The assembly and distribution in vivo of the Escherichia coli RNA degradosome

Biochimie

Volumn 95, Issue 11, 2013, Pages 2034-2041

  Domínguez Malfavón, Lilianha ^a   Islas, León D ^b   Luisi, Ben F ^c   García Villegas, Refugio ^a   García Mena, Jaime ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b Electronic Eng Dept   (Mexico)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Fluorescence energy transfer; Protein distribution; Protein expression; Protein interaction; RNA degradosome

Indexed keywords

BACTERIAL RNA; ENOLASE; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RIBONUCLEASE E;

ARTICLE; BACTERIUM MUTANT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE INTERACTION; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; STOICHIOMETRY;

ESCHERICHIA COLI;

FLUORESCENCE ENERGY TRANSFER; PROTEIN DISTRIBUTION; PROTEIN EXPRESSION; PROTEIN INTERACTION; RNA DEGRADOSOME;

DEAD-BOX RNA HELICASES; ENDORIBONUCLEASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; MICROSCOPY, FLUORESCENCE; MULTIENZYME COMPLEXES; PLASMIDS; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; PROTEIN INTERACTION MAPS; RNA HELICASES;

EID: 84885070661     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2013.07.022     Document Type: Article

References (41)

1. M.F. Symmons, M.G. William, B.F. Luisi, G.H. Jones, and A.J. Carpousis Running rings around RNA: a superfamily of phosphate-dependent Rnases Trends Biochem. Sci. 27 2002 11 19
2. J.M. Caruthers, Y. Feng, D.B. McKay, and S.N. Cohen Retention of core catalytic functions by a conserved minimal ribonuclease E peptide that lacks the domain required for tetramer formation J. Biol. Chem. 281 2006 27046 27051
3. S.N. Cohen, and K.J. McDowall RNase E: still a wonderfully mysterious enzyme Mol. Microbiol. 23 1997 1099 1106
4. A.J. Carpousis The RNA degradosome of Escherichia coli: a multiprotein mRNA-degrading machine assembled on RNase E Annu. Rev. Microbiol. 61 2007 71 87
5. T. Morita, H. Kawamoto, T. Mizota, T. Inada, and H. Aiba 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 2004 1063 1075
6. G.A. Coburn, X. Miao, D.J. Briant, and G.A. Mackie Reconstitution o a minimal RNA degradosome demonstrates functional coordination between a 3′ exonuclease and a DEAD-box RNA helicase Genes Dev. 13 1999 2594 2603
7. J.A. Worrall, M. Górna, N.T. Crump, L.G. Phillips, A.C. Tuck, A.J. Price, V.N. Bavro, and B.F. Luisi Reconstitution and analysis of the multienzyme Escherichia coli RNA degradosome J. Mol. Biol. 382 2008 870 883
8. A. Prud'homme-Généreux, R.K. Beran, I. Iost, C.S. Ramey, G.A. Mackie, and R.W. Simons Physical and functional interactions among RNase E, polynucleotide phosphorylase and the cold-shock protein, CsdA: evidence for a 'cold shock degradosome' Mol. Microbiol. 54 2004 1409 1421
9. V. Khemici, I. Toesca, P. Poljak, N.F. Vanzo, and A.J. Carpousis 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 2004 1422 1430
10. A. Miczak, V.R. Kaberdin, C.L. Wei, and S. Lin-Chao Proteins associated with RNase E in a multicomponent ribonucleolytic complex Proc. Natl. Acad. Sci. U. S. A. 93 1996 3865 3869
11. B. Py, H. Causton, E.A. Mudd, and C.F. Higgins A protein complex mediating mRNA degradation in Escherichia coli Mol. Microbiol. 14 1994 717 729
12. N.F. Vanzo, Y.S. Li, B. Py, E. Blum, C.F. Higgins, L.C. Raynal, H.M. Krisch, and A.J. Carpousis Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome Genes Dev. 12 1998 2770 2781
13. V.R. Kaberdin, and S. Lin-Chao Unraveling new roles for minor components of the E. coli RNA degradosome RNA Biol. 6 2009 402 405
14. S. Jain, B. Pragai, and D. Apirion A possible complex containing RNA processing enzymes Biochem. Biophys. Res. Commun. 106 1982 768 778
15. A.J. Carpousis, G. Van Houwe, C. Ehretsmann, and H.M. Krisch Copurification of E. coli RNase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation Cell 76 1994 889 900
16. G. Butland, J.M. Peregrin-Alvarez, J. Li, W. Yang, X. Yang, V. Canadien, A. Starostine, D. Richards, B. Beattie, N. Krogan, M. Davey, J. Parkinson, J. Greenblatt, and A. Emili Interaction network containing conserved and essential protein complexes in Escherichia coli Nature 433 2005 531 537
17. N.V. Durán-Figueroa, A. Piña-Escobedo, I. Schroeder, R.W. Simons, and J. García-Mena Polynucleotide phosphorylase interacts with ribonuclease E through a ββαββα domain Biochimie 88 2006 725 735
