rRNA transcription in Escherichia coli

Annual Review of Genetics

Volumn 38, Issue , 2004, Pages 749-770

  Paul, Brian J ^a   Ross, Wilma ^a   Gaal, Tamas ^a   Gourse, Richard L ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

DksA; PpGpp; Regulation of gene expression; Ribosome synthesis; RNA polymerase

Indexed keywords

PROTEIN; PROTEIN DKSA; RIBOSOME RNA; RNA POLYMERASE; UNCLASSIFIED DRUG;

CELL GROWTH; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA INTERACTION; PROTEIN PROTEIN INTERACTION; REVIEW; RIBOSOME; RNA PROCESSING; RNA SYNTHESIS; RNA TRANSCRIPTION; TRANSCRIPTION INITIATION;

BINDING SITES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, GENETIC; MODELS, MOLECULAR; PROMOTER REGIONS (GENETICS); RNA, RIBOSOMAL; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

ESCHERICHIA COLI; NEGIBACTERIA; PROKARYOTA;

EID: 10044234372     PISSN: 00664197     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.genet.38.072902.091347     Document Type: Review

References (122)

1. Afflerbach H, Schroder O, Wagner R. 1998. Effects of the Escherichia coli DNA-binding protein H-NS on rRNA synthesis in vivo. Mol. Microbiol. 28:641-53
2. Aiyar SE, McLeod SM, Ross W, Hirvonen CA, Thomas MS, et al. 2002. Architecture of Fis-activated transcription complexes at the Escherichia coli rrnB P1 and rrnE P1 promoters. J. Mol. Biol. 316:501-16
3. Appleman JA, Ross W, Salomon J, Gourse RL. 1998. Activation of Escherichia coli rRNA transcription by FIS during a growth cycle. J. Bacteriol. 180:1525-32
4. Artsimovitch I, Patlan V, Sekine S, Vassylyeva MN, Hosaka T, et al. 2004. Structural basis for transcription regulation by alarmone ppGpp. Cell 117:299-310
5. Ball CA, Osuna R, Ferguson KC, Johnson RC. 1992. Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J. Bacteriol. 174:8043-56
6. Barker MM, Gaal T, Gourse RL. 2001. Mechanism of regulation of transcription initiation by ppGpp. II. Models for positive control based on properties of RNAP mutants and competition for RNAP. J. Mol. Biol. 305:689-702
7. Barker MM, Gaal T, Josaitis CA, Gourse RL. 2001. Mechanism of regulation of transcription initiation by ppGpp. I. Effects of ppGpp on transcription initiation in vivo and in vitro. J. Mol. Biol. 305:673-88
8. Barker MM, Gourse RL. 2001. Regulation of rRNA transcription correlates with nucleoside triphosphate sensing. J. Bacteriol. 183:6315-23
9. Bartlett MS, Gaal T, Ross W, Gourse RL. 1998. RNA polymerase mutants that destabilize RNA polymerase-promoter complexes alter NTP-sensing by rrn P1. promoters. J. Mol. Biol. 279:331-45
10. Bartlett MS, Gaal T, Ross W, Gourse RL. 2000. Regulation of rRNA transcription is remarkably robust: FIS compensates for altered nucleoside triphosphate sensing by mutant RNA polymerases at Escherichia coli rrn P1 promoters. J. Bacteriol. 182:1969-77
11. Bartlett MS, Gourse RL. 1994. Growth rate-dependent control of the rrnB P1 core promoter in Escherichia coli. J. Bacteriol. 176:5560-64
12. Benoff B, Yang H, Lawson CL, Parkinson G, Liu J, et al. 2002. Structural basis of transcription activation: the CAP-alpha CTD-DNA complex. Science 297:1562-66
13. Berg KL, Squires C, Squires CL. 1989. Ribosomal RNA operon anti-termination. Function of leader and spacer region box B-box A sequences and their conservation in diverse micro-organisms. J. Mol. Biol. 209:345-58
14. Blatter EE, Ross W, Tang H, Gourse RL, Ebright RH. 1994. Domain organization of RNA polymerase alpha subunit: C-terminal 85 amino acids constitute a domain capable of dimerization and DNA binding. Cell 78:889-96
15. Bokal AJ, Ross W, Gaal T, Johnson RC, Gourse RL. 1997. Molecular anatomy of a transcription activation patch: FIS-RNA polymerase interactions at the Escherichia coli rrnB P1 promoter. EMBO J. 16:154-62
