Unified two-metal mechanism of RNA synthesis and degradation by RNA polymerase

EMBO Journal

Volumn 22, Issue 9, 2003, Pages 2234-2244

  Sosunov, Vasily ^a,b   Sosunova, Ekaterina ^a,c   Mustaev, Arkady ^a   Bass, Irina ^c   Nikiforov, Vadim ^a,c   Goldfarb, Alex ^a  

^a PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

^b ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

^c INSTITUTE OF MOLECULAR GENETICS   (Russian Federation)

Author keywords

Catalytic magnesium; Exonuclease; RNA polymerase; Stimulating NTP; Two metal mechanism

Indexed keywords

DNA DIRECTED RNA POLYMERASE; EXONUCLEASE; MAGNESIUM ION; NUCLEOSIDE TRIPHOSPHATE; PHOSPHATE; RNA POLYMERASE;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME DEGRADATION; ENZYME MECHANISM; ENZYME SUBSTRATE; ENZYME SUBUNIT; HYDROLYSIS; POLYMERIZATION; PRIORITY JOURNAL; RNA SYNTHESIS;

BINDING SITES; CATALYSIS; DNA-DIRECTED RNA POLYMERASES; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; MODELS, MOLECULAR; PYROPHOSPHATASES; RNA;

EID: 0037543997     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg193     Document Type: Article

References (34)

