Bacterial helicases in post-transcriptional control

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1829, Issue 8, 2013, Pages 878-883

  Kaberdin, Vladimir R ^a,b   Bläsi, Udo ^c  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b BASQUE FOUNDATION FOR SCIENCE   (Spain)

^c UNIVERSITY OF VIENNA   (Austria)

Author keywords

Bacterium; MRNA stability; RNA helicase; Translation

Indexed keywords

DEAD BOX PROTEIN; DEAH BOX HELICASE; RNA HELICASE; UNCLASSIFIED DRUG;

CONTROLLED STUDY; ENZYME DEGRADATION; ENZYME METABOLISM; ENZYME STABILITY; ESCHERICHIA COLI; NONHUMAN; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; PROTEIN FAMILY; REGULATORY MECHANISM; REVIEW; RNA DEGRADATION; RNA PROCESSING; RNA STRUCTURE; RNA TRANSCRIPTION; TEMPERATURE SENSITIVITY; TRANSLATION INITIATION;

BACTERIA; DEAD-BOX RNA HELICASES; RNA; RNA PROCESSING, POST-TRANSCRIPTIONAL;

BACTERIA (MICROORGANISMS);

EID: 84877921782     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2012.12.005     Document Type: Review

References (86)

1. Singleton M.R., Dillingham M.S., Wigley D.B. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 2007, 76:23-50.
2. Rabni M., Raumoni R., Boudvillain M. Transcription termination factor Rho: a ring-shaped RNA helicase from bacteria. RSC Biomolecular Sciences 2010, vol. 19:243-271. E. Jankowski (Ed.).
3. Tanner N.K., Cordin O., Banroques J., Doere M., Linder P. The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol. Cell 2003, 11:127-138.
4. Linder P., Lasko P.F., Ashburner M., Leroy P., Nielsen P.J., Nishi K., Schnier J., Slonimski P.P. Birth of the D-E-A-D box. Nature 1989, 337:121-122.
5. Py B., Higgins C.F., Krisch H.M., Carpousis A.J. A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature 1996, 381:169-172.
6. Bizebard T., Ferlenghi I., Iost I., Dreyfus M. Studies on three E. coli DEAD-box helicases point to an unwinding mechanism different from that of model DNA helicases. Biochemistry 2004, 43:7857-7866.
7. Turner A.M., Love C.F., Alexander R.W., Jones P.G. Mutational analysis of the Escherichia coli DEAD box protein CsdA. J. Bacteriol. 2007, 189:2769-2776.
8. Charollais J., Pflieger D., Vinh J., Dreyfus M., Iost I. The DEAD-box RNA helicase SrmB is involved in the assembly of 50S ribosomal subunits in Escherichia coli. Mol. Microbiol. 2003, 48:1253-1265.
9. Peil L., Virumae K., Remme J. Ribosome assembly in Escherichia coli strains lacking the RNA helicase DeaD/CsdA or DbpA. FEBS J. 2008, 275:3772-3782.
10. Nishi K., Morel-Deville F., Hershey J.W., Leighton T., Schnier J. An eIF-4A-like protein is a suppressor of an Escherichia coli mutant defective in 50S ribosomal subunit assembly. Nature 1988, 336:496-498.
11. Toone W.M., Rudd K.E., Friesen J.D. deaD, a new Escherichia coli gene encoding a presumed ATP-dependent RNA helicase, can suppress a mutation in rpsB, the gene encoding ribosomal protein S2. J. Bacteriol. 1991, 173:3291-3302.
12. Moll I., Grill S., Grundling A., Blasi U. Effects of ribosomal proteins S1, S2 and the DeaD/CsdA DEAD-box helicase on translation of leaderless and canonical mRNAs in Escherichia coli. Mol. Microbiol. 2002, 44:1387-1396.
13. Prud'homme-Genereux A., Beran R.K., Iost I., Ramey C.S., Mackie G.A., Simons R.W. Physical and functional interactions among RNase E, polynucleotide phosphorylase and the cold-shock protein, CsdA: evidence for a 'cold shock degradosome'. Mol. Microbiol. 2004, 54:1409-1421.