16. Bokal AJ, Ross W, Gourse RL. 1995. The transcriptional activator protein FIS: DNA interactions and cooperative interactions with RNA polymerase at the Escherichia coli rrnB P1 promoter. J. Mol. Biol. 245:197-207
17. Borukhov S, Sagitov V, Josaitis CA, Gourse RL, Goldfarb A. 1993. Two modes of transcription initiation in vitro at the rrnB P1 promoter of Escherichia coli. J. Biol. Chem. 268:23477-82
18. Bremer H, Dennis PP. 1996. Modulation of chemical composition and other parameters of the cell by growth rate. See Ref. 70a, pp. 1553-69
19. Bremer H, Dennis PP. 1996. Modulation of chemical composition and other parameters of the cell by growth rate. See Ref. 70a, pp. 1553-69
20. Bylund GO, Wipemo LC, Lundberg LA, Wikstrom PM. 1998. RimM and RbfA are essential for efficient processing of 16S rRNA in Escherichia coli. J. Bacteriol 180:73-82
21. Campbell EA, Muzzin O, Chlenov M, Sun JL, Olson CA, et al. 2002. Structure of the bacterial RNA polymerase promoter specificity sigma subunit. Mol. Cell 9:527-39
22. Cashel M, Gallant J. 1969. Two compounds implicated in the function of the RC gene of Escherichia coli. Nature 221:838-41
23. Cashel M, Gentry DR, Hernandez VJ, Vinella D. 1996. The stringent response. See Ref. 70a, pp. 1458-96
24. Cashel M, Gentry DR, Hernandez VJ, Vinella D. 1996. The stringent response. See Ref. 70a, pp. 1458-96
25. Chang DE, Smalley DJ, Conway T. 2002. Gene expression profiling of Escherichia coli growth transitions: an expanded stringent response model. Mol. Microbiol. 45:289-306
26. Chatterji D, Fujita N, Ishihama A. 1998. The mediator for stringent control, ppGpp, binds to the beta-subunit of Escherichia coli RNA polymerase. Genes Cells 3:279-87
27. Chen H, Tang H, Ebright RH. 2003. Functional interaction between RNA polymerase alpha subunit C-terminal domain and sigma70 in UP-element- and activator-dependent transcription. Mol. Cell 11:1621-33
28. Choy HE. 2000. The study of guanosine 5′-diphosphate 3′-diphosphate-mediated transcription regulation in vitro using a coupled transcription-translation system. J. Biol. Chem. 275:6783-89
29. Cole JR, Olsson CL, Hershey JW, Grunberg-Manago M, Nomura M. 1987. Feedback regulation of rRNA synthesis in Escherichia coli. Requirement for initiation factor IF2. J. Mol. Biol. 198:383-92
30. Condon C, French S, Squires C, Squires CL. 1993. Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies. EMBO J. 12:4305-15
31. Dame RT, Wyman C, Wurm R, Wagner R, Goosen N. 2002. Structural basis for H-NS-mediated trapping of RNA polymerase in the open initiation complex at the rrnB P1. J. Biol. Chem. 277:2146-50
32. Dickson RR, Gaal T, deBoer HA, deHaseth PL, Gourse RL. 1989. Identification of promoter mutants defective in growth-rate-dependent regulation of rRNA transcription in Escherichia coli. J. Bacteriol. 171:4862-70
33. Estrem ST, Gaal T, Ross W, Gourse RL. 1998. Identification of an UP element consensus sequence for bacterial promoters. Proc. Natl. Acad. Sci. USA 95:9761-66
34. Estrem ST, Ross W, Gaal T, Chen ZW, Niu W, et al. 1999. Bacterial promoter architecture: subsite structure of UP elements and interactions with the carboxy-terminal domain of the RNA polymerase alpha subunit. Genes Dev. 13:2134-47
35. Gaal T, Bartlett MS, Ross W, Turnbough CL Jr, Gourse RL. 1997. Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. Science 278:2092-97
36. Gaal T, Gourse RL. 1990. Guanosine 3′-diphosphate 5′-diphosphate is not required for growth rate-dependent control of rRNA synthesis in Escherichia coli. Proc. Natl. Acad. Sci. USA 87:5533-37
37. Gaal T, Ross W, Blatter EE, Tang H, Jia X, et al. 1996. DNA-binding determinants of the alpha subunit of RNA polymerase: novel DNA-binding domain architecture. Genes Dev. 10:16-26
