Hfq binding changes the structure of Escherichia coli small noncoding RNAs OxyS and RprA, which are involved in the riboregulation of rpoS

RNA

Volumn 19, Issue 8, 2013, Pages 1089-1104

  Henderson, Charlotte A ^a   Vincent, Helen A ^a,d   Casamento, Alessandra ^a,e   Stone, Carlanne M ^a   Phillips, Jack O ^a   Cary, Peter D ^a   Sobott, Frank ^b,c   Gowers, Darren M ^a   Taylor, James E N ^a   Callaghan, Anastasia J ^a  

^a UNIVERSITY OF PORTSMOUTH   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e UNIVERSITY OF PALERMO   (Italy)

Author keywords

Hfq; OxyS; rpoS; RprA; sRNA

Indexed keywords

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RIBONUCLEASE E; RNA BINDING PROTEIN; SMALL UNTRANSLATED RNA; SUCCINATE DEHYDROGENASE (UBIQUINONE); TRANSFER RNA;

ARTICLE; BINDING AFFINITY; CHROMATOPHORE; COMPLEX FORMATION; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RNA BINDING; RNA CONFORMATION; RNA DEGRADATION; RNA STABILITY; STOICHIOMETRY; SURFACE PLASMON RESONANCE; ULTRACENTRIFUGATION;

EID: 84880678756     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.034595.112     Document Type: Article

References (86)

