Recognition of the 70S ribosome and polysome by the RNA degradosome in Escherichia coli

Nucleic Acids Research

Volumn 40, Issue 20, 2012, Pages 10417-10431

  Tsai, Yi Chun ^a   Du, Dijun ^a   Domínguez Malfavón, Lilianha ^b   Dimastrogiovanni, Daniela ^a   Cross, Jonathan ^a   Callaghan, Anastasia J ^c   García Mena, Jaime ^b   Luisi, Ben F ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c UNIVERSITY OF PORTSMOUTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MULTIPROTEIN COMPLEX; PROTEIN RHLB; RIBONUCLEASE E; RIBOSOME PROTEIN; RNA; RNA 9S; RNA DEGRADOSOME; RNA HELICASE; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

70S RIBOSOME SUBUNIT; ARTICLE; CATALYSIS; COMPLEX FORMATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; IN VIVO STUDY; MOLECULAR RECOGNITION; NONHUMAN; POLYSOME; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RIBOSOME SUBUNIT; RNA PROCESSING;

BINDING SITES; CROSS-LINKING REAGENTS; DEAD-BOX RNA HELICASES; ENDORIBONUCLEASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; MULTIENZYME COMPLEXES; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; POLYRIBOSOMES; PROTEIN INTERACTION DOMAINS AND MOTIFS; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, LARGE, BACTERIAL; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RIBOSOMES; RNA; RNA HELICASES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, SMALL UNTRANSLATED;

ESCHERICHIA COLI;

EID: 84869021523     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks739     Document Type: Article

References (58)

