Studies of the RNA degradosome-organizing domain of the Escherichia coli ribonuclease RNase E

Journal of Molecular Biology

Volumn 340, Issue 5, 2004, Pages 965-979

  Callaghan, Anastasia J ^a   Aurikko, Jukka P ^a   Ilag, Leopold L ^a   Gunter Grossmann J ^b   Chandran, Vidya ^a   Kühnel, Karin ^a   Poljak, Leonora ^c   Carpousis, Agamennon J ^c   Robinson, Carol V ^a   Symmons, Martyn F ^a   Luisi, Ben F ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b DARESBURY LABORATORY   (United Kingdom)

^c CNRS   (France)

Author keywords

CD, circular dichroism; CTD, carboxy terminal domain; intrinsically unstructured proteins; NTD, amino terminal domain; protein protein interactions; ribonuclease E; RNA degradosome; RNA processing

Indexed keywords

BACTERIAL RNA; RIBONUCLEASE; RIBONUCLEASE E; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; ESCHERICHIA COLI; PREDICTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; RNA DEGRADATION;

ESCHERICHIA COLI;

EID: 3242802943     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.05.046     Document Type: Article

References (58)

1. Ehretsmann C.P., Carpousis A.J., Krisch H.M. Specificity of Escherichia coli endoribonuclease RNase E: in vivo and in vitro analysis of mutants in a bacteriophage T4 mRNA processing site. Genes Dev. 6:1992;149-159
2. Ono M., Kuwano M. A conditional lethal mutation in an Escherichia coli strain with a longer chemical half life of mRNA. J. Mol. Biol. 129:1979;343-357
3. Jain C., Deana A., Balasco J.G. Consequence of RNase E scarcity in Escherichia coli. Mol. Microbiol. 43:2002;1053-1064
4. Huang H., Liao J., Cohen S.N. Poly(A)- and poly(U)-specific RNA 3′ tail shortening by E. coli ribonuclease E. Nature. 391:1998;99-102
5. Kushner S.R. mRNA decay in Escherichia coli comes of age. J. Bacteriol. 184:2002;4658-4665
6. Ow M.C., Kushner S.R. Initiation of tRNA maturation by RNase E is essential for cell viability in E. coli. Genes Dev. 16:2002;1102-1115
7. Steege D.A. Emerging features of mRNA decay in bacteria. RNA. 6:2000;1079-1090
8. Lee K., Bernstein J.A., Cohen S.N. RNase G complementation of rne null mutation identifies functional interrelationships with RNase E in Escherichia coli. Mol. Microbiol. 43:2002;1445-1456
9. Jain C., Belasco J.G. RNase E autoregulates its synthesis by controlling the degradation of its own mRNA in Escherichia coli: unusual sensitivity of the rne transcript to RNase E activity. Genes Dev. 9:1995;84-96
10. Diwa A.A., Belasco J.G. Critical features of a conserved RNA stem-loop important for feedback regulation of RNase E synthesis. J. Biol. Chem. 277:2002;20415-20422
11. Massé E., Escorcia F.E., Gottesman S. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev. 17:2003;2374-2383
12. Claverie-Martin F., Diaz-Torres M.R., Yancey S.D., Kushner S.R. Analysis of the altered mRNA stability (ams) gene from Escherichia coli. Nucleotide sequence, transcriptional analysis, and homology of its product to MRP3, a mitochondrial ribosomal protein from Neurospora crassa. J. Biol. Chem. 266:1991;2843-2851
13. Casaregola S., Jacq A., Laoudj D., McGurk G., Margarson S., Tempete M., et al. Cloning and analysis of the entire Escherichia coli ams gene. Ams is identical to hmp1 and encodes a 114 kDa protein that migrates as a 180 kDa protein. J. Mol. Biol. 228:1992;30-40
14. Lopez P.J., Marchand I., Joyce S.A., Dreyfus M. The C-terminal half of RNase E, which organises the Escherichia coli degradosome, participates in mRNA degradation but not rRNA processing in vivo. Mol. Microbiol. 33:1999;188-199
15. Cohen S.N., McDowall K.J. RNase E: still a wonderfully mysterious enzyme. Mol. Microbiol. 23:1997;1099-1106
16. Wachi M., Umitsuki G., Shimitzu M., Takada A., Nagai K. Escherichia coli cafA gene encodes a novel RNase, designated as RNase G, involved in processing of the 5′ end of 16 S rRNA. Biochem. Biophys. Res. Commun. 259:1999;483-488