1. Ali Azam T, Iwata A, Nishimura A, Ueda S, Ishihama A. 1999. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181: 6361-6370.
2. Altuvia S, Weinstein-Fischer D, Zhang A, Postow L, Storz G. 1997. A small, stable RNA induced by oxidative stress: Role as a pleiotropic regulator and antimutator. Cell 90: 43-53.
3. Altuvia S, Zhang A, Argaman L, Tiwari A, Storz G. 1998. The Escherichia coli OxyS regulatory RNA represses fhlA translation by blocking ribosome binding. EMBO J 17: 6069-6075.
4. Aparicio F, Vilar M, Perez-Paya E, Pallas V. 2003. The coat protein of prunus necrotic ringspot virus specifically binds to and regulates the conformation of its genomic RNA. Virology 313: 213-223.
5. Argaman L, Altuvia S. 2000. fhlA repression by OxyS RNA: Kissing complex formation at two sites results in a stable antisense-target RNA complex. J Mol Biol 300: 1101-1112.
6. Bandyra KJ, Said N, Pfeiffer V, Gorna MW, Vogel J, Luisi BF. 2012. The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol Cell 47: 943-953.
7. Beich-Frandsen M, Vecerek B, Konarev PV, Sjöblom B, Kloiber K, Hämmerle H, Rajkowitsch L, Miles AJ, Kontaxis G, Wallace BA, et al. 2011a. Structural insights into the dynamics and function of the C-terminus of the E. coli RNA chaperone Hfq. Nucleic Acids Res 39: 4900-4915.
8. Beich-Frandsen M, Vecerek B, Sjoblom B, Blasi U, Djinovic-Carugo K. 2011b. Structural analysis of full-length Hfq from Escherichia coli. Acta Crystallogr Sect F Struct Biol Cryst Commun 67: 536-540.
9. Brescia CC, Mikulecky PJ, Feig AL, Sledjeski DD. 2003. Identification of the Hfq-binding site on DsrA RNA: Hfq binds without altering DsrA secondary structure. RNA 9: 33-43.
10. Brown L, Elliott T. 1997. Mutations that increase expression of the rpoS gene and decrease its dependence on hfq function in Salmonella typhimurium. J Bacteriol 179: 656-662.
11. Callaghan AJ, Grossmann JG, Redko YU, Ilag LL, Moncrieffe MC, Symmons MF, Robinson CV, McDowall KJ, Luisi BF. 2003. Quaternary structure and catalytic activity of the Escherichia coli ribonuclease E amino-terminal catalytic domain. Biochemistry 42: 13848-13855.
12. Carmichael GG, Weber K, Niveleau A, Wahba AJ. 1975. The host factor required for RNA phage Qβ RNA replication in vitro: Intracellular location, quantitation, and purification by polyadenylate-cellulose chromatography. J Biol Chem 250: 3607-3612.
13. Daly TJ, Rusche JR, Maione TE, Frankel AD. 1990. Circular dichroism studies of the HIV-1 Rev protein and its specific RNA binding site. Biochemistry 29: 9791-9795.
14. de Haseth PL, Uhlenbeck OC. 1980. Interaction of Escherichia coli host factor protein with oligoriboadenylates. Biochemistry 19: 6138-6146.
15. De Lay N, Schu DJ, Gottesman S. 2013. Bacterial small RNA-based negative regulation: Hfq and its accomplices. J Biol Chem 288: 7966-8003.
16. Deana A, Celesnik H, Belasco JG. 2008. The bacterial enzyme RppH triggers messenger RNA degradation by 5' pyrophosphate removal. Nature 451: 355-358.
17. Fender A, Elf J, Hampel K, Zimmermann B, Wagner EG. 2010. RNAs actively cycle on the Sm-like protein Hfq. Genes Dev 24: 2621-2626.
18. Folichon M, Arluison V, Pellegrini O, Huntzinger E, Regnier P, Hajnsdorf E. 2003. The poly(A) binding protein Hfq protects RNA from RNase E and exoribonucleolytic degradation. Nucleic Acids Res 31: 7302-7310.
19. Franke D, Svergun DI. 2009. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J Appl Cryst 42: 342-346.
20. Gao X, Yo P, Keith A, Ragan TJ, Harris TK. 2003. Thermodynamically balanced inside-out (TBIO) PCR-based gene synthesis: A novel method of primer design for high-fidelity assembly of longer gene sequences. Nucleic Acids Res 31: e143.
21. Henderson CA, Vincent HA, Stone CM, Phillips JO, Cary PD, Gowers DM, Callaghan AJ. 2013. Characterization of MicA interactions suggests a potential novel means of gene regulation by small non-coding RNAs. Nucleic Acids Res 41: 3386-3397.
22. Hussein R, Lim HN. 2011. Disruption of small RNA signaling caused by competition for Hfq. Proc Natl Acad Sci 108: 1110-1115.
23. Ishikawa H, Otaka H, Maki K, Morita T, Aiba H. 2012. The functional Hfq-binding module of bacterial sRNAs consists of a double or single hairpin preceded by a U-rich sequence and followed by a 3' poly (U) tail. RNA 18: 1062-1074.
24. Kaberdin VR, Walsh AP, Jakobsen T, McDowall KJ, von Gabain A. 2000. Enhanced cleavage of RNA mediated by an interaction between substrates and the arginine-rich domain of E. coli ribonuclease E. J Mol Biol 301: 257-264.
