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Nus transcription elongation factors and RNase III modulate small ribosome subunit biogenesis in E scherichia coli

dc.contributor.authorBubunenko, Mikhailen_US
dc.contributor.authorCourt, Donald L.en_US
dc.contributor.authorAl Refaii, Abdallaen_US
dc.contributor.authorSaxena, Shivalikaen_US
dc.contributor.authorKorepanov, Alexeyen_US
dc.contributor.authorFriedman, David I.en_US
dc.contributor.authorGottesman, Max E.en_US
dc.contributor.authorAlix, Jean‐hervéen_US
dc.date.accessioned2013-02-12T19:00:53Z
dc.date.available2014-03-03T15:09:24Zen_US
dc.date.issued2013-01en_US
dc.identifier.citationBubunenko, Mikhail; Court, Donald L.; Al Refaii, Abdalla; Saxena, Shivalika; Korepanov, Alexey; Friedman, David I.; Gottesman, Max E.; Alix, Jean‐hervé (2013). " Nus transcription elongation factors and RNase III modulate small ribosome subunit biogenesis in E scherichia coli ." Molecular Microbiology (2): 382-393. <http://hdl.handle.net/2027.42/96334>en_US
dc.identifier.issn0950-382Xen_US
dc.identifier.issn1365-2958en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/96334
dc.publisherWiley Periodicals, Inc.en_US
dc.publisherAcademic Pressen_US
dc.titleNus transcription elongation factors and RNase III modulate small ribosome subunit biogenesis in E scherichia colien_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelMicrobiology and Immunologyen_US
dc.subject.hlbtoplevelScienceen_US
dc.description.peerreviewedPeer Revieweden_US
dc.identifier.pmid23190053en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/96334/1/mmi12105.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/96334/2/mmi12105-sup-0001-si.pdf
dc.identifier.doi10.1111/mmi.12105en_US
dc.identifier.sourceMolecular Microbiologyen_US
dc.identifier.citedreferenceShiba, K., Ito, K., and Yura, T. ( 1986a ) Suppressors of the secY24 mutation: identification and characterization of additional ssy genes in Escherichia coli. J Bacteriol 166: 849 – 856.en_US
dc.identifier.citedreferenceSchweimer, K., Prasch, S., Sujatha, P.S., Bubunenko, M., Gottesman, M.E., and Rosch, P. ( 2011 ) NusA interaction with the α subunit of E. coli RNA polymerase is via the UP element site and releases autoinhibition. Structure 19: 945 – 954.en_US
dc.identifier.citedreferenceSharrock, R.A., Gourse, R.L., and Nomura, M. ( 1985 ) Defective antitermination of rRNA transcription and derepression of rRNA and tRNA synthesis in the nusB5 mutant of Escherichia coli. Proc Natl Acad Sci USA 82: 5275 – 5279.en_US
dc.identifier.citedreferenceShiba, K., Ito, K., Nakamura, Y., Dondon, J., and Grunberg‐Manago, M. ( 1986b ) Altered translation initiation factor 2 in the cold‐sensitive ssyG mutant affects protein export in Escherichia coli. EMBO J 5: 3001 – 3006.en_US
dc.identifier.citedreferenceSquires, C.L., Greenblatt, J., Li, J., Condon, C., and Squires, C.L. ( 1993 ) Ribosomal RNA antitermination in vitro: requirement for Nus factors and one or more unidentified cellular components. Proc Natl Acad Sci USA 90: 970 – 974.en_US
dc.identifier.citedreferenceSrivastava, A.K., and Schlessinger, D. ( 1990 ) Mechanism and regulation of bacterial ribosomal RNA processing. Annu Rev Microbiol 44: 105 – 129.en_US
dc.identifier.citedreferenceStagno, J.R., Altieri, A.S., Bubunenko, M., Tarasov, S.G., Li, J., Court, D.L., et al. ( 2011 ) Structural basis for RNA recognition by NusB and NusE in the initiation of transcription antitermination. Nucleic Acids Res 39: 7803 – 7815.en_US
