Transcription regulation of the Escherichia coli pcnB gene coding for poly(A) polymerase I: Roles of ppGpp, DksA and sigma factors

Molecular Genetics and Genomics

Volumn 284, Issue 4, 2010, Pages 289-305

  Nadratowska Wesołowska, Beata ^a   Słomijska Wojewódzka, Monika ^a   Łyżeń, Robert ^a   Wdgrzyn, Alicja ^b   Szalewska Pałasz, Agnieszka ^a   Węgrzyn, Grzegorz ^a  

^a University of Gdajsk   (Poland)

^b UNIVERSITY OF GDA SK   (Poland)

Author keywords

DksA; PcnB gene; PpGpp; RNA polyadenylation; Sigma factors; Transcription initiation

Indexed keywords

BACTERIAL PROTEIN; GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE; NUCLEOTIDYLTRANSFERASE; POLYADENYLIC ACID POLYMERASE I; PROTEIN DKSA; SIGMA FACTOR; UNCLASSIFIED DRUG; BACTERIAL DNA; DKSA PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; GUANOSINE 3',5' BIS(DIPHOSPHATE) 3' PYROPHOSPHATASE; GUANOSINE-3',5'-BIS(DIPHOSPHATE) 3'-PYROPHOSPHATASE; INORGANIC PYROPHOSPHATASE; PCNB PROTEIN, E COLI; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; PRIMER DNA;

ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL GROWTH; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SYNTHESIS; ESCHERICHIA COLI; GENETIC TRANSCRIPTION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; CHEMISTRY; DNA FOOTPRINTING; ENZYMOLOGY; ESCHERICHIA COLI K 12; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLASMID;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

BASE SEQUENCE; DNA FOOTPRINTING; DNA PRIMERS; DNA, BACTERIAL; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; PLASMIDS; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; PROMOTER REGIONS, GENETIC; PYROPHOSPHATASES; SIGMA FACTOR; TRANSCRIPTION, GENETIC;

EID: 78049424922     PISSN: 16174615     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00438-010-0567-y     Document Type: Article

References (74)

