RpoS regulation of gene expression during exponential growth of Escherichia coli K12

Molecular Genetics and Genomics

Volumn 279, Issue 3, 2008, Pages 267-277

  Dong, Tao ^a   Kirchhof, Mark G ^b   Schellhorn, Herb E ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Exponential phase; Microarray; Regulation; RpoS; Stress response

Indexed keywords

IRON; MALTOSE; SIGMA FACTOR RPOS;

ARTICLE; BACTERIAL GROWTH; BIOCHEMISTRY; CARBON SOURCE; ESCHERICHIA COLI; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENOMICS; MICROARRAY ANALYSIS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN FUNCTION; TRANSCRIPTION REGULATION;

BACTERIAL PROTEINS; BASE SEQUENCE; BLOTTING, WESTERN; DNA PRIMERS; DNA, BACTERIAL; ESCHERICHIA COLI K12; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, BACTERIAL; HEAT-SHOCK PROTEINS; IRON; MALTOSE; MODELS, BIOLOGICAL; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN FOLDING; SIGMA FACTOR;

ESCHERICHIA COLI;

EID: 39249084651     PISSN: 16174615     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00438-007-0311-4     Document Type: Article

References (70)

1. Alteri CJ, Mobley HL (2007) Quantitative profile of the uropathogenic Escherichia coli outer membrane proteome during growth in human urine. Infect Immun 75:2679-2688
2. Baev MV, Baev D, Radek AJ, Campbell JW (2006) Growth of Escherichia coli MG1655 on LB medium: monitoring utilization of sugars, alcohols, and organic acids with transcriptional microarrays. Appl Microbiol Biotechnol 71:310-316
3. Barnard TJ, Watson ME Jr, McIntosh MA (2001) Mutations in the Escherichia coli receptor FepA reveal residues involved in ligand binding and transport. Mol Microbiol 41:527-536
4. Barrick JE, Sudarsan N, Weinberg Z, Ruzzo WL, Breaker RR (2005) 6S RNA is a widespread regulator of eubacterial RNA polymerase that resembles an open promoter. RNA 11:774-784
5. Boos W, Shuman H (1998) Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol Mol Biol Rev 62:204-229
6. Bougdour A, Lelong C, Geiselmann J (2004) Crl, a low temperature-induced protein in Escherichia coli that binds directly to the stationary phase sigma subunit of RNA polymerase. J Biol Chem 279:19540-19550
7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
8. Chen G, Patten CL, Schellhorn HE (2004) Positive selection for loss of RpoS function in Escherichia coli. Mutat Res 554:193-203
9. Cheung KJ, Badarinarayana V, Selinger DW, Janse D, Church GM (2003) A microarray-based antibiotic screen identifies a regulatory role for supercoiling in the osmotic stress response of Escherichia coli. Genome Res 13:206-215
10. Constantinidou C, Hobman JL, Griffiths L, Patel MD, Penn CW, Cole JA, Overton TW (2006) A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to anaerobic growth. J Biol Chem 281:4802-4815
11. Costanzo A, Ades SE (2006) Growth phase-dependent regulation of the extracytoplasmic stress factor, sigmaE, by guanosine 3′,5′- bispyrophosphate (ppGpp). J Bacteriol 188:4627-4634
12. Dahl MK, Manson MD (1985) Interspecific reconstitution of maltose transport and chemotaxis in Escherichia coli with maltose-binding protein from various enteric bacteria. J Bacteriol 164:1057-1063
13. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640-6645
14. Dippel R, Bergmiller T, Bohm A, Boos W (2005) The maltodextrin system of Escherichia coli: glycogen-derived endogenous induction and osmoregulation. J Bacteriol 187:8332-8339
15. Farewell A, Kvint K, Nystrom T (1998) Negative regulation by RpoS: a case of sigma factor competition. Mol Microbiol 29:1039-1051
16. Fayet O, Ziegelhoffer T, Georgopoulos C (1989) The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J Bacteriol 171:1379-1385
17. Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W (1998a) Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282:2215-2220
18. Ferguson GP, Creighton RI, Nikolaev Y, Booth IR (1998b) Importance of RpoS and Dps in survival of exposure of both exponential- and stationary-phase Escherichia coli cells to the electrophile N-ethylmaleimide. J Bacteriol 180:1030-1036
19. Gaal T, Mandel MJ, Silhavy TJ, Gourse RL (2006) Crl facilitates RNA polymerase holoenzyme formation. J Bacteriol 188:7966-7970