dc.identifier.citedreferenceTaura, T., Ueguchi, C., Shiba, K., and Ito, K. ( 1992 ) Insertional disruption of the nusB ( ssyB ) gene leads to cold‐sensitive growth of Escherichia coli and suppression of the secY24 mutation. Mol Gen Genet 234: 429 – 432.en_US
dc.identifier.citedreferenceTheissen, G., Behrens, S.E., and Wagner, R. ( 1990 ) Functional importance of the Escherichia coli ribosomal RNA leader boxA sequence for post‐transcriptional events. Mol Microbiol 4: 1667 – 1678.en_US
dc.identifier.citedreferenceTorres, M., Condon, C., Balada, J.M., Squires, C., and Squires, C.L. ( 2001 ) Ribosomal protein S4 is a transcription factor with properties remarkably similar to NusA, a protein involved in both non‐ribosomal and ribosomal RNA antitermination. EMBO J 20: 3811 – 3820.en_US
dc.identifier.citedreferenceTorres, M., Balada, J.M., Zellars, M., Squires, C., and Squires, C.L. ( 2004 ) In vivo effect of NusB and NusG on rRNA transcription antitermination. J Bacteriol 186: 1304 – 1310.en_US
dc.identifier.citedreferenceTu, C., Zhou, X., Tropea, J., Austin, B., Waugh, D., Court, D., and Ji, X. ( 2009 ) Structure of ERA in complex with the 3′ end of 16S rRNA: implications for ribosome biogenesis. Proc Natl Acad Sci USA 106: 14843 – 14848.en_US
dc.identifier.citedreferenceVogel, U., and Jensen, K.F. ( 1997 ) NusA is required for ribosomal antitermination and for modulation of the transcription elongation rate of both antiterminated RNA and mRNA. J Biol Chem 272: 12265 – 12271.en_US
dc.identifier.citedreferenceWilson, H.R., Yu, D., Peters, H.K., 3rd, Zhou, J.G., and Court, D.L. ( 2002 ) The global regulator RNase III modulates translation repression by the transcription elongation factor N. EMBO J 21: 4154 – 4161.en_US
dc.identifier.citedreferenceWilson, H.R., Zhou, J.G., Yu, D., and Court, D.L. ( 2004 ) Translation repression by an RNA polymerase elongation complex. Mol Microbiol 53: 821 – 828.en_US
dc.identifier.citedreferenceWong, T., Sosnick, T.R., and Pan, T. ( 2005 ) Mechanistic insights on the folding of a large ribozyme during transcription. Biochemistry 44: 7535 – 7542.en_US
dc.identifier.citedreferenceWoodson, S.A. ( 2008 ) RNA folding and ribosome assembly. Curr Opin Chem Biol 12: 667 – 673.en_US
dc.identifier.citedreferenceYoung, R.A., and Steitz, J.A. ( 1978 ) Complementary sequences 1700 nucleotides apart form a ribonuclease III cleavage site in Escherichia coli ribosomal precursor RNA. Proc Natl Acad Sci USA 75: 3593 – 3597.en_US
dc.identifier.citedreferenceYu, D., Ellis, H.M., Lee, E.C., Jenkins, N.A., Copeland, N.G., and Court, D.L. ( 2000 ) An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci USA 97: 5978 – 5983.en_US
dc.identifier.citedreferenceZellars, M., and Squires, C.L. ( 1999 ) Antiterminator‐dependent modulation of transcription elongation rates by NusB and NusG. Mol Microbiol 32: 1296 – 1304.en_US
dc.identifier.citedreferenceZhou, Y., Mah, T.F., Yu, Y.T., Mogridge, J., Olson, E.R., Greenblatt, J., and Friedman, D.I. ( 2001 ) Interactions of an Arg‐rich region of transcription elongation protein NusA with NUT RNA: implications for the order of assembly of the lambda N antitermination complex in vivo. J Mol Biol 310: 33 – 49.en_US
dc.identifier.citedreferenceAl Refaii, A., and Alix, J.H. ( 2009 ) Ribosome biogenesis is temperature‐dependent and delayed in Escherichia coli lacking the chaperones DnaK or DnaJ. Mol Microbiol 71: 748 – 762.en_US
