The social fabric of the RNA degradosome

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1829, Issue 6-7, 2013, Pages 514-522

  Bandyra, Katarzyna J ^a   Bouvier, Marie ^b   Carpousis, Agamemnon J ^b   Luisi, Ben F ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UPS   (France)

Author keywords

Ribonuclease; RNA decay; RNA degradosome; RNA processing; RNase E; SRNA

Indexed keywords

BACTERIAL RNA; ENZYME; RIBONUCLEASE E; RNA DEGRADOSOME; RNA HELICASE; TRANSFER RNA; UNCLASSIFIED DRUG;

CATALYSIS; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; HUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN QUATERNARY STRUCTURE; REGULATORY RNA SEQUENCE; REVIEW; RNA DEGRADATION; RNA PROCESSING;

CELL MEMBRANE; ENDORIBONUCLEASES; ESCHERICHIA COLI; MULTIENZYME COMPLEXES; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RNA HELICASES; RNA STABILITY; RNA, BACTERIAL;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84877795525     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2013.02.011     Document Type: Review

References (90)

1. Dressaire C., Picard F., Redon E., Loubière P., Queinnec I., Girbal L., Cocaign-Bousquet M. Role of mRNA stability during bacterial adaptation. PloS One 2013, 8:e59059. 10.1371/journal.pone.0059059.
2. Miller C., Schwalb B., Maier K., Schulz D., Dumcke S., Zacher B., Mayer A., Sydow J., Marcinowski L., Dolken L., Martin D.E., Tresch A., Cramer P. Dynamic transcriptome analysis measures rates of mRNA synthesis and decay in yeast. Mol. Syst. Biol. 2011, 7:458.
3. Richards J., Sundermeier T., Svetlanov A., Karzai A.W. Quality control of bacterial mRNA decoding and decay. Biochim. Biophys. Acta 2008, 1779:574-582.
4. Selinger D.W., Saxena R.M., Cheung K.J., Church G.M., Rosenow C. Global RNA half-life analysis in Escherichia coli reveals positional patterns of transcript degradation. Genome Res. 2003, 13:216-223.
5. Carpousis A.J. The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol. 2007, 61:71-87.
6. Stead M.B., Marshburn S., Mohanty B.K., Mitra J., Pena Castillo L., Ray D., van Bakel H., Hughes T.R., Kushner S.R. Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays. Nucleic Acids Res. 2010, 39:3188-3203.
7. Mackie G.A. Ribonuclease E is a 5'-end-dependent endonuclease. Nature 1998, 395:720-723.
8. Celesnik H., Deana A., Belasco J.G. Initiation of RNA decay in Escherichia coli by 5' pyrophosphate removal. Mol. Cell 2007, 27:79-90.
9. Deana A., Celesnik H., Belasco J.G. The bacterial enzyme RppH triggers messenger RNA degradation by 5' pyrophosphate removal. Nature 2008, 451:355-358.
10. Callaghan A.J., Marcaida M.J., Stead J.A., McDowall K.J., Scott W.G., Luisi B.F. Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature 2005, 437:1187-1191.
11. Garrey S.M., Blech M., Riffell J.L., Hankins J.S., Stickney L.M., Diver M., Hsu Y.H., Kunanithy V., Mackie G.A. Substrate binding and active site residues in RNases E and G: role of the 5'-sensor. J. Biol. Chem. 2009, 284:31843-31850.
12. Baker K.E., Mackie G.A. Ectopic RNase E sites promote bypass of 5'-end-dependent mRNA decay in Escherichia coli. Mol. Microbiol. 2003, 47:75-88.
13. Dreyfus M. Killer and protective ribosomes. Prog. Mol. Biol. Transl. Sci. 2009, 85:423-466.
14. Joyce S.A., Dreyfus M. In the absence of translation, RNase E can bypass 5' mRNA stabilizers in Escherichia coli. J. Mol. Biol. 1998, 282:241-254.
15. Leroy A., Vanzo N.F., Sousa S., Dreyfus M., Carpousis A.J. Function in Escherichia coli of the non-catalytic part of RNase E: role in the degradation of ribosome-free mRNA. Mol. Microbiol. 2002, 45:1231-1243.
16. Lopez P.J., Marchand I., Joyce S.A., Dreyfus M. The C-terminal half of RNase E, which organizes the Escherichia coli degradosome, participates in mRNA degradation but not rRNA processing in vivo. Mol. Microbiol. 1999, 33:188-199.