18. J. Gao, K. Lee, M. Zhao, J. Qiu, X. Zhan, A. Saxena, C.J. Moore, S.N. Cohen, and G. Georgiou Differential modulation of E. coli mRNA abundance by inhibitory proteins that alter the composition of the degradosome Mol. Microbiol. 61 2006 384 406
19. T. Morita, K. Maki, and H. Aiba RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs Genes Dev. 19 2005 2176 2186
20. M.E. Regonesi, M. Del Favero, F. Basilico, F. Briani, L. Benazzi, P. Tortora, P. Mauri, and G. Dehò Analysis of the Escherichia coli RNA degradosome composition by a proteomic approach Biochimie 88 2006 151 161
21. S. Jager, M. Hebermehl, E. Schiltz, and G. Klug Composition and activity of the Rhodobacter capsulatus degradosome vary under different oxygen concentrations J. Mol. Microbiol. Biotechnol. 7 2004 148 154
22. S. Baginsky, A. Shteiman-Kotler, V. Liveanu, S. Yehudai-Resheff, M. Bellaoui, R.E. Settlage, J. Shabanowitz, D.F. Hunt, G. Schuster, and W. Gruissem Chloroplast PNPase exists as a homo-multimer enzyme complex that is distinct from the Escherichia coli degradosome RNA 7 2001 1464 1475
23. A. Dziembowski, J. Piwowarski, R. Hoser, M. Minczuk, A. Dmochowska, M. Siep, H. van der Spek, L. Grivell, and P.P. Stepien The yeast mitochondrial degradosome. Its composition, interplay between RNA helicase and RNase activities and the role in mitochondrial RNA metabolism J. Biol. Chem. 278 2003 1603 1611
24. A. Miczak, R.A. Srivastava, and D. Apirion Location of the RNA-processing enzymes RNase III, RNase E and RNase P in the Escherichia coli cell Mol. Microbiol. 5 1991 1801 1810
25. G. Liou, W. Jane, S. Cohen, N. Lin, and S. Lin-Chao RNA degradosomes exist in vivo in Escherichia coli as multicomponent complexes associated with the cytoplasmic membrane via the N-terminal region of Ribonuclease E Proc. Natl. Acad. Sci. U. S. A. 98 2001 63 68
26. V. Khemici, L. Poljak, B.F. Luisi, and A.J. Carpousis The RNase E of Escherichia coli is a membrane-binding protein Mol. Microbiol. 70 2008 799 813
27. Y.-C. Tsai, D. Du, L. Domínguez-Malfavón, D. Dimastrogiovanni, J. Cross, A.J. Callaghan, J. García-Mena, and B.F. Luisi Recognition of the 70S ribosome and polysome by the RNA degradosome in Escherichia coli Nucleic Acids Res. 2012 1 15 10.1093/nar/gks739
28. M.J. Marcaida, M.A. DePristo, V. Chandran, A.J. Carpousis, and B.F. Luisi The RNA degradosome: life in the fast lane of adaptive molecular evolution Trends Biochem. Sci. 31 2006 359 365
29. J. Sambrook, and D.W. Russell Molecular Cloning: a Laboratory Manual third ed. 2001 Cold Spring Harbor Laboratory Press
30. L.D. Islas, and W.N. Zagotta Short-range molecular rearrangements in ion channels detected by tryptophan quenching of bimane fluorescence J. Gen. Physiol. 128 2006 337 346
31. S. Nurmohamed, B. Vaidialingam, A.J. Callaghan, and B.F. Luisi 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. 389 2009 17 33
32. F.J. Trueba, and C.L. Woldringh Changes in cell diameter during the division cycle of Escherichia coli J. Bacteriol. 142 1980 869 878
33. M. Kido, K. Yamanaka, T. Mitani, H. Niki, T. Ogura, and S. Hiraga RNase E polypeptides lacking a carboxyl-terminal half suppress a mukB mutation in Escherichia coli J. Bacteriol. 178 1996 3917 3925
34. A. Vendeville, D. Larivière, and E. Fourmentin An inventory of the bacterial macromolecular components and their spatial organization FEMS Microbiol. 35 2010 395 414
35. A. Taghbalout, and Q. Yang Self-assembly of the bacterial cytoskeleton-associated RNA helicase B protein into polymeric filamentous structures J. Bacteriol. 192 2010 3222 3226
36. A. Burger, C. Whiteley, and A. Boshoff Current perspectives of the Escherichia coli RNA degradosome Biotechnol. Lett. 33 2011 2337 2350
37. C. Jain, and J.G. Belasco Autoregulation of RNase E synthesis in Escherichia coli Nucleic Acids Symp. Ser. 33 1995 85 88
38. A.-C. Jarrige, N. Mathy, and C. Portier PNPase autocontrols its expression by degrading a double-stranded structure in the pnp mRNA leader EMBO J. 20 2001 6845 6855
39. A. Taghbalout, and L. Rothfield RNase E and the other constituents of the RNA degradosome are components of the bacterial cytoskeleton Proc. Natl. Acad. Sci. U. S. A. 104 2007 1667 1672
40. A. Taghbalout, and L. Rothfield RNase E and RNA helicase B play central roles in the cytoskeletal organization of the RNA degradosome J. Biol. Chem. 283 2008 13850 13855
41. J.R. Lakowicz Principles of Fluorescence Spectroscopy 2006 Springer New York