dc.identifier.citedreferenceAlbrechtsen, B., Squires, C.L., Li, S., and Squires, C. ( 1990 ) Antitermination of characterized transcriptional terminators by the Escherichia coli rrnG leader region. J Mol Biol 213: 123 – 134.en_US
dc.identifier.citedreferenceBalzer, M., and Wagner, R. ( 1998 ) Mutations in the leader region of ribosomal RNA operons cause structurally defective 30S ribosomes as revealed by in vivo structural probing. J Mol Biol 276: 547 – 557.en_US
dc.identifier.citedreferenceBesancon, W., and Wagner, R. ( 1999 ) Characterization of transient RNA–RNA interactions important for the facilitated structure formation of bacterial ribosomal 16S RNA. Nucleic Acids Res 27: 4353 – 4362.en_US
dc.identifier.citedreferenceBeuth, B., Pennell, S., Arnvig, K.B., Martin, S.R., and Taylor, I.A. ( 2005 ) Structure of a Mycobacterium tuberculosis NusA–RNA complex. EMBO J 24: 3576 – 3587.en_US
dc.identifier.citedreferenceBochner, B.R., Huang, H.C., Schieven, G.L., and Ames, B.N. ( 1980 ) Positive selection for loss of tetracycline resistance. J Bacteriol 143: 926 – 933.en_US
dc.identifier.citedreferenceBubunenko, M., Baker, T., and Court, D.L. ( 2007 ) Essentiality of ribosomal and transcription antitermination proteins analyzed by systematic gene replacement in Escherichia coli. J Bacteriol 189: 2844 – 2853.en_US
dc.identifier.citedreferenceConant, C.R., Goodarzi, J., Weitzel, S.E., and von Hippel, P.H. ( 2008 ) The antitermination activity of bacteriophage lambda N protein is controlled by the kinetics of an RNA‐looping‐facilitated interaction with the transcription complex. J Mol Biol 384: 87 – 108.en_US
dc.identifier.citedreferenceCondon, C., French, S., Squires, C., and Squires, C.L. ( 1993 ) Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies. EMBO J 12: 4305 – 4315.en_US
dc.identifier.citedreferenceCondon, C., Squires, C., and Squires, C.L. ( 1995 ) Control of rRNA transcription in Escherichia coli. Microbiol Rev 59: 623 – 645.en_US
dc.identifier.citedreferenceCourt, D.L. ( 1993 ) RNA processing and degradation by RNase III. In Control of Messenger RNA Stability. Belasco, J., and Brawerman, G. (eds). New York: Academic Press, pp. 71 – 116.en_US
dc.identifier.citedreferenceCourt, D.L., Swaminathan, S., Yu, D., Wilson, H., Baker, T., Bubunenko, M., et al. ( 2003 ) Mini‐lambda: a tractable system for chromosome and BAC engineering. Gene 315: 63 – 69.en_US
dc.identifier.citedreferenceCourt, D.L., Oppenheim, A.B., and Adhya, S.L. ( 2007 ) A new look at bacteriophage lambda genetic networks. J Bacteriol 189: 298 – 304.en_US
dc.identifier.citedreferenceCraven, M.G., and Friedman, D.I. ( 1991 ) Analysis of the Escherichia coli nusA10 (Cs) allele: relating nucleotide changes to phenotypes. J Bacteriol 173: 1485 – 1491.en_US
dc.identifier.citedreferenceDas, A. ( 1993 ) Control of transcription termination by RNA‐binding proteins. Annu Rev Biochem 62: 893 – 930.en_US
dc.identifier.citedreferenceDeutscher, M.P. ( 2009 ) Maturation and degradation of ribosomal RNA in bacteria. Prog Mol Biol Transl Sci 85: 369 – 391.en_US
dc.identifier.citedreferenceDeVito, J., and Das, A. ( 1994 ) Control of transcription processivity in phage λ: Nus factors strengthen the termination‐resistant state of RNA polymerase induced by N antiterminator. Proc Natl Acad Sci USA 91: 8660 – 8664.en_US
dc.identifier.citedreferenceDunn, J.J., and Studier, F.W. ( 1973 ) T7 early RNAs and Escherichia coli ribosomal RNAs are cut from large precursor RNAs in vivo by ribonuclease III. Proc Natl Acad Sci USA 70: 3296 – 3300.en_US
