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Bacterial RNA polymerases: structural and functional relationships

  • Special Topic Review: Control of Gene Expression Microorganisms. Edited by Miguel Vicente
  • Special Topic Review
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Abstract

The essential role of DNA-dependent RNA polymerases in gene expression and the fact that the multimeric species are highly conserved throughout nature makes these enzymes a particular fascinating area of study. Here we shall review the conservation of structures and their relationship to function, especially in the multimeric eubacterial RNA polymerases, paying particular attention to the β core subunit and to recent studies of σ-factors of both the σ 70 and σ 54 families. We shall conclude with a brief consideration of phage-encoded RNA polymerases and phage-mediated modification of the host enzyme, and of the evolution of RNA-synthesising enzymes.

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References

  • Abdulwajid, A.W. & Wu, F.Y.-H. 1986 Chemical modification of Escherichia coli RNA polymerase by diethyl pyrocarbonate: evidence of histidine requirement for enzyme activity and intrinsic zinc binding. Biochemistry 25, 8167–8172.

    Google Scholar 

  • Adhya, S. & Gottesman, M. 1978 Control of transcription termination. Annual Review of Biochemistry 47, 967–996.

    Google Scholar 

  • Aldhea, M., Garrido, T., Pla, J. & Vicente, M. 1990 Division genes in E. coli are expressed coordinately to cell septum requirements by gearbox promoters. EMBO Journal 9, 3787–3794.

    Google Scholar 

  • Bear, D.G. & Peabody, D.S. 1988 The E. coli Rho protein: an ATPase that terminates transcription. Trends in Biochemical Sciences 13, 343–347.

    Google Scholar 

  • Buck, M. & Cannon, W. 1992 Specific binding of the transcription factor 411-1 to promoter DNA. Nature 358, 422–424.

    Google Scholar 

  • Burgess, R.R. 1971 RNA polymerase. Annual Review of Biochemistry 40, 711–740.

    Google Scholar 

  • Burgess, R.R. 1976 Purification and physical properties of E. coli RNA polymerase. In RNA polymerase, eds Losick, R. & Chamberlin, M. pp. 69–100. New York: Cold Spring Harbor Laboratory.

    Google Scholar 

  • Burgess, R.R., Erickson, B., Gentry, D., Gribskov, M., Hager, D., Lesley, S., Strickland, M. & Thompson, N. 1987 Bacterial RNA polymerase subunits and genes. In RNA Polymerase and the Regulation of Transcription, eds Reznikoff, W.S., Burgess, R.R., Dahlberg, J.E., Gross, C.A., Record, M.T. & Wickens, M.P. pp. 3–15. New York: Elsevier.

    Google Scholar 

  • Burgess, R.R., Travers, A.A., Dunn, J.J. & Bautz, E.K.F. 1969 Factor stimulating transcription by RNA polymerase. Nature 221, 43–46.

    Google Scholar 

  • Buttner, M.J. 1989 RNA polymerase heterogeneity in Streptomyces coelicolor A3(2). Molecular Microbiology 3, 1653–1659.

    Google Scholar 

  • Buttner, M.J. & Lewis, C.G. 1992 Construction and characterisation of Streptomyces coelicolor A3(2) mutants that are multiply deficient in the non-essential Hrd-encoded RNA polymerase sigma factors. Journal of Bacteriology 174, 5165–5167.

    Google Scholar 

  • Buttner, J.M. & Lewis, C.G. 1992 Construction and characterisation of Streptomyces coelicolor A3(2) mutants that are multiply deficient in the non-essential Hrd-encoded RNA polymerase sigma factors. Journal of Bacteriology 174, 5165–5167.

    Google Scholar 

  • Chamberlin, M., Kingston, R., Gilman, M., Wiggs, J. & DeVera, A. 1983 Isolation of bacterial and bacteriophage RNA polymerases and their use in the synthesis of RNA in vitro. Methods in Enzymology 101, 540–568.

    Google Scholar 

  • Chater, K.F., Bruton, C.J., Plaskitt, K.A., Buttner, M.J., Mendez, C. & Helmann, J.D. 1989 The developmental fate of S. coelicolor hyphae depends upon a gene product homologous with the mobility sigma factor of B. subtilis. Cell 59, 133–143.