25. Kajitani M, Kato A, Wada A, Inokuchi Y, Ishihama A. 1994. Regulation of the Escherichia coli hfq gene encoding the host factor for phage Qβ. J Bacteriol 176: 531-534.
26. Konarev PV, Petoukhov MV, Svergun DI. 2001. MASSHA-a graphic system for rigid body modelling of macromolecular complexes against solution scattering data. J Appl Cryst 34: 527-532.
27. Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI. 2003. PRIMUS: A Windows PC-based system for small-angle scattering data analysis. J Appl Cryst 36: 1277-1282.
28. Kozin MB, Svergun DI. 2001. Automated matching of high-and lowresolution structural models. J Appl Cryst 34: 33-41.
29. Lease RA, Woodson SA. 2004. Cycling of the Sm-like protein Hfq on the DsrA small regulatory RNA. J Mol Biol 344: 1211-1223.
30. Lease RA, Cusick ME, Belfort M. 1998. Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci. Proc Natl Acad Sci 95: 12456-12461.
31. LinkTM,Valentin-HansenP, Brennan RG. 2009. Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc Natl Acad Sci 106: 19292-19297.
32. Mackie GA. 1998. Ribonuclease E is a 5'-end-dependent endonuclease. Nature 395: 720-723.
33. 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.
34. 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: 1382-1394.
35. 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: 813-826.
36. Mandin P, Gottesman S. 2010. Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 29: 3094-3107.
37. McCullen CA, Benhammou JN, Majdalani N, Gottesman S. 2010. Mechanism of positive regulation by DsrA and RprA small noncoding RNAs: Pairing increases translation and protects rpoS mRNA from degradation. J Bacteriol 192: 5559-5571.
38. McDowall KJ, Lin-Chao S, Cohen SN. 1994. A+U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. J Biol Chem 269: 10790-10796.
39. McDowall KJ, Kaberdin VR,Wu SW, Cohen SN, Lin-Chao S. 1995. Sitespecific RNase E cleavage of oligonucleotides and inhibition by stem-loops. Nature 374: 287-290.
40. Melefors O, von Gabain A. 1988. Site-specific endonucleolytic cleavages and the regulation of stability of E. coliompAmRNA.Cell 52: 893-901.
41. Mika F, Busse S, Possling A, Berkholz J, Tschowri N, Sommerfeldt N, Pruteanu M, Hengge R. 2012. Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. Mol Microbiol 84: 51-65.
42. Mikulecky PJ, Kaw MK, Brescia CC, Takach JC, Sledjeski DD, Feig AL. 2004. Escherichia coli Hfq has distinct interaction surfaces for DsrA, rpoS and poly(A) RNAs. Nat Struct Mol Biol 11: 1206-1214.
43. Moll I, Afonyushkin T, Vytvytska O, Kaberdin VR, Blasi U. 2003. Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. RNA 9: 1308-1314.
44. 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.
45. Olejniczak M.2011. Despite similar binding to the Hfq protein regulatory RNAs widely differ in their competition performance. Biochemistry 50: 4427-4440.
46. Olsen AS, Møller-Jensen J, Brennan RG, Valentin-Hansen P. 2010. Cterminally truncated derivatives of Escherichia coli Hfq are proficient in riboregulation. J Mol Biol 404: 173-182.
47. Otaka H, Ishikawa H, Morita T, Aiba H. 2011. PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action. Proc Natl Acad Sci 108: 13059-13064.
48. Panja S, Woodson SA. 2012. Hfq proximity and orientation controls RNA annealing. Nucleic Acids Res 40: 8690-8697.
49. Pfeiffer V, Papenfort K, Lucchini S, Hinton JC, Vogel J. 2009. Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat Struct Mol Biol 16: 840-846.
50. Prevost K, Desnoyers G, Jacques JF, Lavoie F, Masse E. 2011. Small RNA-induced mRNA degradation achieved through both translation block and activated cleavage. Genes Dev 25: 385-396.
51. 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.
52. 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: 855-861.
53. Ribeiro Ede A Jr, Beich-Frandsen M, Konarev PV, ShangW, Vecerek B, Kontaxis G, Hämmerle H, Peterlik H, Svergun DI, Bläsi U, et al. 2012. Structural flexibility of RNA as molecular basis for Hfq chaperone function. Nucleic Acids Res 40: 8072-8084.
54. Sahagan BG, Dahlberg JE. 1979. A small, unstable RNA molecule of Escherichia coli: Spot 42 RNA. II: Accumulation and distribution. J Mol Biol 131: 593-605.
55. Salim NN, Feig AL. 2010. An upstream Hfq binding site in the fhlA mRNA leader region facilitates the OxyS-fhlA interaction. PLoS One 5: e13028.
56. Sauer E, Weichenrieder O. 2011. Structural basis for RNA 3'-end recognition by Hfq. Proc Natl Acad Sci 108: 13065-13070.