38. Gafny R, Cohen S, Nachaliel N, Glaser G. 1994. Isolated P2 rRNA promoters of Escherichia coli are strong promoters that are subject to stringent control. J. Mol. Biol. 243:152-156
39. Gausing K. 1980. Regulation of ribosome biosynthesis in E. coli. In Ribosomes: Structure, Function, and Genetics, ed. G Chambliss, GR Craven, J Davies, K Davis, L Kahan, M Nomura, pp. 693-718. Baltimore: Univ. Park Press
40. Gotta SL, Miller OL Jr., French SL. 1991. rRNA transcription rate in Escherichia coli. J. Bacteriol. 173:6647-49
41. Gourse RL. 1988. Visualization and quantitative analysis of complex formation between E. coli RNA polymerase and an rRNA promoter in vitro. Nucleic Acids Res. 16:9789-809
42. Gourse RL, de Boer HA, Nomura M. 1986. DNA determinants of rRNA synthesis in E. coli: growth rate dependent regulation, feedback inhibition, upstream activation, antitermination. Cell 44:197-205
43. Grundy FJ, Henkin TM. 1992. Characterization of the Bacillus subtilis rpsD regulatory target site. J. Bacteriol. 174:6763-70
44. Hernandez VJ, Cashel M. 1995. Changes in conserved region 3 of Escherichia coli sigma 70 mediate ppGpp-dependent functions in vivo. J. Mol. Biol. 252:536-49
45. Hirvonen CA. 2002. Determinants of rRNA promoter strength in E. coli: transcription activation by UP elements and the transcription factor Fis. PhD thesis. Univ. Wisconsin-Madison. 196 pp.
46. Hirvonen CA, Ross W, Wozniak CE, Marasco E, Anthony JR, et al. 2001. Contributions of UP elements and the transcription factor Fis to expression from the seven rrn P1 promoters in Escherichia coli. J. Bacteriol. 183:6305-14
47. Hogg T, Mechold U, Malke H, Cashel M, Hilgenfeld R. 2004. Conformational antagonism between opposing active sites in a bifunctional RelA/SpoT homolog modulates (p)ppGpp metabolism during the stringent response. Cell 117:57-68
48. Husnain SI, Meng W, Busby SJ, Thomas MS. 2004. Escherichia coli can tolerate insertions of up to 16 amino acids in the RNA polymerase alpha subunit interdomain linker. Biochim. Biophys. Acta 1678:47-56
49. Jacobson A,Gillespie D. 1968. Metabolic events occurring during recovery from prolonged glucose starvation in Escherichia coli. J. Bacteriol. 95:1030-39
50. Jinks-Robertson S, Gourse RL, Nomura M. 1983. Expression of rRNA and tRNA genes in Escherichia coli: evidence for feedback regulation by products of rRNA operons. Cell 33:865-76
51. Jores L, Wagner R. 2003. Essential steps in the ppGpp-dependent regulation of bacterial ribosomal RNA promoters can be explained by substrate competition. J. Biol. Chem. 278:16834-43
52. Josaitis CA, Gaal T, Gourse RL. 1995. Stringent control and growth-rate-dependent control have nonidentical promoter sequence requirements. Proc. Natl. Acad. Sci. USA 92:1117-21
53. Kajitani M, Ishihama A. 1984. Promoter selectivity of Escherichia coli RNA polymerase. Differential stringent control of the multiple promoters from ribosomal RNA and protein operons. J. Biol. Chem. 259:1951-57
54. Kang PJ, Craig EA. 1990. Identification and characterization of a new Escherichia coli gene that is a dosage-dependent suppressor of a dnaK deletion mutation. J. Bacteriol. 172:2055-64
55. Keener J, Nomura M. 1996. Regulation of ribosome biosynthesis. See Ref. 70a, pp. 1417-31
56. Keener J, Nomura M. 1996. Regulation of ribosome biosynthesis. See Ref. 70a, pp. 1417-31
57. Laptenko O, Lee J, Lomakin I, Borukhov S. 2003. Transcript cleavage factors GreA and GreB act as transient catalytic components of RNA polymerase. EMBO J. 22:6322-34
58. Lee DJ, Busby SJ, Lloyd GS. 2003. Exploitation of a chemical nuclease to investigate the location and orientation of the Escherichia coli RNA polymerase alpha subunit C-terminal domains at simple promoters that are activated by cyclic AMP receptor protein. J. Biol. Chem. 278:52944-52
59. Lew CM, Gralla JD. 2004. Mechanism of stimulation of ribosomal promoters by binding of the +1 and +2 nucleotides. J. Biol. Chem. 279:19481-85
