Caught at its own game: Regulatory small RNA inactivated by an inducible transcript mimicking its target

Genes and Development

Volumn 23, Issue 17, 2009, Pages 2004-2015

  Figueroa Bossi, Nara ^a   Valentini, Martina ^a,b   Malleret, Laurette ^a   Bossi, Lionello ^a  

^a CNRS   (France)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Antisense regulation; Chitobiose; Chitoporin; Hfq; Small RNA

Indexed keywords

BACTERIAL RNA; CHITIN; OLIGOSACCHARIDE; OUTER MEMBRANE PROTEIN;

ARTICLE; BACTERIAL GENE; CHIP GENE; CHIX GENE; GENE CONTROL; GENE MUTATION; GENE SILENCING; GENETIC STABILITY; GENETIC TRANSCRIPTION; NONHUMAN; OPERON; PRIORITY JOURNAL; SALMONELLA;

BACTERIAL PROTEINS; BASE SEQUENCE; DNA MUTATIONAL ANALYSIS; GENE EXPRESSION REGULATION, BACTERIAL; HOST FACTOR 1 PROTEIN; MICRORNAS; MOLECULAR SEQUENCE DATA; MUTATION; PORINS; RNA STABILITY; SALMONELLA;

ENTEROBACTERIACEAE; SALMONELLA;

EID: 69749123311     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.541609     Document Type: Article

References (69)