1. Aberg A, Shingler V, Balsalobre C (2008) Regulation of the fimB promoter: A case of diferential regulation by ppGpp and DksA in vivo. Mol Microbiol 67:1223-1241
2. Artsimovitch I et al (2004) Structural basis for transcription regulation by alarmone ppGpp. Cell 117:299-310
3. August JT, Ortiz PJ, Hurwitz J (1962) Ribonucleic acid-dependent ribonucleotide incorporation. I. Purification and properties of the enzyme. J Biol Chem 237:3786-3793
4. Aviv M, Giladi H, Schreiber G, Oppenheim AB, Glaser G (1994) Expression of the genes coding for the Escherichia coli integration host factor are controlled by growth phase, rpoS, ppGpp and by autoregulation. Mol Microbiol 14:1021-1031
5. Baracchini E, Bremer H (1988) Stringent and growth control of rRNA synthesis in Escherichia coli are both mediated by ppGpp. J Biol Chem 263:2597-2602
6. Barker MM, Gaal T, Gourse RL (2001a) 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 (2001b) Mechanism of regulation of transcription initiation by ppGpp. I. Effects of ppG-pp on transcription initiation in vivo and in vitro. J Mol Biol 305:673-688
8. Bernardo LM, Johansson LU, Solera D, Skarfstad E, Shingler V (2006) The guanosine tetraphosphate (ppGpp) alarmone, DksA and promoter affinity for RNA polymerase in regulation of sigma-depen-dent transcription. Mol Microbiol 60:749-764
9. Bernardo LM, Johansson LU, Skarfstad E, Shingler V (2009) Sigma 54-promoter discrimination and regulation by ppGpp and DksA. J Biol Chem 284:828-838
10. Binns N, Masters M (2002) Expression of the Escherichia coli pcnB gene is translationally limited using an ineicient start codon: A second chromosomal example of translation initiated at AUU. Mol Microbiol 44:1287-1298
11. Blum E, Carpousis AJ, Higgins CF (1999) Polyadenylation promotes degradation of 3′-structured RNA by the Escherichia coli mRNA degradosome in vitro. J Biol Chem 274:4009-4016
12. Bougdour A, Gottesman S (2007) ppGpp regulation of RpoS degradation via anti-adaptor protein IraP. Proc Natl Acad Sci USA 104:12896-12901
13. Brown L, Gentry D, Elliott T, Cashel M (2002) DksA afects ppGpp induction of RpoS at a translational level. J Bacteriol 184:4455-4465
14. Cao GJ, Sarkar N (1992) Identification of the gene for an Escherichia coli poly(A) polymerase. Proc Natl Acad Sci USA 89:10380-10384
15. Costa CS, Pizarro RA, Anton DN (2009) Influence of RpoS, cAMP-receptor protein, and ppGpp on expression of the opgGH operon and osmoregulated periplasmic glucan content of Salmonella ent-erica serovar Typhimurium. Can J Microbiol 55:1284-1293
16. Costanzo A, Ades SE (2006) Growth phase-dependent regulation of the extracytoplasmic stress factor, sigma E, by guanosine 3′,5′- bispyrophosphate (ppGpp). J Bacteriol 188:4627-4634
17. Costanzo A, Nicolof H, Barchinger SE, Banta AB, Gourse RL, Ades SE (2008) ppGpp and DksA likely regulate the activity of the extracytoplasmic stress factor sigma E in Escherichia coli by both direct and indirect mechanisms. Mol Microbiol 67:619-632
18. Durfee T, Hansen AM, Zhi H, Blattner FR, Jin DJ (2008) Transcription proiling of the stringent response in Escherichia coli. J Bacteriol 190:1084-1096
19. Eichel J, Chang YY, Riesenberg D, Cronan JE Jr (1999) Effect of ppG-pp on Escherichia coli cyclopropane fatty acid synthesis is mediated through the RpoS sigma factor (sigma S). J Bacteriol 181:572-576
20. Elliott T, Geiduschek EP (1984) Deining a bacteriophage T4 late promoter: Absence of a "-35" region. Cell 36:211-219
21. Gamer J, Bujard H, Bukau B (1992) Physical interaction between heat shock proteins DnaK, DnaJ, and GrpE and the bacterial heat shock transcription factor sigma 32. Cell 69:833-842
22. Gentry DR, Hernandez VJ, Nguyen LH, Jensen DB, Cashel M (1993) Synthesis of the stationary-phase sigma factor sigma S is positively regulated by ppGpp. J Bacteriol 175:7982-7989
23. Grossman AD, Burgess RR, Walter W, Gross CA (1983) Mutations in the Ion gene of E. coli K12 phenotypically suppress a mutation in the sigma subunit of RNA polymerase. Cell 32:151-159