17. Anupama K., Leela J.K., Gowrishankar J. Two pathways for RNase E action in Escherichia coli in vivo and bypass of its essentiality in mutants defective for Rho-dependent transcription termination. Mol. Microbiol. 2011, 82:1330-1348.
18. Bouvier M., Carpousis A.J. A tale of two mRNA degradation pathways mediated by RNase E. Mol. Microbiol. 2011, 82:1305-1310.
19. Garrey S.M., Mackie G.A. Roles of the 5'-phosphate sensor domain in RNase E. Mol. Microbiol. 2011, 80:1613-1624.
20. Callaghan A.J., Aurikko J.P., Ilag L.L., Gunter Grossmann J., Chandran V., Kuhnel K., Poljak L., Carpousis A.J., Robinson C.V., Symmons M.F., Luisi B.F. Studies of the RNA degradosome-organizing domain of the Escherichia coli ribonuclease RNase E. J. Mol. Biol. 2004, 340:965-979.
21. Marcaida M.J., DePristo M.A., Chandran V., Carpousis A.J., Luisi B.F. The RNA degradosome: life in the fast lane of adaptive molecular evolution. Trends Biochem. Sci. 2006, 31:359-365.
22. Py B., Causton H., Mudd E.A., Higgins C.F. A protein complex mediating mRNA degradation in Escherichia coli. Mol. Microbiol. 1994, 14:717-729.
23. 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.
24. 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.
25. Gorna M.W., Carpousis A.J., Luisi B.F. From conformational chaos to robust regulation: the structure and function of the multi-enzyme RNA degradosome. Q. Rev. Biophys. 2012, 45:105-145.
26. 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.
27. 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.
28. Chandran V., Luisi B.F. Recognition of enolase in the Escherichia coli RNA degradosome. J. Mol. Biol. 2006, 358:8-15.
29. 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.
30. Carpousis A.J., Van Houwe G., Ehretsmann C., Krisch H.M. Copurification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell 1994, 76:889-900.
31. Taraseviciene L., Bjork G.R., Uhlin B.E. Evidence for an RNA binding region in the Escherichia coli processing endoribonuclease RNase E. J. Biol. Chem. 1995, 270:26391-26398.
32. 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.
33. Lee K., Cohen S.N. A Streptomyces coelicolor functional orthologue of Escherichia coli RNase E shows shuffling of catalytic and PNPase-binding domains. Mol. Microbiol. 2003, 48:349-360.
34. Kovacs L., Csanadi A., Megyeri K., Kaberdin V.R., Miczak A. Mycobacterial RNase E-associated proteins. Microbiol. Immunol. 2005, 49:1003-1007.
35. Ait-Bara S., Carpousis A.J. Characterization of the RNA degradosome of Pseudoalteromonas haloplanktis: conservation of the RNase E-RhlB interaction in the gammaproteobacteria. J. Bacteriol. 2010, 192:5413-5423.
36. Erce M.A., Low J.K., Wilkins M.R. Analysis of the RNA degradosome complex in Vibrio angustum S14. FEBS J. 2010, 277:5161-5173.
37. Hardwick S.W., Chan V.S., Broadhurst R.W., Luisi B.F. An RNA degradosome assembly in Caulobacter crescentus. Nucleic Acids Res. 2011, 39:1449-1459.
38. 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.
39. 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.
40. Yang J., Jain C., Schesser K. RNase E regulates the Yersinia type 3 secretion system. J. Bacteriol. 2008, 190:3774-3778.
41. Condon C., Putzer H. The phylogenetic distribution of bacterial ribonucleases. Nucleic Acids Res. 2002, 30:5339-5346.
42. Even S., Pellegrini O., Zig L., Labas V., Vinh J., Brechemmier-Baey D., Putzer H. Ribonucleases J1 and J2: two novel endoribonucleases in B.subtilis with functional homology to E.coli RNase E. Nucleic Acids Res. 2005, 33:2141-2152.
43. 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.
44. Li de la Sierra-Gallay I., Zig L., Jamalli A., Putzer H. Structural insights into the dual activity of RNase J. Nat. Struct. Mol. Biol. 2008, 15:206-212.
45. Shahbabian K., Jamalli A., Zig L., Putzer H. RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J. 2009, 28:3523-3533.
46. 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.