60. Li SC, Squires CL, Squires C. 1984. Antitermination of E. coli rRNA transcription is caused by a control region segment containing lambda nut-like sequences. Cell 38:851-60
61. Li Z, Pandit S, Deutscher MP. 1999. RNase G (CafA protein) and RNase E are both required for the 5′ maturation of 16S ribosomal RNA. EMBO J. 18:2878-85
62. Lukacsovich T, Boros I, Venetianer P. 1987. New regulatory features of the promoters of an Escherichia coli rRNA gene. J. Bacteriol. 169:272-77
63. Mallic P, Pratt TS, Beach MB, Bradley MD, Undamatla J, Osuna R. 2004. Growth phase-dependent regulation and stringent control of fis are conserved processes in enteric bacteria and involve a single promoter (fis P) in Escherichia coli. J. Bacteriol. 186:122-35
64. Mason SW, Li J, Greenblatt J. 1992. Direct interaction between two Escherichia coli transcription antitermination factors, NusB and ribosomal protein S10. J. Mol. Biol. 223:55-66
65. McLeod SM, Aiyar SE, Gourse RL, Johnson RC. 2002. The C-terminal domains of the RNA polymerase alpha subunits: contact site with Fis and localization during co-activation with CRP at the Escherichia coli proP P2 promoter. J. Mol. Biol. 316:517-29
66. McLeod SM, Xu J, Cramton SE, Gaal T, Gourse RL, Johnson RC. 1999. Localization of amino acids required for Fis to function as a class II transcriptional activator at the RpoS-dependent proP P2 promoter. J. Mol. Biol. 294:333-46
67. Mekler V, Kortkhonjia E, Mukhopadhyay J, Knight J, Revyakin A, et al. 2002. Structural organization of bacterial RNA polymerase holoenzyme and the RNA polymerase-promoter open complex. Cell 108:599-614
68. Meng W, Belyaeva T, Savery NJ, Busby SJ, Ross WE, et al. 2001. UP element-dependent transcription at the Escherichia coli rrnB P1 promoter: positional requirements and role of the RNA polymerase alpha subunit linker. Nucleic Acids Res. 29:4166-78
69. Murakami KS, Masuda S, Campbell EA, Muzzin O, Darst SA. 2002. Structural basis of transcription initiation: an RNA polymerase holoenzyme-DNA complex. Science 296:1285-90
70. Murray HD, Appleman JA, Gourse RL. 2003. Regulation of the Escherichia coli rrnB P2 promoter. J. Bacteriol. 185:28-34
71. Murray HD, Gourse RL. 2004. Unique roles of the rrn P2 rRNA promoters in Escherichia coli. Mol. Microbiol. 52:1375-87
72. Murray HD, Schneider DA, Gourse RL. 2003. Control of rRNA expression by small molecules is dynamic and nonredundant. Mol. Cell 12:125-34
73. Naryshkin N, Revyakin A, Kim Y, Mekler V, Ebright RH. 2000. Structural organization of the RNA polymerase-promoter open complex. Cell 101:601-11
74. a. Neidhardt FC, Curtiss R III, Gross CA, et al., eds. 1996. Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. Washington, DC: ASM Press
75. Nilsson L, Vanet A, Vijgenboom E, Bosch L. 1990. The role of FIS in trans activation of stable RNA operons of E. coli. EMBO J. 9:727-34
76. Nilsson L, Verbeek H, Vijgenboom E, van Drunen C, Vanet A, Bosch L. 1992. FIS-dependent Irans activation of stable RNA operons of Escherichia coli under various growth conditions. J. Bacteriol. 174:921-29
77. Ofengand J, Malhotra A, Remme J, Gutgsell NS, Del Campo M, et al. 2001. Pseudouridines and pseudouridine synthases of the ribosome. Cold Spring Harbor Symp. Quant. Biol. 66:147-59
78. Ohlsen KL, Gralla JD. 1992. Interrelated effects of DNA supercoiling, ppGpp, and low salt on melting within the Escherichia coli ribosomal RNA rrB P1 promoter. Mol. Microbiol. 6:2243-51
79. Opalka N, Chlenov M, Chacon P, Rice WJ, Wriggers W, Darst SA. 2003. Structure and function of the transcription elongation factor GreB bound to bacterial RNA polymerase. Cell 114:335-45
80. Osuna R, Lienau D, Hughes KT, Johnson RC. 1995. Sequence, regulation, and functions of fis in Salmonella typhimurium. J. Bacteriol. 177:2021-32