14. Yamanaka K., Inouye M. Selective mRNA degradation by polynucleotide phosphorylase in cold shock adaptation in Escherichia coli. J. Bacteriol. 2001, 183:2808-2816.
15. Jones P.G., Mitta M., Kim Y., Jiang W., Inouye M. Cold shock induces a major ribosomal-associated protein that unwinds double-stranded RNA in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:76-80.
16. Fuller-Pace F.V., Nicol S.M., Reid A.D., Lane D.P. DbpA: a DEAD box protein specifically activated by 23S rRNA. EMBO J. 1993, 12:3619-3626.
17. Diges C.M., Uhlenbeck O.C. Escherichia coli DbpA is an RNA helicase that requires hairpin 92 of 23S rRNA. EMBO J. 2001, 20:5503-5512.
18. Tsu C.A., Kossen K., Uhlenbeck O.C. The Escherichia coli DEAD protein DbpA recognizes a small RNA hairpin in 23S rRNA. RNA 2001, 7:702-709.
19. Coburn G.A., Miao X., Briant D.J., Mackie G.A. Reconstitution of a minimal RNA degradosome demonstrates functional coordination between a 3' exonuclease and a DEAD-box RNA helicase. Genes Dev. 1999, 13:2594-2603.
20. Khemici V., Toesca I., Poljak L., Vanzo N.F., Carpousis A.J. The RNase E of Escherichia coli has at least two binding sites for DEAD-box RNA helicases: functional replacement of RhlB by RhlE. Mol. Microbiol. 2004, 54:1422-1430.
21. Jain C. The E. coli RhlE RNA helicase regulates the function of related RNA helicases during ribosome assembly. RNA 2008, 14:381-389.
22. Charollais J., Dreyfus M., Iost I. CsdA, a cold-shock RNA helicase from Escherichia coli, is involved in the biogenesis of 50S ribosomal subunit. Nucleic Acids Res. 2004, 32:2751-2759.
23. Morita M., Kanemori M., Yanagi H., Yura T. Heat-induced synthesis of sigma32 in Escherichia coli: structural and functional dissection of rpoH mRNA secondary structure. J. Bacteriol. 1999, 181:401-410.
24. Morita M.T., Tanaka Y., Kodama T.S., Kyogoku Y., Yanagi H., Yura T. Translational induction of heat shock transcription factor sigma32: evidence for a built-in RNA thermosensor. Genes Dev. 1999, 13:655-665.
25. Tamura M., Kers J.A., Cohen S.N. Second-site suppression of RNase E essentiality by mutation of the deaD RNA helicase in Escherichia coli. J. Bacteriol. 2012, 194:1919-1926.
26. Chamot D., Magee W.C., Yu E., Owttrim G.W. A cold shock-induced cyanobacterial RNA helicase. J. Bacteriol. 1999, 181:1728-1732.
27. Rosana A.R., Chamot D., Owttrim G.W. Autoregulation of RNA helicase expression in response to temperature stress in Synechocystis sp. PCC 6803. PLoS One 2012, 7:e48683.
28. Rosana A.R., Ventakesh M., Chamot D., Patterson-Fortin L.M., Tarassova O., Espie G.S., Owttrim G.W. Inactivation of a low temperature-induced RNA helicase in Synechocystis sp. PCC 6803: physiological and morphological consequences. Plant Cell Physiol. 2012, 53:646-658.
29. Prakash J.S., Krishna P.S., Sirisha K., Kanesaki Y., Suzuki I., Shivaji S., Murata N. An RNA helicase, CrhR, regulates the low-temperature-inducible expression of heat-shock genes groES, groEL1 and groEL2 in Synechocystis sp. PCC 6803. Microbiology 2010, 156:442-451.
30. Lu J., Aoki H., Ganoza M.C. Molecular characterization of a prokaryotic translation factor homologous to the eukaryotic initiation factor eIF4A. Int. J. Biochem. Cell Biol. 1999, 31:215-229.
31. Butland G., Krogan N.J., Xu J., Yang W.H., Aoki H., Li J.S., Krogan N., Menendez J., Cagney G., Kiani G.C., Jessulat M.G., Datta N., Ivanov I., Abouhaidar M.G., Emili A., Greenblatt J., Ganoza M.C., Golshani A. Investigating the in vivo activity of the DeaD protein using protein-protein interactions and the translational activity of structured chloramphenicol acetyltransferase mRNAs. J. Cell. Biochem. 2007, 100:642-652.
