Turn-over of the small non-coding RNA RprA in E. coli is influenced by osmolarity

Molecular Genetics and Genomics

Volumn 284, Issue 4, 2010, Pages 307-318

  Madhugiri, Ramakanth ^a   Basineni, Sobha Rani ^a   Klug, Gabriele ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Osmotic stress; RpoS mRNA; RprA; Srna stability; Temperature

Indexed keywords

CHAPERONE; MESSENGER RNA; PROTEIN HFQ; RIBONUCLEASE E; RIBONUCLEASE III; SIGMA FACTOR RPOS; SUCROSE; UNCLASSIFIED DRUG; UNTRANSLATED RNA; ADENOSINE TRIPHOSPHATE; BACTERIAL DNA; BACTERIAL PROTEIN; BACTERIAL RNA; ESCHERICHIA COLI PROTEIN; HFQ PROTEIN, E COLI; HOST FACTOR 1; OXYS PROTEIN, E COLI; PRIMER DNA; REPRESSOR PROTEIN; RIBONUCLEASE; SIGMA FACTOR; SIGMA FACTOR KATF PROTEIN, BACTERIA;

ARTICLE; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OSMOLARITY; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA METABOLISM; RNA STABILITY; TEMPERATURE DEPENDENCE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; HALF LIFE TIME; ISOLATION AND PURIFICATION; METABOLISM; NORTHERN BLOTTING; PHYSIOLOGY; PROTEIN SYNTHESIS; TRANSCRIPTION INITIATION;

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; BLOTTING, NORTHERN; DNA PRIMERS; DNA, BACTERIAL; ENDORIBONUCLEASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOTYPE; HALF-LIFE; HOST FACTOR 1 PROTEIN; OSMOLAR CONCENTRATION; PROTEIN BIOSYNTHESIS; REPRESSOR PROTEINS; RIBONUCLEASE III; RNA, BACTERIAL; RNA, MESSENGER; RNA, UNTRANSLATED; SIGMA FACTOR; TRANSCRIPTIONAL ACTIVATION;

EID: 78049423172     PISSN: 16174615     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00438-010-0568-x     Document Type: Article

References (41)