dc.identifier.citedreferenceFrauenfeld, J., Gumbart, J., Sluis, E.O., Funes, S., Gartmann, M., Beatrix, B., et al. ( 2011 ) Cryo‐EM structure of the ribosome–SecYE complex in the membrane environment. Nat Struct Mol Biol 18: 614 – 621.en_US
dc.identifier.citedreferenceFrench, S.L., and Miller, O.L. ( 1989 ) Transcription mapping of the Escherichia coli chromosome by electron microscopy. J Bacteriol 171: 4207 – 4216.en_US
dc.identifier.citedreferenceFriedman, D.I., and Court, D.L. ( 1995 ) Transcription antitermination: the lambda paradigm updated. Mol Microbiol 18: 191 – 200.en_US
dc.identifier.citedreferenceFriedman, D.I., Schauer, A.T., Baumann, M.R., Baron, L.S., and Adhya, S.L. ( 1981 ) Evidence that ribosomal protein S10 participates in control of transcription termination. Proc Natl Acad Sci USA 78: 1115 – 1118.en_US
dc.identifier.citedreferenceGegenheimer, P., and Apirion, D. ( 1975 ) Escherichia coli ribosomal ribonucleic acids are not cut from an intact precursor molecule. J Biol Chem 250: 2407 – 2409.en_US
dc.identifier.citedreferenceGegenheimer, P., and Apirion, D. ( 1978 ) Processing of rRNA by RNAase P: spacer tRNAs are linked to 16S rRNA in an RNAase P RNAase III mutant strain of E. coli. Cell 15: 527 – 539.en_US
dc.identifier.citedreferenceGreenblatt, J., Nodwell, J.R., and Mason, S.W. ( 1993 ) Transcriptional antitermination. Nature 364: 401 – 406.en_US
dc.identifier.citedreferenceGreive, S.J., Lins, A.F., and von Hippel, P.H. ( 2005 ) Assembly of an RNA–protein complex. Binding of NusB and NusE (S10) proteins to boxA RNA nucleates the formation of the antitermination complex involved in controlling rRNA transcription in Escherichia coli. J Biol Chem 280: 36397 – 36408.en_US
dc.identifier.citedreferenceHeinrich, T., Condon, C., Pfeiffer, T., and Hartmann, R.K. ( 1995 ) Point mutations in the leader boxA of a plasmid‐encoded Escherichia coli rrnB operon cause defective antitermination in vivo. J Bacteriol 177: 3793 – 3800.en_US
dc.identifier.citedreferenceKaczanowska, M., and Ryden‐Aulin, M. ( 2007 ) Ribosome biogenesis and the translation process in Escherichia coli. Microbiol Mol Biol Rev 71: 477 – 494.en_US
dc.identifier.citedreferenceKlumpp, S., and Hwa, T. ( 2008 ) Stochasticity and traffic jams in the transcription of ribosomal RNA: intriguing role of termination and antitermination. Proc Natl Acad Sci USA 105: 18159 – 18164.en_US
dc.identifier.citedreferenceLee, C., and Beckwith, J. ( 1986 ) Cotranslational and posttranslational protein translocation in prokaryotic systems. Annu Rev Cell Biol 2: 315 – 336.en_US
dc.identifier.citedreferenceLi, J., Horwitz, R., McCracken, S., and Greenblatt, J. ( 1992 ) NusG, a new Escherichia coli elongation factor involved in transcriptional antitermination by the N protein of phage lambda. J Biol Chem 267: 6012 – 6019.en_US
dc.identifier.citedreferenceLi, S.C., Squires, C.L., and Squires, C. ( 1984 ) Antitermination of E. coli rRNA transcription is caused by a control region segment containing lambda nut ‐like sequences. Cell 38: 851 – 860.en_US
dc.identifier.citedreferenceLindahl, L. ( 1975 ) Intermediates and time kinetics of the in vivo assembly of Escherichia coli ribosomes. J Mol Biol 92: 15 – 37.en_US
dc.identifier.citedreferenceLuo, X., Hsiao, H.H., Bubunenko, M., Weber, G., Court, D.L., Gottesman, M.E., et al. ( 2008 ) Structural and functional analysis of the E. coli NusB–S10 transcription antitermination complex. Mol Cell 32: 791 – 802.en_US
dc.identifier.citedreferenceMason, S.W., Li, J., and Greenblatt, J. ( 1992 ) Direct interaction between two Escherichia coli transcription antitermination factors, NusB and ribosomal protein S10. J Mol Biol 223: 55 – 66.en_US