32. Storz G., Vogel J., Wassarman K.M. Regulation by small RNAs in bacteria: expanding frontiers. Mol. Cell 2011, 43:880-891.
33. Frohlich K.S., Vogel J. Activation of gene expression by small RNA. Curr. Opin. Microbiol. 2009, 12:674-682.
34. Repoila F., Majdalani N., Gottesman S. Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. Mol. Microbiol. 2003, 48:855-861.
35. Sledjeski D.D., Gupta A., Gottesman S. The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J. 1996, 15:3993-4000.
36. Sledjeski D.D., Whitman C., Zhang A. Hfq is necessary for regulation by the untranslated RNA DsrA. J. Bacteriol. 2001, 183:1997-2005.
37. Resch A., Afonyushkin T., Lombo T.B., McDowall K.J., Blasi U., Kaberdin V.R. Translational activation by the noncoding RNA DsrA involves alternative RNase III processing in the rpoS 5'-leader. RNA 2008, 14:454-459.
38. Soper T.J., Woodson S.A. The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 2008, 14:1907-1917.
39. Resch A., Vecerek B., Palavra K., Blasi U. Requirement of the CsdA DEAD-box helicase for low temperature riboregulation of rpoS mRNA. RNA Biol. 2010, 7:796-802.
40. Butland G., Peregrin-Alvarez J.M., Li J., Yang W., Yang X., Canadien V., Starostine A., Richards D., Beattie B., Krogan N., Davey M., Parkinson J., Greenblatt J., Emili A. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 2005, 433:531-537.
41. Iost I., Dreyfus M. mRNAs can be stabilized by DEAD-box proteins. Nature 1994, 372:193-196.
42. Carpousis A.J. The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol. 2007, 61:71-87.
43. Kaberdin V.R., Singh D., Lin-Chao S. Composition and conservation of the mRNA-degrading machinery in bacteria. J. Biomed. Sci. 2011, 18:23.
44. Miczak A., Kaberdin V.R., Wei C.L., Lin-Chao S. Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:3865-3869.
45. Kaberdin V.R., Lin-Chao S. Unraveling new roles for minor components of the E. coli RNA degradosome. RNA Biol. 2009, 6:402-405.
46. Carabetta V.J., Silhavy T.J., Cristea I.M. The response regulator SprE (RssB) is required for maintaining poly(A) polymerase I-degradosome association during stationary phase. J. Bacteriol. 2010, 192:3713-3721.
47. Regonesi M.E., Del Favero M., Basilico F., Briani F., Benazzi L., Tortora P., Mauri P., Deho G. Analysis of the Escherichia coli RNA degradosome composition by a proteomic approach. Biochimie 2006, 88:151-161.
48. Bachellier S., Clement J.M., Hofnung M. Short palindromic repetitive DNA elements in enterobacteria: a survey. Res. Microbiol. 1999, 150:627-639.
49. McLaren R.S., Newbury S.F., Dance G.S., Causton H.C., Higgins C.F. mRNA degradation by processive 3'-5' exoribonucleases in vitro and the implications for prokaryotic mRNA decay in vivo. J. Mol. Biol. 1991, 221:81-95.
50. Spickler C., Mackie G.A. Action of RNase II and polynucleotide phosphorylase against RNAs containing stem-loops of defined structure. J. Bacteriol. 2000, 182:2422-2427.
51. Khemici V., Carpousis A.J. The RNA degradosome and poly(A) polymerase of Escherichia coli are required in vivo for the degradation of small mRNA decay intermediates containing REP-stabilizers. Mol. Microbiol. 2004, 51:777-790.
52. Bernstein J.A., Lin P.H., Cohen S.N., Lin-Chao S. Global analysis of Escherichia coli RNA degradosome function using DNA microarrays. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:2758-2763.