20. Gragerov A, Nudler E, Komissarova N, Gaitanaris GA, Gottesman ME, Nikiforov V (1992) Cooperation of GroEL/GroES and DnaK/DnaJ heat shock proteins in preventing protein misfolding in Escherichia coli. Proc Natl Acad Sci USA 89:10341-10344
21. Gyaneshwar P, Paliy O, McAuliffe J, Jones A, Jordan MI, Kustu S (2005) Lessons from Escherichia coli genes similarly regulated in response to nitrogen and sulfur limitation. Proc Natl Acad Sci USA 102:3453-3458
22. Hansen UM, McClure WR (1980) Role of the sigma subunit of Escherichia coli RNA polymerase in initiation. II. Release of sigma from ternary complexes. J Biol Chem 255:9564-9570
23. Hantash FM, Ammerlaan M, Earhart CF (1997) Enterobactin synthase polypeptides of Escherichia coli are present in an osmotic-shock-sensitive cytoplasmic locality. Microbiology 143(Pt 1):147-156
24. Hantke K (1990) Dihydroxybenzoylserine-a siderophore for E. coli. FEMS Microbiol Lett 55:5-8
25. Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852-1858
26. Heitzer A, Mason CA, Snozzi M, Hamer G (1990) Some effects of growth conditions on steady state and heat shock induced htpG gene expression in continuous cultures of Escherichia coli. Arch Microbiol 155:7-12
27. Hengge-Aronis R (1996) Back to log phase: sigma S as a global regulator in the osmotic control of gene expression in Escherichia coli. Mol Microbiol 21:887-893
28. Hengge-Aronis R (2002) Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66:373-95
29. Heyde M, Portalier R (1990) Acid shock proteins of Escherichia coli. FEMS Microbiol Lett 57:19-26
30. Hirsch M, Elliott T (2005) Stationary-phase regulation of RpoS translation in Escherichia coli. J Bacteriol 187:7204-7213
31. Horwich AL, Low KB, Fenton WA, Hirshfield IN, Furtak K (1993) Folding in vivo of bacterial cytoplasmic proteins: role of GroEL. Cell 74:909-917
32. Jishage M, Ishihama A (1995) Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of sigma 70 and sigma 38. J Bacteriol 177:6832-6835
33. Jishage M, Ishihama A (1998) A stationary phase protein in Escherichia coli with binding activity to the major sigma subunit of RNA polymerase. Proc Natl Acad Sci USA 95:4953-4958
34. Jishage M, Iwata A, Ueda S, Ishihama A (1996) Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of four species of sigma subunit under various growth conditions. J Bacteriol 178:5447-5451
35. Jishage M, Kvint K, Shingler V, Nystrom T (2002) Regulation of sigma factor competition by the alarmone ppGpp. Genes Dev 16:1260-1270
36. Kang Y, Weber KD, Qiu Y, Kiley PJ, Blattner FR (2005) Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. J Bacteriol 187:1135-1160
37. Khil PP, Camerini-Otero RD (2002) Over 1000 genes are involved in the DNA damage response of Escherichia coli. Mol Microbiol 44:89-105
38. Kluck CJ, Patzelt H, Genevaux P, Brehmer D, Rist W, Schneider-Mergener J, Bukau B, Mayer MP (2002) Structure-function analysis of HscC, the Escherichia coli member of a novel subfamily of specialized Hsp70 chaperones. J Biol Chem 277:41060-41069
39. Kobayashi A, Hirakawa H, Hirata T, Nishino K, Yamaguchi A (2006) Growth phase-dependent expression of drug exporters in Escherichia coli and its contribution to drug tolerance. J Bacteriol 188:5693-5703
40. Lacour S, Landini P (2004) SigmaS-dependent gene expression at the onset of stationary phase in Escherichia coli: function of sigmaS-dependent genes and identification of their promoter sequences. J Bacteriol 186:7186-7195
41. Lange R, Fischer D, Hengge-Aronis R (1995) Identification of transcriptional start sites and the role of ppGpp in the expression of rpoS, the structural gene for the sigma S subunit of RNA polymerase in Escherichia coli. J Bacteriol 177:4676-4680
42. Lange R, Hengge-Aronis R (1994a) The cellular concentration of the sigma S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev 8:1600-1612
43. Lange R, Hengge-Aronis R (1994b) The nlpD gene is located in an operon with rpoS on the Escherichia coli chromosome and encodes a novel lipoprotein with a potential function in cell wall formation. Mol Microbiol 13:733-743
44. Lee HJ, Park KJ, Lee AY, Park SG, Park BC, Lee KH, Park SJ (2003) Regulation of fur expression by RpoS and fur in Vibrio vulnificus. J Bacteriol 185:5891-5896