24. Harinarayanan R, Murphy H, Cashel M (2008) Synthetic growth phe-notypes of Escherichia coli lacking ppGpp and transketolase A (tktA) are due to ppGpp-mediated transcriptional regulation of tktB. Mol Microbiol 69:882-894
25. Janaszak A, Majczak W, Nadratowska B, Szalewska-Palasz A, Konopa G, Taylor A (2007) A sigma54-dependent promoter in the regulatory region of the Escherichia coli rpoH gene. Microbiology 153:111-123
26. Jasiecki J, Wegrzyn G (2003) Growth-rate dependent RNA polyade-nylation in Escherichia coli. EMBO Rep 4:172-177
27. Jasiecki J, Wegrzyn G (2005) Localization of Escherichia coli poly(A) polymerase I in cellular membrane. Biochem Biophys Res Commun 329:598-602
28. Jasiecki J, Wegrzyn G (2006a) Phosphorylation of Escherichia coli poly(A) polymerase I and efects of this modiication on the enzyme activity. FEMS Microbiol Lett 261:118-122
29. Jasiecki J, Wegrzyn G (2006b) Transcription start sites in the promoter region of the Escherichia coli pcnB (plasmid copy number) gene coding for poly(A) polymerase I. Plasmid 55:169-172
30. Jishage M, Ishihama A (1999) Transcriptional organization and in vivo role of the Escherichia coli rsd gene, encoding the regulator of RNA polymerase sigma D. J Bacteriol 181:3768-3776
31. Joanny G et al (2007) Polyadenylation of a functional mRNA controls gene expression in Escherichia coli. Nucleic Acids Res 35:2494-2502
32. 54 transcription activator, PspF, and its DNA-binding mutant, PspF△HTH. J Mol Biol 285:469-483
33. Kang PJ, Craig EA (1990) Identiication and characterization of a new Escherichia coli gene that is a dosage-dependent suppressor of a dnaK deletion mutation. J Bacteriol 172:2055-2064
34. Kvint K, Farewell A, Nystrom T (2000) RpoS-dependent promoters require guanosine tetraphosphate for induction even in the presence of high levels of sigma S. J Biol Chem 275:14795-14798
35. S -RNA polymerase. J Biol Chem 278:37160-37168
36. Lange R, Hengge-Aronis R (1991) Identiication of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol 5:49-59
37. Lange R, Fischer D, Hengge-Aronis R (1995) Identification of tran-scriptional 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
38. Laurie AD et al (2003) The role of the alarmone (p)ppGpp in sigma N competition for core RNA polymerase. J Biol Chem 278:1494-1503
39. Lemke JJ, Durfee T, Gourse RL (2009) DksA and ppGpp directly regulate transcription of the Escherichia coli lagellar cascade. Mol Microbiol 74:1368-1379
40. Liebke H, Gross C, Walter W, Burgess R (1980) A new mutation rpoD800, affecting the sigma subunit of E. coli RNA polymerase is allelic to two other sigma mutants. Mol Gen Genet 177:277-282
41. Liu JD, Parkinson JS (1989) Genetics and sequence analysis of the pcnB locus, an Escherichia coli gene involved in plasmid copy number control. J Bacteriol 171:1254-1261
42. Lopilato J, Bortner S, Beckwith J (1986) Mutations in a new chromosomal gene of Escherichia coli K-12, pcnB, reduce plasmid copy number of pBR322 and its derivatives. Mol Gen Genet 205:285-290
43. Lowe PA, Aebi U, Gross C, Burgess RR (1981) In vitro thermal inac-tivation of a temperature-sensitive sigma subunit mutant (rpoD800) of Escherichia coli RNA polymerase proceeds by aggregation. J Biol Chem 256:2010-2015
44. Lyzen R, Kochanowska M, Wegrzyn G, Szalewska-Palasz A (2009) Transcription from bacteriophage lambda pR promoter is regulated independently and antagonistically by DksA and ppGpp. Nucleic Acids Res 37:6655-6664
45. Magnusson LU, Farewell A, Nystrom T (2005) ppGpp: A global regulator in Escherichia coli. Trends Microbiol 13:236-242
46. Magnusson LU, Gummesson B, Joksimovic P, Farewell A, Nystrom T (2007) Identical, independent, and opposing roles of ppGpp and DksA in Escherichia coli. J Bacteriol 189:5193-5202
47. Merrikh H, Ferrazzoli AE, Lovett ST (2009) Growth phase and (p)ppGpp control of IraD, a regulator of RpoS stability, in Escherichia coli. J Bacteriol 191:7436-7446