    Google Scholar 

  • Darst, S.A., Kubalek, E.W. & Kornberg, R.D. 1989 Three-dimensional structure of Escherichia coli RNA polymerase holoenzyme determined by electron crystallography. Nature 340, 730–732.

    Google Scholar 

  • Dombroski, A.J., Walter, A.W., Record, M.T.Jr, Siegele, D.A. & Gross, C.A. 1992 Polypeptides containing highly conserved regions of transcription initiation factor 411-2 exhibit specificity of binding to promoter DNA. Cell 70, 501–512.

    Google Scholar 

  • Friedman, D.I. 1988 Regulation of phage gene expression by termination and antitermination of transcription. In The Bacteriophages, Vol. 2, ed Calendar, R. pp. 263–319. New York: Plenum Press.

    Google Scholar 

  • Friedman, D.I., Imperiale, M.J. & Adhya, S.L. 1987 RNA 3′ end formation in the control of gene expression. Annual Review of Genetics 21, 453–488.

    Google Scholar 

  • Geiduschek, E.P. & Kassavetis, G.A. 1988 Changes in RNA polymerase. In The Bacteriophages, Vol. 1., ed Calendar, R. pp. 93–115. New York: Plenum Press.

    Google Scholar 

  • Gentry, D., Xiao, H., Burgess, R. & Cashel, M. 1991 The omega subunit of Escherichia coli K/12 RNA polymerase is not required for stringent RNA control in vivo. Journal of Bacteriology 173, 3901–3903.

    Google Scholar 

  • Goff, C.G. 1984 Coliphage-induced ADP-ribosylation of Escherichia coli RNA polymerase. Methods in Enzymology 106, 418–429.

    Google Scholar 

  • Gribskov, M. & Burgess, R.R. 1986 Sigma factors from E. coli, B. subtilis, phage SPO1 and phage T4 are homologous proteins. Nucleic Acids Research 14, 6745–6763.

    Google Scholar 

  • Gropp, F., Reiter, W.D., Sentenac, A., Zillig, W., Schnabel, R., Thomm, M. & Stetter, R.O. 1986 Homologies of components of DNA-dependent RNA polymerase of archaebacteria, eukaryotes and eubacteria. Systematic Applied Microbiology 7, 95–101.

    Google Scholar 

  • Gussin, G.N., Ronson, C.W. & Ausubel, F.M. 1986 Regulation of nitrogen fixation genes. Annual Review of Genetics 20, 567–591.

    Google Scholar 

  • Hayward, R.S., Kumar, A., Grimes, B. & Logan, M. 1992 A hybrid sigma complements a hybrid promoter. Journal of Cellular Biochemistry, Suppl 16E, 141.

  • Helmann, J.D. 1991 Alternative sigma factors and the regulation of flagellar gene expression. Molecular Microbiology 5, 2875–2882.

    Google Scholar 

  • Helmann, J.D. & Chamberlin, M.J. 1988 Structure and function of bacterial sigma factors. Annual Review of Biochemistry 57, 839–872.

    Google Scholar 

  • Hesselbach, B.A. & Nakada, D. 1977 “Host-shutoff” function of bacteriophage T7: Involvement of T7 gene 2 and gene 0.7 in the inactivation of E. coli RNA polymerase. Journal of Virology 24, 736–745.

    Google Scholar 

  • Heumann, H., Lederer, H., Barr, G., May, R.P., Kjems, J.K. & Crespi, H.L. 1988 Spatial arrangement of DNA-dependent RNA polymerase of Escherichia coli and DNA in the specific complex. Journal of Molecular Biology 201, 115–125.

    Google Scholar 

  • Hoover, T.R., Santero, E., Porter, S. & Kustu, S. 1990 The integration host factor stimulates interaction of RNA polymerase with NIFA, the transcriptional activator for nitrogen fixation operons. Cell 63, 11–22.

    Google Scholar 

  • Igarashi, K., Fujita, N. & Ishihama, A. 1989 Promoter selectivity of Escherichia coli RNA polymerase: Omega factor is responsible for the ppGpp sensitivity. Nucleic Acids Research 17, 8755–8765.

    Google Scholar 

  • Ikeda, R.A. & Richardson, C.C. 1987 Enzymatic properties of a proteolytically nicked RNA polymerase of bacteriophage T7. Journal of Biological Chemistry 262, 3790–3799.