45. Lelong C, Aguiluz K, Luche S, Kuhn L, Garin J, Rabilloud T, Geiselmann J (2007) The Crl-RpoS regulon of Escherichia coli. Mol Cell Proteomics 6:648-659
46. Li C, Wong WH (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA 98:31-36
47. Locher KP, Rees B, Koebnik R, Mitschler A, Moulinier L, Rosenbusch JP, Moras D (1998) Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95:771-778
48. Lombardo MJ, Aponyi I, Rosenberg SM (2004) General stress response regulator RpoS in adaptive mutation and amplification in Escherichia coli. Genetics 166:669-680
49. Marshall OJ (2004) PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20:2471-2472
50. Mason CA, Dunner J, Indra P, Colangelo T (1999) Heat-induced expression and chemically induced expression of the Escherichia coli stress protein HtpG are affected by the growth environment. Appl Environ Microbiol 65:3433-3440
51. Nunoshiba T, Obata F, Boss AC, Oikawa S, Mori T, Kawanishi S, Yamamoto K (1999) Role of iron and superoxide for generation of hydroxyl radical, oxidative DNA lesions, and mutagenesis in Escherichia coli. J Biol Chem 274:34832-34837
52. Nystrom T (2004) Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition? Mol Microbiol 54:855-862
53. Patten CL, Kirchhof MG, Schertzberg MR, Morton RA, Schellhorn HE (2004) Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol Genet Genomics 272:580-591
54. Pease AJ, Roa BR, Luo W, Winkler ME (2002) Positive growth rate-dependent regulation of the pdxA, ksgA, and pdxB genes of Escherichia coli K-12. J Bacteriol 184:1359-1369
55. Rahman M, Hasan MR, Oba T, Shimizu K (2006) Effect of rpoS gene knockout on the metabolism of Escherichia coli during exponential growth phase and early stationary phase based on gene expressions, enzyme activities and intracellular metabolite concentrations. Biotechnol Bioeng 94:585-595
56. Robbe-Saule V, Lopes MD, Kolb A, Norel F (2007) Physiological effects of Crl in Salmonella are modulated by sigmaS level and promoter specificity. J Bacteriol 189:2976-2987
57. 2 and broad-spectrum near-UV radiation by the Escherichia coli katF (rpoS) locus. J Bacteriol 168:13-21
58. Schellhorn HE, Audia JP, Wei LI, Chang L (1998) Identification of conserved, RpoS-dependent stationary-phase genes of Escherichia coli. J Bacteriol 180:6283-6291
59. Schellhorn HE, Stones VL (1992) Regulation of katF (rpoS) and katE in Escherichia coli K-12 by weak acids. J Bacteriol 174:4769-4776
60. Schembri MA, Kjaergaard K, Klemm P (2003) Global gene expression in Escherichia coli biofilms. Mol Microbiol 48:253-267
61. Schweder T, Lee KH, Lomovskaya O, Matin A (1996) Regulation of Escherichia coli starvation sigma factor (sigmaS) by ClpXP protease. J Bacteriol 178:470-476
62. Seputiene V, Daugelavicius A, Suziedelis K, Suziedeliene E (2006) Acid response of exponentially growing Escherichia coli K-12. Microbiol Res 161:65-74
63. Shea CM, McIntosh MA (1991) Nucleotide sequence and genetic organization of the ferric enterobactin transport system: homology to other periplasmic binding protein-dependent systems in Escherichia coli. Mol Microbiol 5:1415-1428
64. Torres AG, Redford P, Welch RA, Payne SM (2001) TonB-dependent systems of uropathogenic Escherichia coli: aerobactin and heme transport and TonB are required for virulence in the mouse. Infect Immun 69:6179-6185
65. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116-5121
66. Typas A, Barembruch C, Possling A, Hengge R (2007) Stationary phase reorganisation of the Escherichia coli transcription machinery by Crl protein, a fine-tuner of sigmas activity and levels. EMBO J 26:1569-1578
67. Van Hove B, Staudenmaier H, Braun V (1990) Novel two-component transmembrane transcription control: regulation of iron dicitrate transport in Escherichia coli K-12. J Bacteriol 172:6749-6758
68. Vijayakumar SR, Kirchhof MG, Patten CL, Schellhorn HE (2004) RpoS-regulated genes of Escherichia coli identified by random lacZ fusion mutagenesis. J Bacteriol 186:8499-8507
69. Wassarman KM, Storz G (2000) 6S RNA regulates E. coli RNA polymerase activity. Cell 101:613-623
70. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R (2005) Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187:1591-1603