1. Afonyushkin T, Vecerek B, Moll I, Blasi U, Kaberdin VR (2005) Both RNase E and RNase III control the stability of sodB mRNA upon translational inhibition by the small regulatory RNA RyhB. Nucleic Acids Res 33(5):1678-1689. DOI:10.1093/nar/gki313 (Pubitemid 41418396)
2. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, Margalit H, Altuvia S (2001) Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 11(12): 941-950. DOI:S0960-9822(01)00270-6
3. Basineni SR, Madhugiri R, Kolmsee T, Hengge R, Klug G (2009) The influence of Hfq and ribonucleases on the stability of the small non-coding RNA OxyS and its target rpoS in E. coli is growth phase dependent. RNA Biol 6(5):584-594
4. Becker G, Klauck E, Hengge-Aronis R (1999) Regulation of RpoS proteolysis in Escherichia coli: The response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. Proc Natl Acad Sci USA 96(11):6439-6444
5. Berghoff BA, Glaeser J, Sharma CM, Vogel J, Klug G (2009) Photooxidative stress-induced and abundant small RNAs in Rhodobacter sphaeroides. Mol Microbiol 74(6):1497-1512. DOI: 10.1111/j.1365-2958.2009.06949.x
6. Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The Complete Genome Sequence of Escherichia coli K-12. Science 277:1453-1462 (Pubitemid 27449228)
7. Brandi A, Pietroni P, Gualerzi CO, Pon CL (1996) Post-transcrip-tional regulation of CspA expression in Escherichia coli. Mol Microbiol 19(2):231-240
8. Carpousis AJ (2007) The RNA degradosome of Escherichia coli:An mRNA-degrading machine assembled on RNase E. Annu Rev Microbiol 61:71-87. DOI:10.1146/annurev.micro.61.080706.093440 (Pubitemid 350058200)
9. Conrad C, Rauhut R, Klug G (1998) Different cleavage specificities of RNase III from Rhodobacter capsulatus and Escherichia coli. Nucleic Acids Res 26(19):4446-4453
10. Frohlich KS, Vogel J (2009) Activation of gene expression by small RNA. Curr Opin Microbiol 12(6):674-682. DOI:10.1016/j.mib.2009.09.009
11. Goldblum K, Apririon D (1981) Inactivation of the ribonucleic acid-processing enzyme ribonuclease E blocks cell division. J Bacte-riol 146(1):128-132
12. Goldenberg D, Azar I, Oppenheim AB (1996) Differential mRNA stability of the cspA gene in the cold-shock response of Escherichia coli. Mol Microbiol 19(2):241-248
13. Heck C, Rothfuchs R, Jager A, Rauhut R, Klug G (1996) Effect of the pufQ-pufB intercistronic region on puf mRNA stability in Rhodobacter capsulatus. Mol Microbiol 20(6):1165-1178
14. Hengge-Aronis R (2002) Stationary phase gene regulation: What makes an Escherichia coli promoter sigma S-selective? Curr Opin Microbiol 5(6):591-595. DOI:S1369527402003727
15. Jager S, Fuhrmann O, Heck C, Hebermehl M, Schiltz E, Rauhut R, Klug G (2001) An mRNA degrading complex in Rhodobacter capsulatus. Nucleic Acids Res 29(22):4581-4588
16. Jager S, Evguenieva-Hackenberg E, Klug G (2004) Temperature-dependent processing of the cspA mRNA in Rhodobacter capsulatus. Microbiology 150(Pt 3):687-695
17. Mackie GA (1992) Secondary structure of the mRNA for ribosomal protein S20. Implications for cleavage by ribonuclease E. J Biol Chem 267(2):1054-1061
18. Majdalani N, Cunning C, Sledjeski D, Elliott T, Gottesman S (1998) DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc Natl Acad Sci USA 95(21):12462-12467
19. Majdalani N, Chen S, Murrow J, St John K, Gottesman S (2001) Regulation of RpoS by a novel small RNA: The characterization of RprA. Mol Microbiol 39(5):1382-1394
20. Majdalani N, Hernandez D, Gottesman S (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46(3):813-826
21. Masse E, Escorcia FE, Gottesman S (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 17(19):2374-2383. DOI:10.1101/gad.11271031127103
22. Py B, Causton H, Mudd EA, Higgins CF (1994) A protein complex mediating mRNA degradation in Escherichia coli. Mol Micro-biol 14(4):717-729
23. Rasmussen AA, Eriksen M, Gilany K, Udesen C, Franch T, Petersen C, Valentin-Hansen P (2005) Regulation of ompA mRNA stability: The role of a small regulatory RNA in growth phase-dependent control. Mol Microbiol 58(5):1421-1429. DOI:10.1111/j.1365-2958.2005.04911.x (Pubitemid 41705419)
24. Rauhut R, Klug G (1999) mRNA degradation in bacteria. FEMS Microbiol Rev 23(3):353-370. DOI:S0168-6445(99)00012-1
25. 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 polyadenylation in Escherichia coli. Nucleic Acids Res 36(8): 2570-2580. DOI:10.1093/nar/gkn091 (Pubitemid 351659572)
26. Repoila F, Gottesman S (2001) Signal transduction cascade for regulation of RpoS: Temperature regulation of DsrA. J Bacteriol 183(13):4012-W23. DOI:10.1128/JB.183.13.4012-4023.2001 (Pubitemid 32565482)
27. Repoila F, Gottesman S (2003) Temperature sensing by the dsrA promoter. J Bacteriol 185(22):6609-6614
28. Repoila F, Majdalani N, Gottesman S (2003) Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: The RpoS paradigm. Mol Microbiol 48(4):855-861
29. Resch A, Afonyushkin T, Lombo TB, McDowall KJ, Blasi U, Kaberdin VR (2008) Translational activation by the noncoding RNA DsrA involves alternative RNase III processing in the rpoS 5'-leader. RNA 14(3):454-459. DOI:10.1261/rna.603108 (Pubitemid 351397810)
30. Robert-Le Meur M, Portier C (1992) E. coli polynucleotide phosphorylase expression is autoregulated through an RNase III-dependent mechanism. EMBO J 11(7):2633-2641
31. Schweder T, Lee KH, Lomovskaya O, Matin A (1996) Regulation of Escherichia coli starvation sigma factor (sigma S) by ClpXp protease. J Bacteriol 178(2):470-476
32. Sledjeski D, Gottesman S (1995) A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli. Proc Natl Acad Sci USA 92(6):2003-2007
33. Sledjeski DD, Gupta A, Gottesman S (1996) The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J 15(15): 3993-4000
34. Sledjeski DD, Whitman C, Zhang A (2001) Hfq is necessary for regulation by the untranslated RNA DsrA. J Bacteriol 183(6):1997-2005. DOI:10.1128/JB.183. 6.1997-2005.2001 (Pubitemid 32225995)
35. Studier F (1975) Genetic mapping of a mutation that causes ribonuclease III deficiency in Escherichia coli. J Bacteriol 124:307-316
36. Updegrove T, Wilf N, Sun X, Wartell RM (2008) Effect of Hfq on RprA-rpoS mRNA pairing: Hfq-RNA binding and the influence of the 5' rpoS mRNA leader region. Biochemistry 47(43): 11184-11195. DOI:10.1021/bi800479p
37. Urban JH, Vogel J (2007) Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res 35(3):1018-1037. DOI:10.1093/nar/gkl1040 (Pubitemid 46344726)
38. Valverde C, Haas D (2008) Small RNAs controlled by two-component systems. Adv Exp Med Biol 631:54-79. DOI:10.1007/ 978-0-387-78885-2-5
39. Vecerek B, Beich-Frandsen M, Resch A, Blasi U (2010) Translational activation of rpoS mRNA by the non-coding RNA DsrA and Hfq does not require ribosome binding. Nucleic Acids Res 38:1284-1293. DOI:10.1093/nar/gkp1125
40. Vogel J, Argaman L, Wagner EG, Altuvia S (2004) The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr Biol 14(24):2271-2276. DOI:10.1016/j.cub.2004.12.003 (Pubitemid 40033365)
41. Zhang A, Wassarman KM, Ortega J, Steven AC, Storz G (2002) The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 9(1):11-22. DOI:S1097276501004373