    Google Scholar 

  • Ishihama, A. 1992 Role of the RNA polymerase α subunit in transcription activation. Molecular Microbiology 6, 3283–3288.

    Google Scholar 

  • Ishihama, A., Fujita, N. & Glass, R.E. 1987 Subunit assembly and metabolic stability of E. coli RNA polymerase. Proteins: Structure, Function and Genetics 2, 42–53.

    Google Scholar 

  • Ito, K., Egawa, K. & Nakamura, Y. 1991 Genetic interaction between the β′ subunit of RNA polymerase and the arginine-rich domain of Escherichia coli nusA protein. Journal of Bacteriology 173, 1492–1501.

    Google Scholar 

  • Jin, D.J. & Gross, C.A. 1989 Characterisation of the pleiotropic phenotypes of rifampicin-resistant rpoB mutants of Escherichia coli. Journal of Bacteriology 171, 5229–5231.

    Google Scholar 

  • Jones, C.H. & Moran, C.P.Jr 1992 Mutant σ factor blocks transition between promoter binding and initiation of transcription. Proceedings of the National Academy of Sciences of the United States of America 89, 1958–1962.

    Google Scholar 

  • Kajitani, M. & Ishihama, A. 1991 Identification and sequence determination of the host factor gene for bacteriophage Qβ. Nucleic Acids Research 19, 1063–1066.

    Google Scholar 

  • King, G.C., Martin, C.T., Pham, T.T. & Coleman, J.E. 1986 Transcription by T7 RNA polymerase is not zinc-dependent and is abolished on amidomethylation of cysteine-347. Biochemistry 25, 36–40.

    Google Scholar 

  • Konarska, M.M. & Sharp, P.A. 1990 Structure of RNAs replicated by the DNA-dependent T7 RNA polymerase. Cell 63, 609–619.

    Google Scholar 

  • Kustu, S., North, A.K. & Weiss, D.S. 1991 Prokaryotic transcriptional enhancers and enhancer-binding proteins. Trends in Biochemical Sciences 16, 397–402.

    Google Scholar 

  • Kutsu, S., Santero, E., Keener, J., Popham, D. & Weiss, D. 1989 Expression of 412-1 (NtrA)-dependent genes is probably united by a common mechanism. Microbiological Review 53, 367–376.

    Google Scholar 

  • Kustu, S., Sei, K. & Keener, J. 1986 Nitrogen regulation in enteric bacteria. Society for General Microbiology Symposium 39, 139–165.

    Google Scholar 

  • Landick, R., Stewart, J. & Lee, D.N. 1990 Amino acid changes in conserved regions of the β-subunit of Escherichia coli RNA polymerase alter transcription pausing and termination. Genes and Development 4, 1623–1636.

    Google Scholar 

  • Lange, R. & Hengge-Aronis, R. 1991 Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Molecular Microbiology 5, 49–59.

    Google Scholar 

  • Lathe, R. 1978 RNA polymerase of Escherichia coli. Current Topics in Microbiology and Immunology 83, 38–91.

    Google Scholar 

  • Lesley, S.A. & Burgess, R.R. 1989 Characterisation of the Escherichia coli transcription factor 412-2: localisation of a region involved in the interaction with core RNA polymerase. Biochemistry 28, 7728–7734.

    Google Scholar 

  • Lindquist, S. & Craig, E.A. 1988 The heat-shock proteins. Annual Review of Genetics 22, 631–677.

    Google Scholar 

  • Lombardo, M.-J., Bagga, D. & Miller, C.G. 1991 Mutations in rpoA affect expression of anaerobically regulated genes in Salmonella typhimurium. Journal of Bacteriology 173, 7511–7518.

    Google Scholar 

  • Lonetto, M., Gribskov, M. & Gross, C.A. 1992 The 412-3 family: sequence conservation and evolutionary relationships. Journal of Bacteriology 174, 3843–3849.

    Google Scholar 

  • Losick, R. & Chamberlin, M. (eds) 1976 RNA Polymerase. New York: Cold Spring Harbor Laboratory.

    Google Scholar 

  • Makino, K., Amemura, M., Kim, S.-K., Nakata, A. & Shinagawa, H. 1993 Role of the 412-4 subunit of RNA polymerase in transcriptional activation by activator protein PhoB in Escherichia coli. Genes and Development 7, 149–160.