1. Aiba H. 2007. Mechanism of RNA silencing by Hfq-binding small RNAs. Curr Opin Microbiol 10: 134-139. (Pubitemid 46590050)
2. Aiba H, Hanamura A, Yamano H. 1991. Transcriptional terminator is a positive regulatory element in the expression of the Escherichia coli crp gene. J Biol Chem 266: 1721-1727. (Pubitemid 21908362)
3. Babitzke P, Romeo T. 2007. CsrB sRNA family: Sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 10: 156-163. (Pubitemid 46590047)
4. Bertani G. 2004. Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J Bacteriol 186: 595-600. (Pubitemid 38129635)
5. Bossi L, Figueroa-Bossi N. 2007. A small RNA downregulates LamB maltoporin in Salmonella. Mol Microbiol 65: 799-810. (Pubitemid 47077237)
6. Bouvier M, Sharma CM, Mika F, Nierhaus KH, Vogel J. 2008. Small RNA binding to 59 mRNA coding region inhibits translational initiation. Mol Cell 32: 827-837.
7. Brennan RG, Link TM. 2007. Hfq structure, function and ligand binding. Curr Opin Microbiol 10: 125-133.
8. Brown L, Elliott T. 1996. Efficient translation of the RpoS s factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J Bacteriol 178: 3763-3770. (Pubitemid 26227190)
9. Chen S, Zhang A, Blyn LB, Storz G. 2004. MicC, a second small- RNA regulator of Omp protein expression in Escherichia coli. J Bacteriol 186: 6689-6697. (Pubitemid 39332105)
10. Cisneros B, Court D, Sanchez A, Montanez C. 1996. Point mutations in a transcription terminator, l tI, that affect both transcription termination and RNA stability. Gene 181: 127-133. (Pubitemid 26418259)
11. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci 97: 6640-6645.
12. Ding Y, Davis BM, Waldor MK. 2004. Hfq is essential for Vibrio cholerae virulence and downregulates σ expression. Mol Microbiol 53: 345-354. (Pubitemid 38901403)
13. Douchin V, Bohn C, Bouloc P. 2006. Down-regulation of porins by a small RNA bypasses the essentiality of the regulated intramembrane proteolysis protease RseP in Escherichia coli. J Biol Chem 281: 12253-12259. (Pubitemid 43855309)
14. Ellermeier CD, Janakiraman A, Slauch JM. 2002. Construction of targeted single copy lac fusions using λ Red and FLP-mediated site-specific recombination in bacteria. Gene 290: 153-161. (Pubitemid 34615918)
15. Escott GM, Adams DJ. 1995. Chitinase activity in human serum and leukocytes. Infect Immun 63: 4770-4773.
16. Figueroa-Bossi N, Coissac E, Netter P, Bossi L. 1997. Unsuspected prophage-like elements in Salmonella typhimurium. Mol Microbiol 25: 161-173. (Pubitemid 27316129)
17. E-dependent envelope stress response in Salmonella enterica. Mol Microbiol 62: 838-852.
18. Francetic O, Belin D, Badaut C, Pugsley AP. 2000. Expression of the endogenous type II secretion pathway in Escherichia coli leads to chitinase secretion. EMBO J 19: 6697-6703. (Pubitemid 32011662)
19. Geissmann TA, Touati D. 2004. Hfq, a new chaperoning role: Binding to messenger RNA determines access for small RNA regulator. EMBO J 23: 396-405. (Pubitemid 38294504)
20. Gottesman S, McCullen CA, Guillier M, Vanderpool CK, Majdalani N, Benhammou J, Thompson KM, FitzGerald PC, Sowa NA, FitzGerald DJ. 2006. Small RNA regulators and the bacterial response to stress. Cold Spring Harb Symp Quant Biol 71: 1-11.
21. Guarneros G, Portier C. 1991. Different specificities of ribonuclease II and polynucleotide phosphorylase in 3′mRNA decay. Biochimie 73: 543-549.
22. Guillier M, Gottesman S, Storz G. 2006. Modulating the outer membrane with small RNAs. Genes & Dev 20: 2338-2348. (Pubitemid 44320382)
23. 32-mediated cytoplasmic stress response in Escherichia coli. J Bacteriol 189: 1963-1973.
24. Kachroo AH, Kancherla AK, Singh NS, Varshney U, Mahadevan S. 2007. Mutations that alter the regulation of the chb operon of Escherichia coli allow utilization of cellobiose. Mol Microbiol 66: 1382-1395. (Pubitemid 350179676)
25. Kaspar S, Bott M. 2002. The sensor kinase CitA (DpiB) of Escherichia coli functions as a high-affinity citrate receptor. Arch Microbiol 177: 313-321. (Pubitemid 34230668)
26. Keyhani NO, Roseman S. 1997. Wild-type Escherichia coli grows on the chitin disaccharide, N,N′-diacetylchitobiose, by expressing the cel operon. Proc Natl Acad Sci 94: 14367-14371. (Pubitemid 128617558)
27. Keyhani NO,Li XB, Roseman S. 2000. Chitin catabolism in the marine bacterium Vibrio furnissii. Identification and molecular cloning of a chitoporin. J Biol Chem 275: 33068-33076.
28. Lapouge K, Schubert M, Allain FH, Haas D. 2008. Gac/Rsm signal transduction pathway of γ-proteobacteria: From RNA recognition to regulation of social behaviour. Mol Microbiol 67: 241-253. (Pubitemid 350295835)
29. Lemire S, Figueroa-Bossi N, Bossi L. 2008. A singular case of prophage complementation in mutational activation of recET orthologs in Salmonella enterica serovar Typhimurium. J Bacteriol 190: 6857-6866.
30. Lutgens M, Gottschalk G. 1980. Why a co-substrate is required for anaerobic growth of Escherichia coli on citrate. J Gen Microbiol 119: 63-70. (Pubitemid 10013721)
31. 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 95: 12462-12467. (Pubitemid 28483787)
32. Majdalani N, Vanderpool CK, Gottesman S. 2005. Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 40: 93-113.
33. Maloy SR, Roth JR. 1983. Regulation of proline utilization in Salmonella typhimurium: Characterization of put:Mu d(Ap, lac) operon fusions. J Bacteriol 154: 561-568.