53. Chandran V., Poljak L., Vanzo N.F., Leroy A., Miguel R.N., Fernandez-Recio J., Parkinson J., Burns C., Carpousis A.J., Luisi B.F. Recognition and cooperation between the ATP-dependent RNA helicase RhlB and ribonuclease RNase E. J. Mol. Biol. 2007, 367:113-132.
54. Worrall J.A., Howe F.S., McKay A.R., Robinson C.V., Luisi B.F. Allosteric activation of the ATPase activity of the Escherichia coli RhlB RNA helicase. J. Biol. Chem. 2008, 283:5567-5576.
55. Silverman E., Edwalds-Gilbert G., Lin R.J. DExD/H-box proteins and their partners: helping RNA helicases unwind. Gene 2003, 312:1-16.
56. Marintchev A., Edmonds K.A., Marintcheva B., Hendrickson E., Oberer M., Suzuki C., Herdy B., Sonenberg N., Wagner G. Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 2009, 136:447-460.
57. Montpetit B., Thomsen N.D., Helmke K.J., Seeliger M.A., Berger J.M., Weis K. A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export. Nature 2011, 472:238-242.
58. Polach K.J., Uhlenbeck O.C. Cooperative binding of ATP and RNA substrates to the DEAD/H protein DbpA. Biochemistry 2002, 41:3693-3702.
59. Khemici V., Poljak L., Toesca I., Carpousis A.J. Evidence in vivo that the DEAD-box RNA helicase RhlB facilitates the degradation of ribosome-free mRNA by RNase E. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:6913-6918.
60. Iost I., Dreyfus M. The stability of Escherichia coli lacZ mRNA depends upon the simultaneity of its synthesis and translation. EMBO J. 1995, 14:3252-3261.
61. Lee K., Zhan X., Gao J., Qiu J., Feng Y., Meganathan R., Cohen S.N., Georgiou G. RraA. a protein inhibitor of RNase E activity that globally modulates RNA abundance in E. coli. Cell 2003, 114:623-634.
62. Gao J., Lee K., Zhao M., Qiu J., Zhan X., Saxena A., Moore C.J., Cohen S.N., Georgiou G. Differential modulation of E. coli mRNA abundance by inhibitory proteins that alter the composition of the degradosome. Mol. Microbiol. 2006, 61:394-406.
63. Gorna M.W., Pietras Z., Tsai Y.C., Callaghan A.J., Hernandez H., Robinson C.V., Luisi B.F. The regulatory protein RraA modulates RNA-binding and helicase activities of the E. coli RNA degradosome. RNA 2010, 16:553-562.
64. Awano N., Xu C., Ke H., Inoue K., Inouye M., Phadtare S. Complementation analysis of the cold-sensitive phenotype of the Escherichia coli csdA deletion strain. J. Bacteriol. 2007, 189:5808-5815.
65. Awano N., Rajagopal V., Arbing M., Patel S., Hunt J., Inouye M., Phadtare S. Escherichia coli RNase R has dual activities, helicase and RNase. J. Bacteriol. 2010, 192:1344-1352.
66. Jiang W., Hou Y., Inouye M. CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem. 1997, 272:196-202.
67. Lin P.H., Lin-Chao S. RhlB helicase rather than enolase is the beta-subunit of the Escherichia coli polynucleotide phosphorylase (PNPase)-exoribonucleolytic complex. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:16590-16595.
68. Liou G.G., Chang H.Y., Lin C.S., Lin-Chao S. DEAD box RhlB RNA helicase physically associates with exoribonuclease PNPase to degrade double-stranded RNA independent of the degradosome-assembling region of RNase E. J. Biol. Chem. 2002, 277:41157-41162.
69. Lin-Chao S., Chiou N.T., Schuster G. The PNPase, exosome and RNA helicases as the building components of evolutionarily-conserved RNA degradation machines. J. Biomed. Sci. 2007, 14:523-532.