1. Jain, C., Deana, A. and Belasco, J.G. (2002) Consequences of RNase E scarcity in Escherichia coli. Mol. Microbiol., 43, 1053-1064.
2. Ono, M. and Kuwano, M. (1979) A conditional lethal mutation in an Escherichia coli strain with a longer chemical lifetime of messenger RNA. J. Mol. Biol., 129, 343-357.
3. Carpousis, A.J. (2007) The RNA degradosome of Escherichia coli: An mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol., 61, 71-87.
4. Górna, M.W., Carpousis, A.J. and Luisi, B.F. (2011) From conformational chaos to robust regulation: The structure and function of the multi-enzyme RNA degradosome. Q. Rev. Biophys., 45, 105-145.
5. Carabetta, V.J., Silhavy, T.J. and Cristea, I.M. (2010) The response regulator SprE (RssB) is required for maintaining Poly(A) polymerase I-degradosome association during stationary phase. J. Bacteriol., 192, 3713-3721.
6. Prud'homme-Généreux, A., Beran, R.K., Iost, I., Ramey, C.S., Mackie, G.A. and Simons, R.W. (2004) Physical and functional interactions among RNase E, polynucleotide phosphorylase and the cold-shock protein, CsdA: evidence for a 'cold shock degradosome'. Mol. Microbiol., 54, 1409-1421.
7. Worrall, J.A.R., Górna, M., Crump, N.T., Phillips, L.G., Tuck, A.C., Price, A.J., Bavro, V.N. and Luisi, B.F. (2008) Reconstitution and analysis of the multienzyme Escherichia coli RNA degradosome. J. Mol. Biol., 382, 870-883.
8. Ikeda, Y., Yagi, M., Morita, T. and Aiba, H. (2011) 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., 79, 419-432.
9. Morita, T., Kawamoto, H., Mizota, T., Inada, T. and Aiba, H. (2004) 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., 54, 1063-1075.
10. Leroy, A., Vanzo, N.F., Sousa, S., Dreyfus, M. and Carpousis, A.J. (2002) Function in Escherichia coli of the non-catalytic part of RNase E: role in the degradation of ribosome-free mRNA. Mol. Microbiol., 45, 1231-1243.
11. Bernstein, J.A., Lin, P.-H., Cohen, S.N. and Lin-Chao, S. (2004) Global analysis of Escherichia coli RNA degradosome function using DNA microarrays. Proc. Natl Acad. Sci. USA, 101, 2758-2763.
12. Marcaida, M.J., DePristo, M.A., Chandran, V., Carpousis, A.J. and Luisi, B.F. (2006) The RNA degradosome: life in the fast lane of adaptive molecular evolution. Trends Biochem. Sci., 31, 359-365.
13. Carpousis, A.J., Luisi, B.F. and McDowall, K.J. (2009) Endonucleolytic Initiation of mRNA Decay in Escherichia coli. Prog. Mol. Biol. Transl. Sci., 85, 91-135.
14. Symmons, M.F., Williams, M.G., Luisi, B.F., Jones, G.H. and Carpousis, A.J. (2002) Running rings around RNA: a superfamily of phosphate-dependent RNases. Trends Biochem. Sci., 27, 11-18.
15. Bessarab, D.A., Kaberdin, V.R., Wei, C.-L., Liou, G.-G. and Lin- Chao, S. (1998) RNA components of Escherichia coli degradosome: Evidence for rRNA decay. Proc. Natl Acad. Sci. USA, 95, 3157-3161.
16. Ghora, B.K. and Apirion, D. (1978) Structural analysis and in vitro processing to p5 rRNA of a 9S RNA molecule isolated from an rne mutant of E. coli. Cell, 15, 1055-1066.
17. Misra, T.K. and Apirion, D. (1979) RNase E, an RNA processing enzyme from Escherichia coli. J. Biol. Chem., 254, 11154-11159.
18. Cheng, Z.-F. and Deutscher, M.P. (2003) Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. Proc. Natl Acad. Sci. USA, 100, 6388-6393.
19. Butland, G., Peregrin-Alvarez, J.M., Li, J., Yang, W., Yang, X., Canadien, V., Starostine, A., Richards, D., Beattie, B., Krogan, N. et al. (2005) Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature, 433, 531-537.
20. Singh, D., Chang, S.-J., Lin, P.-H., Averina, O.V., Kaberdin, V.R. and Lin-Chao, S. (2009) Regulation of ribonuclease E activity by the L4 ribosomal protein of Escherichia coli. Proc. Natl Acad. Sci., 106, 864-869.
21. Kaberdin, V.R. and Lin-Chao, S. (2009) Unraveling new roles for minor components of the E. coli RNA degradosome. RNA Biol., 6, 402-405.
22. Thiele, I., Fleming, R.M.T., Bordbar, A., Schellenberger, J. and Palsson, B. (2010) Functional characterization of alternate optimal solutions of Escherichia coli's transcriptional and translational machinery. Biophys. J., 98, 2072-2081.
23. Ederth, J., Mandava, C.S., Dasgupta, S. and Sanyal, S. (2009) A single-step method for purification of active His-tagged ribosomes from a genetically engineered Escherichia coli. Nucleic Acids Res., 37, e15.
24. Wang, H.-W., Noland, C., Siridechadilok, B., Taylor, D.W., Ma, E., Felderer, K., Doudna, J.A. and Nogales, E. (2009) Structural insights into RNA processing by the human RISC-loading complex. Nat. Struct. Mol. Biol., 16, 1148-1153.
25. Palva, E.T. and Randall, L.L. (1976) Nearest-neighbor analysis of Escherichia coli Outer membrane proteins, using cleavable cross-links. J. Bacteriol., 127, 1558-1560.
26. Yu, D., Ellis, H.M., Lee, E.-C., Jenkins, N.A., Copeland, N.G. and Court, D.L. (2000) An efficient recombination system for chromosome engineering in Escherichia coli. Proc. Natl Acad. Sci., 97, 5978-5983.
27. Court, D.L., Sawitzke, J.A. and Thomason, L.C. (2002) Genetic engineering using homologous recombination. Annu. Rev. Genet., 36, 361-388.
28. Callaghan, A.J., Grossmann, J.G., Redko, Y.U., Ilag, L.L., Moncrieffe, M.C., Symmons, M.F., Robinson, C.V., McDowall, K.J. and Luisi, B.F. (2003) Quaternary structure and catalytic activity of the Escherichia coli ribonuclease E amino-terminal catalytic domain. Biochemistry, 42, 13848-13855.
29. Callaghan, A.J., Aurikko, J.P., Ilag, L.L., Günter Grossmann, J., Chandran, V., Kühnel, K., Poljak, L., Carpousis, A.J., Robinson, C.V., Symmons, M.F. et al. (2004) Studies of the RNA degradosome-organizing domain of the Escherichia coli ribonuclease RNase E. J. Mol. Biol., 340, 965-979.