    Google Scholar 

  • Margolis, P.M., Driks, A. & Losick, R. 1991 Establishment of cell type by compartmentalized activation of a transcription factor. Science 254, 562–565.

    Google Scholar 

  • Merrick, M. & Chambers, S. 1992 The helix-turn-helix motif of 412-5 is involved in recognition of the —13 promoter region. Journal of Bacteriology 174, 7221–7226.

    Google Scholar 

  • Morris, C.E., McGraw, N.J., Joho, K., Brown, J.E., Klement, J.F., Ling, M.L. & McAllister, W.T. 1987 Mechanisms of promoter recognition by the bacteriophage T3 and T7 RNA polymerases. In RNA Polymerase and the Regulation of Transcription, eds Reznikoff, W.S., Burgess, R.R., Dahlberg, J.E., Gross, C.A., Record, M.T. & Wickens, M.P. pp. 47–58. New York: Elsevier.

    Google Scholar 

  • Mulvey, M.T. & Loewen, P.C. 1989 Nucleotide sequence of katF of Escherichia coli suggests that KatF protein is a novel σ transcription factor. Nucleic Acids Research 17, 9979–9991.

    Google Scholar 

  • Nene, V. & Glass, R.E. 1984 Genetic studies on the β subunit of Escherichia coli RNA polymerase. IV. Structure-function correlates. Molecular and General Genetics 194, 166–172.

    Google Scholar 

  • Nomura, T., Ishihama, A., Kajitani, M., Takahashi, T., Nakada, N. & Yoshinaga, K. 1984 Promoter selectivity of Escherichia coli RNA polymerase. II. Altered promoter selection by mutant holoenzymes. Molecular and General Genetics 193, 8–16.

    Google Scholar 

  • Ozaki, M., Fujita, N., Wada, A. & Ishihama, A. 1992 Promoter selectivity of the stationary phase forms of E. coli RNA polymerase and conversion in vitro of the S1 form enzyme into a log-phase enzyme-like form. Nucleic Acids Research 20, 257–261.

    Google Scholar 

  • Platt, T. 1986 Transcription termination and the regulation of gene expression. Annual Review of Biochemistry 55, 339–372.

    Google Scholar 

  • Priano, C., Kramer, F.R. & Mills, D.R. 1987 Evolution of the RNA coliphages: The role of secondary structure during RNA replication. Cold Spring Harbor Symposia on Quantitative Biology 52, 321–330.

    Google Scholar 

  • Reznikoff, W.S., Burgess, R.R., Dahlberg, J.E., Gross, C.A., Record, M.T. & Wickens, M.P. (eds) 1987 RNA Polymerase and the Regulation of Transcription. New York: Elsevier.

    Google Scholar 

  • Rothman-Denes, L.B., Abrasaya, K., Glucksmann, A., Malone, C. & Markiewicz, P. 1987 Bacteriophage N4-coded RNA polymerases. In RNA Polymerase and the Regulation of Transcription, eds Reznikoff, W.S., Burgess, R.R., Dahlberg, J.E., Gross, C.A., Record, M.T. & Wickens, M.P. pp. 37–45. New York: Elsevier.

    Google Scholar 

  • Rowland, G.C. & Glass, R.E. 1990 Conservation of RNA polymerase. BioEssays 12, 343–346.

    Google Scholar 

  • Sasse-Dwight, S. & Gralla, J.D. 1990 Role of eukaryotic-type functional domains found in the prokaryotic enhancer receptor factor 412-6. Cell 62, 945–954.

    Google Scholar 

  • Schmidt, R., Margolis, P., Duncan, L., Coppolecchia, R., Moran, C.P.Jr & Losick, R. 1990 Control of developmental transcription factor 412-7 by sporulation regulatory proteins SpollAA and SpollAB in B. subtilis. Proceedings of the National Academy of Sciences of the United States of America 87, 9221–9225.

    Google Scholar 

  • Shiina, T., Tanaka, K. & Takahashi, H. 1991 Sequence of hrdB, an essential gene encoding sigma-like transcription factor of Streptomyces coelicolor A3(2): homology to principal sigma factors. Gene 107, 145–148.

    Google Scholar 

  • Shorenstein, R.G. & Losick, R. 1973 Comparative size and properties of the sigma subunits of ribonucleic acid polymerase from Bacillus subtilis and Escherichia coli. Journal of Biological Chemistry 248, 6170–6173.