70. Kaberdin V.R., Miczak A., Jakobsen J.S., Lin-Chao S., McDowall K.J., von Gabain A. The endoribonucleolytic N-terminal half of Escherichia coli RNase E is evolutionarily conserved in Synechocystis sp. and other bacteria but not the C-terminal half, which is sufficient for degradosome assembly. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:11637-11642.
71. Vanzo N.F., Li Y.S., Py B., Blum E., Higgins C.F., Raynal L.C., Krisch H.M., Carpousis A.J. Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev. 1998, 12:2770-2781.
72. Erce M.A., Low J.K., March P.E., Wilkins M.R., Takayama K.M. Identification and functional analysis of RNase E of Vibrio angustum S14 and two-hybrid analysis of its interaction partners. Biochim. Biophys. Acta 2009, 1794:1107-1114.
73. Henry A., Shanks J., van Hoof A., Rosenzweig J.A. The Yersinia pseudotuberculosis degradosome is required for oxidative stress, while its PNPase subunit plays a degradosome-independent role in cold growth. FEMS Microbiol. Lett. 2012, 39-47.
74. Ait-Bara S., Carpousis A.J. Characterization of the RNA degradosome of Pseudoalteromonas haloplanktis: conservation of the RNase E-RhlB interaction in the {gamma}-Proteobacteria. J. Bacteriol. 2010, 192:5413-5423.
75. Purusharth R.I., Klein F., Sulthana S., Jager S., Jagannadham M.V., Evguenieva-Hackenberg E., Ray M.K., Klug G. Exoribonuclease R interacts with endoribonuclease E and an RNA helicase in the psychrotrophic bacterium Pseudomonas syringae Lz4W. J. Biol. Chem. 2005, 280:14572-14578.
76. Hardwick S.W., Chan V.S., Broadhurst R.W., Luisi B.F. An RNA degradosome assembly in Caulobacter crescentus. Nucleic Acids Res. 2010, 449-459.
77. Jager S., Fuhrmann O., Heck C., Hebermehl M., Schiltz E., Rauhut R., Klug G. An mRNA degrading complex in Rhodobacter capsulatus. Nucleic Acids Res. 2001, 29:4581-4588.
78. Bechhofer D.H. Messenger RNA decay and maturation in Bacillus subtilis. Prog. Mol. Biol. Transl. Sci. 2009, 85:231-273.
79. Lehnik-Habrink M., Lewis R.J., Mader U., Stulke J. RNA degradation in Bacillus subtilis: an interplay of essential endo- and exoribonucleases. Mol. Microbiol. 2012, 84:1005-1017.
80. Commichau F.M., Rothe F.M., Herzberg C., Wagner E., Hellwig D., Lehnik-Habrink M., Hammer E., Volker U., Stulke J. Novel activities of glycolytic enzymes in Bacillus subtilis: interactions with essential proteins involved in mRNA processing. Mol. Cell. Proteomics 2009, 8:1350-1360.
81. Roux C.M., DeMuth J.P., Dunman P.M. Characterization of components of the Staphylococcus aureus mRNA degradosome holoenzyme-like complex. J. Bacteriol. 2011, 193:5520-5526.
82. Oun S., Redder P., Didier J.P., Francois P., Corvaglia A.R., Buttazzoni E., Giraud C., Girard M., Schrenzel J., Linder P. The CshA DEAD-box RNA helicase is important for quorum sensing control in Staphylococcus aureus. RNA Biol. 2012, 10.
83. Moriya H., Kasai H., Isono K. Cloning and characterization of the hrpA gene in the terC region of Escherichia coli that is highly similar to the DEAH family RNA helicase genes of Saccharomyces cerevisiae. Nucleic Acids Res. 1995, 23:595-598.
84. Koo J.T., Choe J., Moseley S.L. HrpA, a DEAH-box RNA helicase, is involved in mRNA processing of a fimbrial operon in Escherichia coli. Mol. Microbiol. 2004, 52:1813-1826.
85. Salman-Dilgimen A., Hardy P.O., Dresser A.R., Chaconas G. HrpA, a DEAH-box RNA helicase, is involved in global gene regulation in the Lyme disease spirochete. PLoS One 2011, 6:e22168.
86. Jankowsky A., Guenther U.P., Jankowsky E. The RNA helicase database. Nucleic Acids Res. 2011, 39:D338-341.