influences transcript displacement by RNA polymerase II in vitro. Biochemistry. 27:1988;3187-3196.
30. Kiyami R., Oishi M. In vitro transcription of a poly(dA)·poly(dT)-containing sequence is inhibited by interaction between the template and its transcripts. Nucl. Acids Res. 24:1996;4577-4583.
31. Komissarova N., Kashlev M. Transcriptional arrest: Escherichia coli RNA polymerase translocates backward, leaving the 3′-end of the RNA intact and extruded. Proc. Natl Acad. Sci. USA. 94:1997;1755-1760.
32. Krasilnikova M. M., Samadashwily G. M., Krasilnikov A. S., Mirkin S. M. Transcription through a simple DNA repeat blocks replication elongation. EMBO J. 17:1998;5095-5102.
33. Kumar A., Patel S. S. Inhibition of T7 RNA polymerase transcription initiation and transition from initiation to elongation are inhibited by T7 lysozyme via a ternary complex with RNA polymerase and promoter DNA. Biochemistry. 36:1997;13954-13962.
34. Landick R. RNA polymerase slides home: pause and termination site recognition. Cell. 88:1997;741-744.
35. Lebowitz P., Bloodgood R. Transcription of simian virus 40 DNA by Escherichia coli RNA polymerase: synthesis of a DNA-RNA hybrid and discrete RNAs under restrictive transcription condition. J. Mol. Biol. 94:1975;183-201.
36. Lee D. Y., Clayton D. A. Properties of a primer RNA-DNA hybrid at the mouse mitochondrial DNA leading-strand origin of replication. J. Biol. Chem. 271:1996;24262-24269.
37. Lilley D. M. J., Houghton M. The interaction of RNA polymerase II from wheat germ with supercoiled and linear templates. Nucl. Acids Res. 6:1979;507-523.
38. Lyakhov D. L., He B., Zhang X., Studier F. W., Dunn J. J., McAllister W. T. Mutant bacteriophage T7 RNA polymerases with altered termination properties. J. Mol. Biol. 269:1997;28-40.
39. Martin C. T., Coleman J. E. Kinetic Analysis of T7 RNA polymerase-promoter interactions with small synthetic promoters. Biochemistry. 26:1987;2690-2696.
40. Martin C. T., Muller D. K., Coleman J. E. Processivity in early stages of transcription by T7 RNA polymerase. Biochemistry. 27:1988;3966-3974.
41. Masukata H., Tomizawa J. A mechanism for formation of a persistent hybrid between elongating RNA and template DNA. Cell. 62:1990;331-338.
42. McAllister W. T. Transcription by T7 RNA polymerase. Eckstein F., Lilley D. M. J. Mechanisms of Transcription. 1997;Springer-Verlag, Berlin.
43. Mead D. A., Skorupa E. S., Kemper B. S. S. DNA 'blue' promoter plasmids: a versatile tandem promoter system for cloning and protein engineering. Protein Eng. 1:1986;67-74.
44. Mingot F., Jorcano J. J., Davila C. A. Titel. Biochem. Biophys. Acta. 520:1978;1-10.
45. Muller D., Martin C. T., Coleman J. E. Processivity of proteolytically modified forms of T7 RNA polymerase. Biochemistry. 27:1988;5763-5771.
46. Nudler E., Mustaev A., Lukhtanov E., Goldfarb A. The RNA-DNA hybrid maintains the register of transcription by preventing backtracking of RNA polymerase. Cell. 89:1997;33-41.
47. Patra D., Lafer E. M., Sousa R. Isolation and characterization of mutant bacteriophage T7 RNA polymerases. J. Mol. Biol. 224:1992;307-318.
48. Polyakov A., Severinova E., Darst S. A. Three-dimensional structure of E. coli core RNA polymerase: promoter binding and elongation conformations of the enzyme. Cell. 83:1995;365-373.
49. Reaban M. E., Griffin J. A. Induction of RNA-stabilized DNA conformers by transcription of an immunoglobulin switch region. Nature. 348:1990;342-344.
50. Reaban M. E., Lebowitz J., Griffin J. A. Transcription induces the formation of a stable RNA:DNA hybrid in the immunoglobulin A switch region. J. Biol. Chem. 269:1994;21850-21875.
51. Richardson J. P. Attachment of nascent RNA molecules to superhelical DNA. J. Mol. Biol. 98:1975;565-579.
52. Roberts R. W., Crothers D. M. Stability and properties of double and triple helices: dramatic effects of RNA or DNA backbone composition. Science. 258:1992;1463-1465.
53. Rong M., Durbin R. K., McAllister W. T. Template strand switching by T7 RNA polymerase. J. Biol. Chem. 273:1998;10253-10260.
54. Sastry S., Ross B. M. RNA-binding site in T7 RNA polymerase. Proc. Natl Acad. Sci. USA. 95:1998;9111-9116.
55. Sousa R. Fundamental aspects of T7 RNA polymerase structure and mechanism. Eckstein F., Lilley D. M. J. Mechanisms of Transcription. 1997;Springer-Verlag, Berlin.
56. Sousa R., Padilla R. A mutant T7 RNA polymerase as a DNA polymerase. EMBO J. 14:1995;4609-4621.
57. Sousa R., Rose J. P., Chung Y. J., Lafer E. M., Wang B. C. Single crystals of bacteriophage T7 RNA polymerase. Proteins: Struct. Funct. Genet. 5:1989;266-270.
58. Sousa R., Patra D., Lafer E. M. Model for the mechanism of bacteriophage T7 RNAP transcription initiation and termination. J. Mol. Biol. 224:1992;319-334.
59. Sousa R., Chung Y. J., Rose J. P., Wang B. C. Crystal structure of bacteriophage T7 RNA polymerase at 3.3 resolution. Nature. 364:1993;593-599.
60. Sousa R., Rose J. P., Wang B. C. The thumb's knuckle. Flexibility in the thumb subdomain of T7 RNA polymerase is revealed by the structure of a chimeric T7/T3 RNA polymerase. J. Mol. Biol. 244:1994;6-12.
61. Tabor S., Richardson C. C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl Acad. Sci. USA. 82:1985;1074-1078.
62. Tomizawa J. I., Masukata H. Factor independent termination of transcription in a stretch of deoxyadenosine residues in the template DNA. Cell. 51:1987;623-630.
63. Tsao Y. P., Wu H.-Y., Liu L. F. Transcription-driven supercoiling of DNA: direct biochemical evidence from in vitro studies. Cell. 56:1989;111-118.
64. Tyagarajan K., Monforte J. A., Hearst J. E. RNA folding during transcription by T7 RNA polymerase analyzed using the self-cleaving transcript assay. Biochemistry. 30:1991;6920-6924.
65. Villemain J., Guajardo R., Sousa R. J. Role of open complex instability in kinetic promoter selection by T7 RNA polymerase. J. Mol. Biol. 273:1997;956-975.
66. Wilson K. S., von Hippel P. H. Stability of Escherichia coli TCs near an intrinsic terminator. J. Mol. Biol. 244:1994;36-51.
67. Xu B., Clayton D. A. A persistent RNA-DNA hybrid is formed during transcription at a phylogenetically conserved mitochondrial DNA sequence. Mol. Cell. Biol. 15:1995;580-589.