30. Worrall, J.A.R., Howe, F.S., McKay, A.R., Robinson, C.V. and Luisi, B.F. (2008) Allosteric activation of the ATPase activity of the Escherichia coli RhlB RNA helicase. J. Biol. Chem., 283, 5567-5576.
31. Khemici, V., Toesca, I., Poljak, L., Vanzo, N.F. and Carpousis, A.J. (2004) 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., 54, 1422-1430.
32. Carpousis, A.J., Van Houwe, G., Ehretsmann, C. and Krisch, H.M. (1994) Copurification of E. coli RNase E and PNPase: Evidence for a specific association between two enzymes important in RNA processing and degradation. Cell, 76, 889-900.
33. Mackie, G.A., Coburn, G.A., Miao, X., Briant, D.J., Prud'homme- Généreux, A., Stickney, L.M., Hankins, J.S., Lynne, E.M. and Cecilia, M.A. (2008) Preparation of the Escherichia coli RNase E Protein and Reconstitution of the RNA Degradosome, Methods in Enzymology. Academic Press, Vol. 447, pp. 199-213.
34. Miczak, A., Kaberdin, V.R., Wei, C.L. and Lin-Chao, S. (1996) Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc. Natl Acad. Sci. USA, 93, 3865-3869.
35. Rasouly, A., Schonbrun, M., Shenhar, Y. and Ron, E.Z. (2009) YbeY, a heat shock protein involved in translation in Escherichia coli. J. Bacteriol., 191, 2649-2655.
36. Górna, M.W., Pietras, Z., Tsai, Y.-C., Callaghan, A.J., Hernández, H., Robinson, C.V. and Luisi, B.F. (2010) The regulatory protein RraA modulates RNA-binding and helicase activities of the E. coli RNA degradosome. RNA, 16, 553-562.
37. Pfeiffer, V., Papenfort, K., Lucchini, S., Hinton, J.C.D. and Vogel, J. (2009) Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat. Struct. Mol. Biol., 16, 840-846.
38. Stark, H. and Grant, J.J. (2010) GraFix: Stabilization of fragile macromolecular complexes for single particle Cryo-EM. Methods Enzymol., 481, 109-126.
39. Nakatogawa, H. and Ito, K. (2002) The ribosomal exit tunnel functions as a discriminating gate. Cell, 108, 629-636.
40. Khemici, V., Poljak, L., Luisi, B.F. and Carpousis, A.J. (2008) The RNase E of Escherichia coli is a membrane-binding protein. Mol. Microbiol., 70, 799-813.
41. Trubetskoy, D., Proux, F., Allemand, F., Dreyfus, M. and Iost, I. (2009) SrmB, a DEAD-box helicase involved in Escherichia coli ribosome assembly, is specifically targeted to 23S rRNA in vivo. Nucleic Acids Res., 37, 6540-6549.
42. Argaman, L., Elgrably-Weiss, M., Hershko, T., Vogel, J. and Altuvia, S. (2012) RelA protein stimulates the activity of RyhB small RNA by acting on RNA-binding protein Hfq. Proc. Natl Acad. Sci. USA, 109, 4621-626.
43. Cormack, R.S. and Mackie, G.A. (1992) Structural requirements for the processing of Escherichia coli 5 S ribosomal RNA by RNase E in vitro. J. Mol. Biol., 228, 1078-1090.
44. Carpousis, A.J., Leroy, A., Vanzo, N. and Khemici, V. (2001) Escherichia coli RNA degradosome, Methods in Enzymology. Academic Press, Vol. 342, pp. 333-345.
45. Morita, T., Maki, K. and Aiba, H. (2005) RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev., 19, 2176-2186.
46. Hardwick, S.W., Chan, V.S.Y., Broadhurst, R.W. and Luisi, B.F. (2011) An RNA degradosome assembly in Caulobacter crescentus. Nucleic Acids Res., 39, 1449-1459.
47. Bremer, H. and Dennix, P.P. (1996) Modulation of Chemical Composition and Other Parameters of the Cell by Growth Rate, 2nd edn American Society for Microbiology, Washington DC.
48. Brandt, F., Etchells, S.A., Ortiz, J.O., Elcock, A.H., Hartl, F.U. and Baumeister, W. (2009) The native 3D organization of bacterial polysomes. Cell, 136, 261-271.
49. Prévost, K., Desnoyers, G., Jacques, J.-F., Lavoie, F. and Massé, E. (2011) Small RNA-induced mRNA degradation achieved through both translation block and activated cleavage. Genes Dev., 25, 385-396.
50. Viegas, S.C., Pfeiffer, V., Sittka, A., Silva, I.J., Vogel, J. and Arraiano, C.M. (2007) Characterization of the role of ribonucleases in Salmonella small RNA decay. Nucleic Acids Res., 35, 7651-7664.
51. Massé, E., Escorcia, F.E. and Gottesman, S. (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev., 17, 2374-2383.
52. Pedersen, K., Zavialov, A.V., Pavlov, M.Y., Elf, J., Gerdes, K. and Ehrenberg, M. (2003) The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell, 112, 131-140.
53. Neubauer, C., Gao, Y.-G., Andersen, K.R., Dunham, C.M., Kelley, A.C., Hentschel, J., Gerdes, K., Ramakrishnan, V. and Brodersen, D.E. (2009) The structural basis for mRNA recognition and cleavage by the ribosome-dependent endonuclease RelE. Cell, 139, 1084-1095.
54. Hayes, C.S., Bose, B. and Sauer, R.T. (2002) Proline residues at the C terminus of nascent chains induce SsrA tagging during translation termination. J. Biol. Chem., 277, 33825-33832.
55. Hayes, C.S. and Sauer, R.T. (2003) Cleavage of the A Site mRNA Codon during ribosome pausing provides a mechanism for translational quality control. Mol. Cell, 12, 903-911.
56. Sunohara, T., Jojima, K., Tagami, H., Inada, T. and Aiba, H. (2004) Ribosome stalling during translation elongation induces cleavage of mRNA being translated in Escherichia coli. J. Biol. Chem., 279, 15368-15375.
57. Doma, M.K. and Parker, R. (2007) RNA quality control in eukaryotes. Cell, 131, 660-668.
58. Becker, T., Armache, J.-P., Jarasch, A., Anger, A.M., Villa, E., Sieber, H., Motaal, B.A., Mielke, T., Berninghausen, O. and Beckmann, R. (2011) Structure of the no-go mRNA decay complex Dom34 -Hbs bound to a stalled 80S ribosome. Nat. Struct. Mol. Biol., 18, 715-720.