81. Ow MC, Liu Q, Kushner SR. 2000. Analysis of mRNA decay and rRNA processing in Escherichia coli in the absence of RNase E-based degradosome assembly. Mol. Microbiol. 38:854-66
82. Paul BJ, Barker MM, Ross W, Schneider DA, Webb C, et al. 2004. DksA: a critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP. Cell. 118:311-22
83. Pemberton IK, Muskhelishvili G, Travers AA, Buckle M. 2002. HS modulates the kinetics of successive interactions of RNA polymerase with the core and upstream regions of the tyrT promoter. J. Mol. Biol. 318:651-63
84. Perederina A, Svetlov V, Vassylyeva MN, Artsimovitch I, Yokoyama S, Vassylyev D. 2004. Regulation through the secondary channel-structural framework for ppGpp-DksA synergism during transcription. Cell. 118:297-309
85. Petersen C, Moller LB. 2000. Invariance of the nucleoside triphosphate pools of Escherichia coli with growth rate. J. Biol. Chem. 275:3931-35
86. Pokholok DK, Redlak M, Turnbough CL Jr, Dylla S, Holmes WM. 1999. Multiple mechanisms are used for growth rate and stringent control of leuV transcriptional initiation in Escherichia coli. J. Bacteriol. 181:5771-82
87. Potrykus K, Wegrzyn G, Hernandez VJ. 2002. Multiple mechanisms of transcription inhibition by ppGpp at the lambda p(R) promoter. J. Biol. Chem. 277:43785-91
88. Ross W, Aiyar SE, Salomon J, Gourse RL. 1998. Escherichia coli promoters with UP elements of different strengths: modular structure of bacterial promoters. J. Bacteriol. 180:5375-83
89. Ross W, Ernst A, Gourse RL. 2001. Fine structure of E. coli RNA polymerase-promoter interactions: alpha subunit binding to the UP element minor groove. Genes Dev. 15:491-506
90. Ross W, Gosink KK, Salomon J, Igarashi K, Zou C, et al. 1993. A third recognition element in bacterial promoters: DNA binding by the alpha subunit of RNA polymerase. Science 262:1407-13
91. Ross W, Salomon J, Holmes WM, Gourse RL. 1999. Activation of Escherichia coli leuV transcription by FIS. J. Bacteriol. 181:3864-68
92. Ross W, Schneider DA, Paul BJ, Mertens A, Gourse RL. 2003. An intersubunit contact stimulating transcription initiation by E coli RNA polymerase: interaction of the alpha C-terminal domain and sigma region 4. Genes Dev. 17:1293-307
93. Ross W, Thompson JF, Newlands JT, Gourse RL. 1990. E. coli Fis protein activates ribosomal RNA transcription in vitro and in vivo. EMBO J. 9:3733-42
94. Sabina J, Dover N, Templeton LJ, Smulski DR, Soil D, LaRossa RA. 2003. Interfering with different steps of protein synthesis explored by transcriptional profiling of Escherichia coli K-12. J. Bacteriol. 185:6158-70
95. Sands MK, Roberts RB. 1952. The effects of a tryptophan-histidine deficiency in a mutant of Escherichia coli. J. Bacteriol. 63:505-11
96. Sarmientos P, Cashel M. 1983. Carbon starvation and growth rate-dependent regulation of the Escherichia coli ribosomal RNA promoters: differential control of dual promoters. Proc. Natl. Acad. Sci. USA 80:7010-13
97. Sarmientos P, Contente S, Chinali G, Cashel M. 1983. Ribosomal RNA operon promoters P1 and P2 show differential regulatory responses. In Gene Expression, ed. DH Hamer, M Rosenberg, pp. 65-74. New York: Liss
98. Schaechter M, Maaloe O, Kjeldgaard NO. 1958. Dependency on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. J. Gen. Microbiol. 19:592-606
99. Schaferkordt J, 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. 29:3394-403
100. Schneider DA, Gaal T, Gourse RL. 2002. NTP-sensing by rRNA promoters in Escherichia coli is direct. Proc. Natl. Acad. Sci. USA 99:8602-7
101. Schneider DA, Gourse RL. 2003. Changes in Escherichia coli rRNA promoter activity correlate with changes in initiating nucleoside triphosphate and guanosine 5′ diphosphate 3′-diphosphate concentrations after induction of feed-back control of ribosome synthesis. J. Bacteriol. 185:6185-91