48. Mohanty BK, Kushner SR (2006) The majority of Escherichia coli mRNAs undergo post-transcriptional modification in exponentially growing cells. Nucleic Acids Res 34:5695-5704
49. Mohanty BK, Maples VF, Kushner SR (2004) The Sm-like protein Hfq regulates polyadenylation dependent mRNA decay in Esche-richia coli. Mol Microbiol 54:905-920
50. O'Hara EB, Chekanova JA, Ingle CA, Kushner ZR, Peters E, Kushner SR (1995) Polyadenylation helps regulate mRNA decay in Esch-erichia coli. Proc Natl Acad Sci USA 92:1807-1811
51. Paul BJ 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 118:311-322
52. Paul BJ, Berkmen MB, Gourse RL (2005) DksA potentiates direct activation of amino acid promoters by ppGpp. Proc Natl Acad Sci USA 102:7823-7828
53. Perederina A et al (2004) Regulation through the secondary channel-structural framework for ppGpp-DksA synergism during transcription. Cell 118:297-309
54. Potamitou A, Neubauer P, Holmgren A, Vlamis-Gardikas A (2002) Expression of Escherichia coli glutaredoxin 2 is mainly regulated by ppGpp and sigma S. J Biol Chem 277:17775-17780
55. Potrykus K, Cashel M (2008) (p)ppGpp: Still magical? Annu Rev Microbiol 62:35-51
56. Potrykus K, Wegrzyn G, Hernandez VJ (2002) Multiple mechanisms of transcription inhibition by ppGpp at the lambda p(R) promoter. J Biol Chem 277:43785-43791
57. Regnier P, Arraiano CM (2000) Degradation of mRNA in bacteria: Emergence of ubiquitous features. Bioessays 22:235-244
58. Regnier P, Hajnsdorf E (2009) Poly(A)-assisted RNA decay and modulators of RNA stability. Prog Mol Biol Transl Sci 85:137-185
59. Reichenbach B, Maes A, Kalamorz F, Hajnsdorf E, Gorke B (2008) The small RNA GlmY acts upstream of the sRNA GlmZ in the activation of glmS expression and is subject to regulation by polyadenyla-tion in Escherichia coli. Nucleic Acids Res 36:2570-2580
60. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
61. Soderbom F, Wagner EG (1998) Degradation pathway of CopA, the antisense RNA that controls replication of plasmid R1. Microbiology 144(Pt 7):1907-1917
62. Srivatsan A, Wang JD (2008) Control of bacterial transcription, translation and replication by (p)ppGpp. Curr Opin Microbiol 11:100-105
63. Szalewska-Palasz A (2008) Properties of Escherichia coli RNA poly-merase from a strain devoid of the stringent response alarmone ppGpp. Acta Biochim Pol 55:317-323
64. Szalewska-Palasz A, Wrobel B, Wegrzyn G (1998) Rapid degradation of polyadenylated oop RNA. FEBS Lett 432:70-72
65. Szalewska-Palasz A et al (2007a) Properties of RNA polymerase bypass mutants: Implications for the role of ppGpp and its co-factor DksA in controlling transcription dependent on sigma 54. J Biol Chem 282:18046-18056
66. Szalewska-Palasz A, Wegrzyn G, Wegrzyn A (2007b) Mechanisms of physiological regulation of RNA synthesis in bacteria: New discoveries breaking old schemes. J Appl Genet 48:281-294
67. Urban JH, Vogel J (2008) Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol 6:e64
68. Viegas SC, Pfeiffer V, Sittka A, Silva IJ, Vogel J, Arraiano CM (2007) Characterization of the role of ribonucleases in Salmonella small RNA decay. Nucleic Acids Res 35:7651-7664
69. Vrentas CE et al (2008) Still looking for the magic spot: The crystallo-graphically deined binding site for ppGpp on RNA polymerase is unlikely to be responsible for rRNA transcription regulation. J Mol Biol 377:551-564
70. Wigneshweraraj SR et al (2003) Enhancer-dependent transcription by bacterial RNA polymerase: The beta subunit downstream lobe is used by sigma 54 during open promoter complex formation. Methods Enzymol 370:646-657
71. Wrobel B, Herman-Antosiewicz A, Szalewska-Palasz S, Wegrzyn G (1998) Polyadenylation of oop RNA in the regulation of bacteriophage lambda development. Gene 212:57-65
72. Wu J, Xie J (2009) Magic spot: (p) ppGpp. J Cell Physiol 220:297-302
73. 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 266:5980-5990
74. Xu F, Cohen SN (1995) RNA degradation in Escherichia coli regulated by 3' adenylation and 5' phosphorylation. Nature 374:180-183