47. Lehnik-Habrink M., Pfortner H., Rempeters L., Pietack N., Herzberg C., Stulke J. The RNA degradosome in Bacillus subtilis: identification of CshA as the major RNA helicase in the multiprotein complex. Mol. Microbiol. 2010, 77:958-971.
48. Mathy N., Hebert A., Mervelet P., Benard L., Dorleans A., Li de la Sierra-Gallay I., Noirot P., Putzer H., Condon C. Bacillus subtilis ribonucleases J1 and J2 form a complex with altered enzyme behaviour. Mol. Microbiol. 2010, 75:489-498.
49. Redko Y., Aubert S., Stachowicz A., Lenormand P., Namane A., Darfeuille F., Thibonnier M., De Reuse H. A minimal bacterial RNase J-based degradosome is associated with translating ribosomes. Nucleic Acids Res. 2013, 41:288-301.
50. Koslover D.J., Callaghan A.J., Marcaida M.J., Garman E.F., Martick M., Scott W.G., Luisi B.F. The crystal structure of the Escherichia coli RNase E apoprotein and a mechanism for RNA degradation. Structure 2008, 16:1238-1244.
51. Kaberdin V.R. Probing the substrate specificity of Escherichia coli RNase E using a novel oligonucleotide-based assay. Nucleic Acids Res. 2003, 31:4710-4716.
52. Jourdan S.S., McDowall K.J. Sensing of 5' monophosphate by Escherichia coli RNase G can significantly enhance association with RNA and stimulate the decay of functional mRNA transcripts in vivo. Mol. Microbiol. 2008, 67:102-115.
53. Nakamura T., Zhao Y., Yamagata Y., Hua Y.J., Yang W. Watching DNA polymerase eta make a phosphodiester bond. Nature 2012, 487:196-201.
54. Rott R., Zipor G., Portnoy V., Liveanu V., Schuster G. RNA polyadenylation and degradation in cyanobacteria are similar to the chloroplast but different from Escherichia coli. J. Biol. Chem. 2003, 278:15771-15777.
55. Bandyra K.J., Said N., Pfeiffer V., Gorna M.W., Vogel J., Luisi B.F. The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol. Cell 2012, 47:943-953.
56. McLennan A.G. The Nudix hydrolase superfamily. Cell Mol. Life Sci. 2006, 63:123-143.
57. Ow M.C., Liu Q., Kushner S.R. Analysis of mRNA decay and rRNA processing in Escherichia coli in the absence of RNase E-based degradosome assembly. Mol. Microbiol. 2000, 38:854-866.
58. Kaberdin V.R., Walsh A.P., Jakobsen T., McDowall K.J., von Gabain A. Enhanced cleavage of RNA mediated by an interaction between substrates and the arginine-rich domain of E. coli ribonuclease E. J. Mol. Biol. 2000, 301:257-264.
59. Nurmohamed S., Vaidialingam B., Callaghan A.J., Luisi B.F. Crystal structure of Escherichia coli polynucleotide phosphorylase core bound to RNase E, RNA and manganese: implications for catalytic mechanism and RNA degradosome assembly. J. Mol. Biol. 2009, 389:17-33.
60. Stickney L.M., Hankins J.S., Miao X., Mackie G.A. Function of the conserved S1 and KH domains in polynucleotide phosphorylase. J. Bacteriol. 2005, 187:7214-7221.
61. Symmons M.F., Jones G.H., Luisi B.F. A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity, and regulation. Structure 2000, 8:1215-1226.
62. Gottesman S., Storz G. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb. Perspect. Biol. 2011, 3.
63. Papenfort K., Vogel J. Regulatory RNA in bacterial pathogens. Cell Host Microbe 2010, 8:116-127.
64. Vogel J., Luisi B.F. Hfq and its constellation of RNA. Nat. Rev. Microbiol. 2011, 9:578-589.
65. Balbontin R., Fiorini F., Figueroa-Bossi N., Casadesus J., Bossi L. Recognition of heptameric seed sequence underlies multi-target regulation by RybB small RNA in Salmonella enterica. Mol. Microbiol. 2010, 78:380-394.
66. Papenfort K., Bouvier M., Mika F., Sharma C.M., Vogel J. Evidence for an autonomous 5' target recognition domain in an Hfq-associated small RNA. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20435-20440.
67. Sauer E., Schmidt S., Weichenrieder O. Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:9396-9401.
68. Aiba H. Mechanism of RNA silencing by Hfq-binding small RNAs. Curr. Opin. Microbiol. 2007, 10:134-139.
69. Caron M.P., Lafontaine D.A., Masse E. Small RNA-mediated regulation at the level of transcript stability. RNA Biol. 2010, 7:140-144.