102. Schneider DA, Gourse RL. 2003. Changes in the concentrations of guanosine 5′-diphosphate 3′-diphosphate and the initiating nucleoside triphosphate account for inhibition of rRNA transcription in fructose-1,6-diphosphate aldolase (fda) mutants. J. Bacteriol. 185:6192-94
103. Schneider DA, Gourse RL. 2004. Relationship between growth rate and ATP concentration in Escherichia coli: a bioassay for available cellular ATP. J. Biol Chem. 279:8262-68
104. Schneider DA, Ross W, Gourse RL. 2003. Control of rRNA expression in Escherichia coli. Curr. Opin. Microbiol. 6:151-56
105. Schroder O, Wagner R. 2000. The bacterial DNA-binding protein H-NS represses ribosomal RNA transcription by trapping RNA polymerase in the initiation complex. J. Mol. Biol. 298:737-48
106. Sharrock RA, Gourse RL, 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 82:5275-79
107. Squires CL, Greenblatt J, Li J, Condon C, Squires CL. 1993. Ribosomal RNA antitermination in vitro: requirement for Nus factors and one or more unidentified cellular components. Proc. Natl. Acad. Sci. USA 90:970-74
108. Stent GS, Brenner S. 1961. A genetic locus for the regulation of ribonucleic acid synthesis. Proc. Natl. Acad. Sci. USA 47:2005-14
109. Stephens JC, Artz SW, Ames BN. 1975. Guanosine 5′-diphosphate 3′-diphosphate (ppGpp): positive effector for histidine operon transcription and general signal for amino-acid deficiency. Proc. Natl. Acad. Sci. USA 72:4389-93
110. Torres M, Balada JM, Zellars M, Squires C, Squires CL. 2004. In vivo effect of NusB and NusG on rRNA transcription antitermination. J. Bacteriol. 186:1304-10
111. Torres M, Condon C, Balada JM, Squires C, Squires CL. 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. 20:3811-20
112. Toulokhonov I, Shulgina I, Hernandez VJ. 2001. Binding of the transcription effector ppGpp to Escherichia coli RNA polymerase is allosteric, modular, and occurs near the N terminus of the beta'-subunit. J. Biol. Chem. 276:1220-25
113. Travers AA. Conserved features of coordinately regulated E. coli promoters. Nucleic Acids Res. 12:2605-18
114. Wendrich TM, Blaha G, Wilson DN, Marahiel MA, Nierhaus KH. 2002. Dissection of the mechanism for the stringent factor Re1A. Mol. Cell 10:779-88
115. Vogel U, Jensen KF. 1997. NusA is required for ribosomal antitermination and for modulation of the transcription elongation rate of both antiterminated RNA and mRNA. J. Biol. Chem. 272:12265-71
116. Voulgaris J, Pokholok D, Holmes WM, Squires C, Squires CL. 2000. The feed-back response of Escherichia coli rRNA synthesis is not identical to the mechanism of growth rate-dependent control. J. Bacteriol. 182:536-39
117. Xiao H, Kalman M, Ikehara K, Zemel S, Glaser G, Cashel M. 1991. Residual guanosine 3′,5′-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J. Biol. Chem. 266:5980-90
118. Xu J, Johnson RC. 1995. Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli. J. Bacteriol. 177:938-47
119. Yamagishi M, de Boer HA, Nomura M. 1987. Feedback regulation of rRNA synthesis. A mutational alteration in the anti-Shine-Dalgarno region of the 16S rRNA gene abolishes regulation. J. Mol. Biol 198:547-50
120. Zengel JM, Lindahl L. 1994. Diverse mechanisms for regulating ribosomal protein synthesis in Escherichia coli. Prog. Nucleic Acid Res. Mol. Biol. 47:331-70
121. Zhi H, Wang X, Cabrera JE, Johnson RC, Jin DJ. 2003. Fis stabilizes the interaction between RNA polymerase and the ribosomal promoter rrnB P1, leading to transcriptional activation. J. Biol. Chem. 278:47340-49
122. Zhou YN, Jin DJ. 1998. The rpoB mutants destabilizing initiation complexes at stringently controlled promoters behave like "stringent" RNA polymerases in Escherichia coli. Proc. Natl. Acad. Sci. USA 95:2908-13