1. Borukhov, S. and Goldfarb, A. (1993) Recombinant Escherichia coli RNA polymerase: purification of individually overexpressed subunits and in vitro assembly. Protein Expr. Purif., 4, 503-511.
2. Borukhov, S., Sagitov, V. and Goldfarb, A. (1993) Transcript cleavage factors from E.coli. Cell, 72, 459-466.
3. Brautigam, C.A. and Steitz, T.A. (1998) Structural principles for the inhibition of the 3′-5′ exonuclease activity of Escherichia coli DNA polymerase I by phosphorothioates. J. Mol. Biol., 277, 363-377.
4. Cramer, P., Bushnell, D.A. and Komberg, R.D. (2001) Structural basis of transcription: RNA polymerase II at 2.8 Å resolution. Science, 292, 1863-1876.
5. Epshtein, V., Mustaev, A., Markovtsov, V., Bereshchenko, O., Nikiforov, V. and Goldfarb, A. (2002) Swing-gate model of nucleotide entry into the RNA polymerase active center. Mol. Cell, 10, 623-634.
6. Foster, J.E., Holmes, S.F. and Erie, D.A. (2001) Allosteric binding of nucleoside triphosphates to RNA polymerase regulates transcription elongation. Cell, 106, 243-252.
7. Gnatt, A.L., Cramer, P., Fu, J., Bushnell, D.A. and Komberg, R.D. (2001) Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 Å resolution. Science, 292, 1876-1882.
8. Hagler, J. and Shuman, S. (1993) Nascent RNA cleavage by purified ternary complexes of vaccinia RNA polymerase. J. Biol. Chem., 268, 2166-2173.
9. Hoard, D.E. and Ott, D.G. (1965) Conversion of mono- and oligodeoxyribonucleotides to 5′-triphosphates. J. Am. Chem. Soc., 87, 1785-1789.
10. Izban, M.G. and Luse, D.S. (1993) The increment of SII-facilitated transcript cleavage varies dramatically between elongation competent and incompetent RNA polymerase II ternary complexes. J. Biol. Chem., 268, 12874-128785.
11. Kashlev, M., Nudler, E., Severinov, K., Borukhov, S., Komissarova, N. and Goldfarb, A. (1996) Histidine-tagged RNA polymerase of Escherichia coli and transcription in solid phase. Methods Enzymol., 274, 326-34.
12. Komissarova, N. and Kashlev, M. (1997a) Transcriptional arrest: Escherichia coli RNA polymerase translocates backward, leaving the 3′ end of the RNA intact and extruded. Proc. Natl Acad. Sci. USA, 94, 1755-1760.
13. Komissarova, N. and Kashlev, M. (1997b) RNA polymerase switches between inactivated and activated states by translocating back and forth along the DNA and the RNA. J. Biol. Chem., 272, 15329-15338.
14. Koren, R. and Mildvan, S. (1977) Magnetic resonance and kinetic studies of the role of the divalent cation activator of RNA polymerase from Escherichia coli. Biochemistry, 16, 241-249.
15. Korzheva, N., Mustaev, A., Kozlov, M., Malhotra, A., Nikiforov, V., Goldfarb, A. and Darst, S.A. (2000) A structural model of transcription elongation. Science, 289, 619-625.
16. Lee, J., Kashlev, M., Borukhov, S. and Goldfarb, A. (1991) A β subunit mutation disrupting the catalytic function of Escherichia coli RNA polymerase. Proc. Natl Acad. Sci. USA, 88, 6018-6022.
17. Li, Y., Korolev, S. and Waksman, G. (1998) Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation. EMBO J., 17, 7514-7525.
18. McClure, W.R. (1980) On the mechanism of streptolydigin inhibition of Escherichia coli RNA polymerase. J. Biol. Chem., 255, 1610-1616.
19. Mustaev, A., Kozlov, M., Markovtsov, V., Zaychikov, E., Denissova, L. and Goldfarb, A. (1997) Modular organization of the catalytic center of RNA polymerase. Proc. Natl Acad. Sci. USA, 94, 6641-6645.
20. Nudler, E., Mustaev, A., Lukhtanov, E. and Goldfarb, A. (1997) The RNA-DNA hybrid maintains the register of transcription by preventing backtracking of RNA polymerase. Cell, 89, 33-41.
21. Orlova, M., Newlands, J., Das, A., Goldfarb, A. and Borukhov, S. (1995) Intrinsic transcript cleavage activity of RNA polymerase. Proc. Natl Acad. Sci. USA, 92, 4596-4600.
22. Reines, D. (1992) Elongation factor-dependent transcript shortening by template-engaged RNA polymerase II. J. Biol. Chem., 267, 3795-3800.
23. Rozovskaya, T.A., Rechinsky, V.O., Bibilashvili, R.S., Karpeisky, M.Ya., Tarusova, N.B., Khomutov, R.M. and Dixon, H.B. (1984) The mechanism of pyrophosphorolysis of RNA by RNA polymerase. Endowment of RNA polymerase with artificial exonuclease activity. Biochem. J., 224, 645-650.
24. Rudd, M.D., Izban, M.G. and Luse, D.S. (1994) The active site of RNA polymerase II participates in transcript cleavage within arrested ternary complexes. Proc. Natl Acad. Sci. USA, 91, 8057-8061.
25. Severinov, K., Kashlev, M., Severinova, E., Bass, I., McWilliams, K., Kutter, E., Nikiforov, V., Snyder, L. and Goldfarb, A. (1994) A non-essential domain of Escherichia coli RNA polymerase required for the action of the termination factor Alc. J. Biol. Chem., 269, 14254-14259
26. Steitz, T.A. (1998) A mechanism for all polymerases. Nature, 391, 231-232.
27. Thomas, M.J., Platas, A.A. and Hawley, D.K. (1998) Transcriptional fidelity and proofreading by RNA polymerase II. Cell, 93, 627-637.
28. Vassylyev, D.G., Sekine, S., Laptenko, O., Lee, J., Vassylyeva, M.N., Borukhov, S. and Yokoyama, S. (2002) Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution. Nature, 417, 712-719.
29. Wang, D. and Hawley, D.K. (1993) Identification of a 3′→5′ exonuclease activity associated with human RNA polymerase II. Proc. Natl Acad. Sci. USA, 90, 843-847.
30. Werner, F. and Weinzierl, R. (2002) A recombinant RNA polymerase II-like enzyme capable of promoter-specific transcription. Mol. Cell, 10, 635-646.
31. Whitehall, S.K., Bardeleben, C. and Kassavetis, G.A. (1994) Hydrolytic cleavage of nascent RNA in RNA polymerase III ternary transcription complexes. J. Biol. Chem., 269, 2299-2306.
32. Yee, D., Armstrong, V.W. and Eckstein, F. (1979) Mechanistic studies on deoxyribonucleic acid dependent ribonucleic acid polymerase from Escherichia coli using phosphorothioate analogues. I. Initiation and pyrophosphate exchange reactions. Biochemistry, 18, 4116-4120.
33. Zaychikov, E. et al. (1996) Mapping of catalytic residues in the RNA polymerase active center. Science, 273, 107-109.
34. Zhang, G., Campbell, E.A., Minakhin, L., Richter, C., Severinov, K. and Darst, S.A. (1999) Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 Å resolution. Cell, 98, 811-824.