70. Masse E., Escorcia F.E., Gottesman S. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev. 2003, 17:2374-2383.
71. Pfeiffer V., Papenfort K., Lucchini S., Hinton J.C., Vogel J. Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat. Struct. Mol. Biol. 2009, 16:840-846.
72. Viegas S.C., Pfeiffer V., Sittka A., Silva I.J., Vogel J., Arraiano C.M. Characterization of the role of ribonucleases in Salmonella small RNA decay. Nucleic Acids Res. 2007, 35:7651-7664.
73. Prevost K., Desnoyers G., Jacques J.F., Lavoie F., Masse E. Small RNA-induced mRNA degradation achieved through both translation block and activated cleavage. Genes Dev. 2011, 25:385-396.
74. Ikeda Y., Yagi M., Morita T., Aiba H. Hfq binding at RhlB-recognition region of RNase E is crucial for the rapid degradation of target mRNAs mediated by sRNAs in Escherichia coli. Mol. Microbiol. 2011, 79:419-432.
75. Morita T., Kawamoto H., Mizota T., Inada T., Aiba H. Enolase in the RNA degradosome plays a crucial role in the rapid decay of glucose transporter mRNA in the response to phosphosugar stress in Escherichia coli. Mol. Microbiol. 2004, 54:1063-1075.
76. Worrall J.A., Gorna M., Crump N.T., Phillips L.G., Tuck A.C., Price A.J., Bavro V.N., Luisi B.F. Reconstitution and analysis of the multienzyme Escherichia coli RNA degradosome. J. Mol. Biol. 2008, 382:870-883.
77. Tsai Y.C., Du D., Dominguez-Malfavon L., Dimastrogiovanni D., Cross J., Callaghan A.J., Garcia-Mena J., Luisi B.F. Recognition of the 70S ribosome and polysome by the RNA degradosome in Escherichia coli. Nucleic Acids Res. 2012, 40:10417-10431.
78. Takyar S., Hickerson R.P., Noller H.F. mRNA helicase activity of the ribosome. Cell 2005, 120:49-58.
79. Khemici V., Poljak L., Luisi B.F., Carpousis A.J. The RNase E of Escherichia coli is a membrane-binding protein. Mol. Microbiol. 2008, 70:799-813.
80. Murashko O.N., Kaberdin V.R., Lin-Chao S. Membrane binding of Escherichia coli RNase E catalytic domain stabilizes protein structure and increases RNA substrate affinity. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:7019-7024.
81. Taghbalout A., Rothfield L. RNaseE and the other constituents of the RNA degradosome are components of the bacterial cytoskeleton. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:1667-1672.
82. Parlitz R., Eitan A., Stjepanovic G., Bahari L., Bange G., Bibi E., Sinning I. Escherichia coli signal recognition particle receptor FtsY contains an essential and autonomous membrane-binding amphipathic helix. J. Biol. Chem. 2007, 282:32176-32184.
83. Pichoff S., Lutkenhaus J. Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol. Microbiol. 2005, 55:1722-1734.
84. Salje J., van den Ent F., de Boer P., Lowe J. Direct membrane binding by bacterial actin MreB. Mol. Cell 2011, 43:478-487.
85. Zhou H., Lutkenhaus J. Membrane binding by MinD involves insertion of hydrophobic residues within the C-terminal amphipathic helix into the bilayer. J. Bacteriol. 2003, 185:4326-4335.
86. Montero Llopis P., Jackson A.F., Sliusarenko O., Surovtsev I., Heinritz J., Emonet T., Jacobs-Wagner C. Spatial organization of the flow of genetic information in bacteria. Nature 2010, 466:77-81.
87. Lehnik-Habrink M., Newman J., Rothe F.M., Solovyova A.S., Rodrigues C., Herzberg C., Commichau F.M., Lewis R.J., Stulke J. RNase Y in Bacillus subtilis: a natively disordered protein that is the functional equivalent of RNase E from Escherichia coli. J. Bacteriol. 2011, 193:5431-5441.
88. Lodato P.B., Hsieh P.K., Belasco J.G., Kaper J.B. The ribosome binding site of a mini-ORF protects a T3SS mRNA from degradation by RNase E. Mol. Microbiol. 2012, 86:1167-1182.
89. Richards J., Luciano D.J., Belasco J.G. Influence of translation on RppH-dependent mRNA degradation in Escherichia coli. Mol. Microbiol. 2012, 86:1063-1072.
90. Mackie G.A. RNase E: at the interface of bacterial RNA processing and decay. Nat. Rev. Microbiol. 2013, 11:45-57.