57. Sauer E, Schmidt S, Weichenrieder O. 2012. Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition. Proc Natl Acad Sci 109: 9396-9401.
58. Sauter C, Basquin J, Suck D. 2003. Sm-like proteins in Eubacteria: The crystal structure of the Hfq protein from Escherichia coli. Nucleic Acids Res 31: 4091-4098.
59. Schuck P. 2000. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys J 78: 1606-1619.
60. SchumacherMA,PearsonRF, MollerT,Valentin-HansenP,BrennanRG. 2002. Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: A bacterial Sm-like protein. EMBO J 21: 3546-3556.
61. Sharma S, Ding F, Dokholyan NV. 2008. iFoldRNA: Three-dimensional RNA structure prediction and folding. Bioinformatics 24: 1951-1952.
62. Shi H, Moore PB. 2000. The crystal structure of yeast phenylalanine tRNA at 1.93 Å resolution: A classic structure revisited. RNA 6: 1091-1105.
63. 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: 3993-4000.
64. Sledjeski DD, Whitman C, Zhang A. 2001. Hfq is necessary for regulation by the untranslated RNA DsrA. J Bacteriol 183: 1997-2005.
65. Sobott F, McCammon MG, Hernandez H, Robinson CV. 2005. The flight of macromolecular complexes in a mass spectrometer. Philos Transact A Math Phys Eng Sci 363: 379-391.
66. Sobott F, Halford SE, Jacklin AJ, Marshall JJT, Smith RM. 2010. DNA nanomachines investigated by non-denaturing mass spectrometry. Biophys J 98: 9a.
67. Soper TJ, Woodson SA. 2008. The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 14: 1907-1917.
68. Soper T, Mandin P, Majdalani N, Gottesman S, Woodson SA. 2010. Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci 107: 9602-9607.
69. Soper TJ, Doxzen K, Woodson SA. 2011. Major role for mRNA binding and restructuring in sRNA recruitment by Hfq. RNA 17: 1544-1550.
70. Svergun D. 1992. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Cryst 25: 495-503.
71. Svergun DI, Nierhaus KH. 2000. A map of protein-rRNA distribution in the 70 S Escherichia coli ribosome. J Biol Chem 275: 14432-14439.
72. Tan R, Frankel AD. 1992. Circular dichroism studies suggest that TAR RNA changes conformation upon specific binding of arginine or guanidine. Biochemistry 31: 10288-10294.
73. Updegrove TB, Wartell RM. 2011. The influence of Escherichia coli Hfq mutations on RNA binding and sRNA·mRNA duplex formation in rpoS riboregulation. Biochim Biophys Acta 1809: 532-540.
74. 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: 11184-11195.
75. Updegrove TB, Correia JJ, Chen Y, Terry C, Wartell RM. 2011. The stoichiometry of the Escherichia coli Hfq protein bound to RNA. RNA 17: 489-500.
76. Vassilieva IM, Rouzanov MV, Zelinskaya NV, Moll I, Blasi U, Garber MB. 2002. Cloning, purification, and crystallization of a bacterial gene expression regulator-Hfq protein from Escherichia coli. Biochemistry (Mosc) 67: 1293-1297.
77. Vecerek B, Rajkowitsch L, Sonnleitner E, Schroeder R, Blasi U. 2008. The C-terminal domain of Escherichia coli Hfq is required for regulation. Nucleic Acids Res 36: 133-143.
78. Vincent HA, Henderson CA, Ragan TJ, Garza-Garcia A, Cary PD, Gowers DM, Malfois M, Driscoll PC, Sobott F, Callaghan AJ. 2012a. Characterization of Vibrio cholerae Hfq provides novel insights into the role of the Hfq C-terminal region. J Mol Biol 420: 56-69.
79. Vincent HA, Henderson CA, Stone CM, Cary PD, Gowers DM, Sobott F, Taylor JE, Callaghan AJ. 2012b. The low-resolution solution structure of Vibrio cholerae Hfq in complex with Qrr1 sRNA. Nucleic Acids Res 40: 8698-8710.
80. Volkov VV, Svergun DI. 2003. Uniqueness of ab initio shape determination in small-angle scattering. J Appl Cryst 36: 860-864.
81. Vytvytska O, Moll I, Kaberdin VR, von Gabain A, Blasi U. 2000. Hfq (HF1) stimulates ompA mRNA decay by interfering with ribosome binding. Genes Dev 14: 1109-1118.
82. Wang W, Wang L, Zou Y, Zhang J, Gong Q, Wu J, Shi Y. 2011. Cooperation of Escherichia coli Hfq hexamers in DsrA binding. Genes Dev 25: 2106-2117.
83. Whitten AE, Cai SZ, Trewhella J. 2008. MULCh: Modules for the analysis of small-angle neutron contrast variation data from biomolecular assemblies. J Appl Cryst 41: 222-226.
84. Zhang A, Altuvia S, Tiwari A, Argaman L, Hengge-Aronis R, Storz G. 1998. The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J 17: 6061-6068.
85. Zhang A, Wassarman KM, Ortega J, Steven AC, Storz G. 2002. The Smlike Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 9: 11-22.
86. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415.