34. Mandin P, Gottesman S. 2009. A genetic approach for finding small RNAs regulators of genes of interest identifies RybC as regulating the DpiA/DpiB two-component system. Mol Microbiol 72: 551-565.
35. Massé E, Gottesman S. 2002. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci 99: 4620-4625.
36. MasséE, Escorcia FE, Gottesman S. 2003. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes & Dev 17: 2374-2383. (Pubitemid 37214786)
37. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, Porwollik S, Ali J, Dante M, Du F, et al. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852-856. (Pubitemid 33026853)
38. Miller JH. 1992. A short course in bacterial genetics. A laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Mizuno T, Chou MY, Inouye M. 1984. A unique mechanism regulating gene expression: Translational inhibition by a complementary RNA transcript (micRNA). Proc Natl Acad Sci 81: 1966-1970. (Pubitemid 14146587)
40. Moll I, Afonyushkin T, Vytvytska O, Kaberdin VR, Bläsi U. 2003. Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. RNA 9: 1308-1314. (Pubitemid 37310861)
41. Morita T, Maki K, Aiba H. 2005. RNase E-based ribonucleoprotein complexes: Mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes & Dev 19: 2176-2186. (Pubitemid 41330319)
42. Morita T, Mochizuki Y, Aiba H. 2006. Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction. Proc Natl Acad Sci 103: 4858-4863.
43. Mott JE, Galloway JL, Platt T. 1985. Maturation of Escherichia coli tryptophan operon mRNA: Evidence for 3′ exonucleolytic processing after rho-dependent termination. EMBO J 4: 1887-1891.
44. Padalon-Brauch G, Hershberg R, Elgrably-Weiss M, Baruch K, Rosenshine I, Margalit H, Altuvia S. 2008. Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res 36: 1913-1927.
45. Papenfort K, Pfeiffer V, Mika F, Lucchini S, Hinton JC, Vogel J. 2006. σE-Dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol Microbiol 62: 1674-1688. (Pubitemid 44813812)
46. Plumbridge J, Pellegrini O. 2004. Expression of the chitobiose operon of Escherichia coli is regulated by three transcription factors: NagC, ChbR and CAP. Mol Microbiol 52: 437-449. (Pubitemid 38520714)
47. 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: 1421-1429. (Pubitemid 41705419)
48. Rasmussen AA, Johansen J, Nielsen JS, Overgaard M, Kallipolitis B, Valentin-Hansen P. 2009. A conserved small RNA promotes silencing of the outer membrane protein YbfM. Mol Microbiol 72: 566-577.
49. Santiviago CA, Toro CS, Hidalgo AA, Youderian P, Mora GC. 2003. Global regulation of the Salmonella enterica serovar typhimurium major porin, OmpD. J Bacteriol 185: 5901-5905. (Pubitemid 37176504)
50. Schmieger H. 1972. Phage P22-mutants with increased or decreased transduction abilities. Mol Gen Genet 119: 75-88.
51. Seitz H. 2009. Redefining MicroRNA targets. Curr Biol 19: 1-4.
52. Sittka A, Pfeiffer V, Tedin K, Vogel J. 2007. The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol Microbiol 63: 193-217. (Pubitemid 44968119)
53. Soper TJ, Woodson SA. 2008. The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 14: 1907-1917.
54. Storz G, Opdyke JA, Zhang A. 2004. Controlling mRNA stability and translation with small, noncoding RNAs. Curr Opin Microbiol 7: 140-144. (Pubitemid 38447046)
55. E Regulates and is regulated by a small RNA in Escherichia coli. J Bacteriol 189: 4243-4256.
56. E Controls biogenesis of the antisense RNA MicA. Nucleic Acids Res 35: 1279-1288.
57. Udekwu KI, Darfeuille F, Vogel J, Reimegard J, Holmqvist E, Wagner EG. 2005. Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes & Dev 19: 2355-2366. (Pubitemid 41396912)
58. Uzzau S, Figueroa-Bossi N, Rubino S, Bossi L. 2001. Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci 98: 15264-15269. (Pubitemid 34014003)
59. Valentin-Hansen P, Johansen J, Rasmussen AA. 2007. Small RNAs controlling outer membrane porins. Curr Opin Microbiol 10: 152-155. (Pubitemid 46590041)
60. Vogel J. 2009. A rough guide to the non-coding RNA world of Salmonella. Mol Microbiol 71: 1-11.
61. Vogel J, Papenfort K. 2006. Small non-coding RNAs and the bacterial outer membrane. Curr Opin Microbiol 9: 605-611. (Pubitemid 44791989)
62. Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jager JG, Huttenhofer A, Wagner EG. 2003. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 31: 6435-6443. (Pubitemid 37508747)
63. Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S. 2001. Identification of novel small RNAs using comparative genomics and microarrays. Genes & Dev 15: 1637-1651. (Pubitemid 32702586)
64. Waters LS, Storz G. 2009. Regulatory RNAs in bacteria. Cell 136: 615-628.
65. Yamamoto K, Matsumoto F, Minagawa S, Oshima T, Fujita N, Ogasawara N, Ishihama A. 2009. Characterization of CitA-CitB signal transduction activating genes involved in anaerobic citrate catabolism in Escherichia coli. Biosci Biotechnol Biochem 73: 346-350.
66. Yu D, Ellis HM, Lee EC, Jenkins NA, Copeland NG, Court DL. 2000. An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci 97: 5978-5983. (Pubitemid 30367509)
67. 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: 11-22. (Pubitemid 34127767)
68. Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, Gottesman S. 2003. Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol 50: 1111-1124. (Pubitemid 37475847)
69. Zhu Z, Zheng T, Homer RJ, Kim YK, Chen NY, Cohn L, Hamid Q, Elias JA. 2004. Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science 304: 1678-1682. (Pubitemid 38765861)