dc.identifier.citedreferenceMiller, J.H. ( 1972 ) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.en_US
dc.identifier.citedreferenceMorgan, E.A. ( 1986 ) Antitermination mechanisms in rRNA operons of Escherichia coli. J Bacteriol 168: 1 – 5.en_US
dc.identifier.citedreferencede Narvaez, C.C., and Schaup, H.W. ( 1979 ) In vivo transcriptionally coupled assembly of Escherichia coli ribosomal subunits. J Mol Biol 134: 1 – 22.en_US
dc.identifier.citedreferenceNierhaus, K.H. ( 2004 ) Assembly of the prokaryotic ribosome. In Protein Synthesis and Ribosome Structure. Nierhaus, K.H., and Wilson, D.N. (eds). Weinheim, Germany: Wiley‐VCH, pp. 85 – 105.en_US
dc.identifier.citedreferenceNodwell, J.R., and Greenblatt, J. ( 1993 ) Recognition of boxA antiterminator RNA by the E. coli antitermination factors NusB and ribosomal protein S10. Cell 72: 261 – 268.en_US
dc.identifier.citedreferenceNoller, H.F. ( 1993 ) Peptidyl transferase: protein, ribonucleoprotein, or RNA? J Bacteriol 175: 5297 – 5300.en_US
dc.identifier.citedreferenceOlson, E.R., Tomich, C.S., and Friedman, D.I. ( 1984 ) The NusA recognition site. Alteration in its sequence or position relative to upstream translation interferes with the action of the N antitermination function of phage lambda. J Mol Biol 180: 1053 – 1063.en_US
dc.identifier.citedreferencePan, T., Artsimovitch, I., Fang, X.W., Landick, R., and Sosnick, T.R. ( 1999 ) Folding of a large ribozyme during transcription and the effect of the elongation factor NusA. Proc Natl Acad Sci USA 96: 9545 – 9550.en_US
dc.identifier.citedreferencePfeiffer, T., and Hartmann, R.K. ( 1997 ) Role of the spacer boxA of Escherichia coli ribosomal RNA operons in efficient 23S rRNA synthesis in vivo. J Mol Biol 265: 385 – 393.en_US
dc.identifier.citedreferencePlumbridge, J.A., and Springer, M. ( 1983 ) Organization of the Escherichia coli chromosome around the genes for translation initiation factor IF2 ( infB ) and a transcription termination factor ( nusA ). J Mol Biol 167: 227 – 243.en_US
dc.identifier.citedreferencePrasch, S., Jurk, M., Washburn, R.S., Gottesman, M.E., Wohrl, B.M., and Rosch, P. ( 2009 ) RNA‐binding specificity of E. coli NusA. Nucleic Acids Res 37: 4736 – 4742.en_US
dc.identifier.citedreferenceQuan, S., Zhang, N., French, S., and Squires, C.L. ( 2005 ) Transcriptional polarity in rRNA operons of Escherichia coli nusA and nusB mutant strains. J Bacteriol 187: 1632 – 1638.en_US
dc.identifier.citedreferenceRajapandi, T., and Oliver, D. ( 1994 ) ssaD1, a suppressor of secA51 (Ts) that renders growth of Escherichia coli cold sensitive, is an early amber mutation in the transcription factor gene nusB. J Bacteriol 176: 4444 – 4447.en_US
dc.identifier.citedreferenceRene, O., and Alix, J.H. ( 2011 ) Late steps of ribosome assembly in E. coli are sensitive to a severe heat stress but are assisted by the HSP70 chaperone machine. Nucleic Acids Res 39: 1855 – 1867.en_US
dc.identifier.citedreferenceRoberts, J.W., Shankar, S., and Filter, J.J. ( 2008 ) RNA polymerase elongation factors. Annu Rev Microbiol 62: 211 – 233.en_US
dc.identifier.citedreferenceSchäferkordt, J., and Wagner, R. ( 2001 ) Effects of base change mutations within an Escherichia coli ribosomal RNA leader region on rRNA maturation and ribosome formation. Nucleic Acids Res 29: 3394 – 3403.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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