    Google Scholar 

  • Skowyra, D., Georgopoulos, C. & Zylicz, M. 1990 The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP-hydrolysis-dependent manner. Cell 62, 939–944.

    Google Scholar 

  • Slauch, J.M., Russo, F.D. & Silhavy, T.J. 1991 Suppressor mutations in rpoA suggest that OmpR controls transcription by direct interaction with the α subunit of RNA polymerase. Journal of Bacteriology 173, 7501–7510.

    Google Scholar 

  • Sousa, R., Rose, J.P., Chung, Y.J., Lafer, E.M. & Wang, B.-C. 1989 Single crystals of bacteriophage T7 RNA polymerase. Proteins: Structure, Function, and Genetics 5, 266–270.

    Google Scholar 

  • Stragier, P. 1991 Dances with sigmas. EMBO Journal 10, 3559–3566.

    Google Scholar 

  • Studier, F.W., Rosenberg, A.H., Dunn, J.J. & Dubendorff, J.W. 1990 Use of T7 RNA polymerase to direct expression of cloned genes. Methods in Enzymology 185, 60–89.

    Google Scholar 

  • Tabor, S. & Richardson, C.C. 1985 A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proceedings of the National Academy of Sciences of the United States of America 82, 1074–1078.

    Google Scholar 

  • Tanaka, K., Shiina, T. & Takahashi, H. 1991 Nucleotide sequence of genes hrdA, hrdC and hrdD from Streptomyces coelicolor A3(2) having similarity to rpoD genes. Molecular and General Genetics 299, 334–340.

    Google Scholar 

  • Tanaka, K., Takayanagi, Y., Fujita, N., Ishihama, A. & Takahashi, H. 1993 Heterogeneity of the principal sigma factor in Escherichia coli: the rpoS gene product, 413-1, is a second principal sigma factor of RNA polymerase in stationary phase Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 90, 3511–3515.

    Google Scholar 

  • Thomas, M. & Glass, R.E. 1991 Escherichia coli rpoA mutation which impairs transcription of positively regulated systems. Molecular Microbiology 5, 2719–2725.

    Google Scholar 

  • Thony, B. & Hennecke, H. 1989 The −24/−12 promoter comes of age. FEMS Microbiology Reviews 5, 341–357.

    Google Scholar 

  • Wedel, A., Weiss, D.S., Popham, D., Droge, P. & Kustu, S. 1990 A bacterial enhancer functions to tether a transcriptional activator near a promoter. Science 248, 486–490.

    Google Scholar 

  • Werhli, W. 1977 Ansamycins: chemistry, biosynthesis and biological activity. Topics Current in Chemistry 72, 21–49.

    Google Scholar 

  • Wu, C.-W., Wu, F. Y.-H. & Speckhard, D.C. 1977 Subunit location of the intrinsic divalent metal ions in RNA polymerase from Escherichia coli. Biochemistry 16, 5449–5454.

    Google Scholar 

  • Yager, T.D. & VonHippel, P.H. 1987 Transcript elongation and termination in Escherichia coli. In Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology, eds Neidhardt, F.C., Ingraham, J.L., Low, K.B., Magasanik, B., Schaechter, M. & Umbarger, H.E. pp. 1241–1275. Washington DC: American Society for Microbiology.

    Google Scholar 

  • Yura, T. & Ishihama, A. 1979 Genetics of bacterial RNA polymerases. Annual Review of Genetics 13, 59–97.

    Google Scholar 

  • Zehring, W.A. & Rothman-Denes, L.B. 1983 Purification and characterisation of coliphage N4 RNA polymerase II activity from infected cell extracts. Journal of Biological Chemistry 258, 8074–8080.

    Google Scholar 

  • Zillig, W., Fujiki, H., Blum, W., Janekovic, D., Schweiger, M., Rahmsdorf, H.J., Ponta, H. & Hirsch-Kaufmann, M. 1975 In vivo and in vitro phosphorylation of DNA-dependent RNA polymerase of E. coli by bacteriophage-T7-induced protein kinase. Proceedings of the National Academy of Sciences of the United States of America 72, 2506–2510.

    Google Scholar 

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Glass, R.E., Hayward, R.S. Bacterial RNA polymerases: structural and functional relationships. World Journal of Microbiology and Biotechnology 9, 403–413 (1993). https://doi.org/10.1007/BF00328028

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