17. 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. USA. 95:1998;11637-11642
18. McDowall K.J., Cohen S.N. The N-terminal domain of the rne gene product has RNase E activity and is non-overlapping with the arginine-rich RNA-binding site. J. Mol. Biol. 255:1996;349-355
19. Vanzo N.F., Li Y.S., Py B., Blum E., Higgins C.F., Raynal L.C., et al. Ribonuclease E organises the protein interactions in the Escherichia coli RNA degradosome. Genes Dev. 12:1998;2770-2781
20. Diwa A.A., Jiang X., Schapira M., Belasco J.G. Two distinct regions on the surface of an RNA-binding domain are crucial for RNase E function. Mol. Microbiol. 46:2002;959-969
21. Carpousis A.J., Van Houwe G., Ehretsmann C., Krisch H.M. 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
22. Py B., Higgins C.F., Krisch H.M., Carpousis A.J. A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature. 381:1996;169-172
23. Miczak A., Kaberdin V.R., Wei C.L., Lin-Chao S. Proteins associated with the RNase E in a multicomponent ribonucleolytic complex. Proc. Natl Acad. Sci. USA. 93:1996;3865-3869
24. Py B., Causton H., Mudd E.A., Higgins C.F. A protein complex mediating mRNA degradation in Escherichia coli. Mol. Microbiol. 14:1994;717-729
25. Blum E., Py B., Carpousis A.J., Higgins C.F. Polyphosphate kinase is a component of the Escherichia coli RNA degradosome. Mol. Microbiol. 387:1997;398
26. Wootton J.C. Non-globular domains in protein sequences: automated segmentation using complexity measures. Comput. Chem. 18:1994;269-285
27. Callaghan A.J., Grossmann J.G., Redko Y.U., Ilag L.L., Moncrieffe M.C., Symmons M.F., et al. Quarternary structure and catalytic activity of the Escherichia coli ribonuclease E amino-terminal catalytic domain. Biochemistry. 42:2003;13848-13855
28. Glatter O., Kratzy O. Small Angle X-ray Scattering. 1980;Academic Press, London, UK
29. Longhi S., Receveur-Brechot V., Karlin D., Johansson K., Darbon H., Yeo R. The C-terminal domain of measles virus nucleoprotein is intrinsically disordered and folds upon binding to the C-terminal moiety of the phosphoprotein. J. Biol. Chem. 278:2003;18628-18648
30. Cantor C.R., Schimmel P.R. Biophysical Chemistry Part III. 1980;WH Freeman and Company, New York
31. Perez J., Vachette P., Russo D., Desmadril M., Durand D. Heat-induced unfolding of neocarzinostatin, a small all-beta protein investigated by small-angle X-ray scattering. J. Mol. Biol. 308:2001;721-743
32. Linding R., Russell R.B., Neduva V., Gibson T.J. GlobPlot: exploring protein sequences for globularity and disorder. Nucl. Acids Res. 31:2003;3701-3708
33. Garner E., Guilliot S., Dunker A.K., Romero P., Obradovic Z. Predicting long disordered regions in protein from amino acid sequence. Biophys. J. 74:1998;A1-A452
34. Li X., Romero P., Rani M., Dunker A.K., Obradovic Z. Predicting protein disorder for N-, C- and internal regions. Genome Inform. 10:1999;30-40
35. Li X., Obradovic Z., Brown C.J., Garner E.C., Dunker A.K. Comparing predictors of disordered protein. Genome Inform. 11:2000;172-184
36. Dunker A.K., Lawson J.D., Brown C.J., Williams R.M., Romero P., Oh J.S. Intrinsically disordered protein. J. Mol. Graph. Model. 19:2001;26-59
37. Romero P., Obradovic Z., Li X., Garner E., Brown C., Dunker A.K. Sequence complexity of disordered protein. Proteins: Struct. Funct. Genet. 42:2001;38-48
38. Lupas A., Van Dyke M., Stock J. Predicting coiled coils from protein sequences. Science. 252:1991;1162-1164
39. Taraseviciene L., Bjork G.R., Bernt E.U. Evidence for an RNA binding region in Escherichia coli processing endoribonuclease RNase E. J. Biol. Chem. 270:1995;26391-26398
40. Hanson C.L., Robinson C.V. Protein-nucleic acid interactions - the expanding role of mass spectrometry (MS). J. Biol. Chem. 279:2004;24907-24910
41. Spring T.G., Wold F. Enolase from Escherichia coli. Methods Enzymol. 42:1975;323-329
42. Kühnel K., Luisi B.F. Crystal structure of the Escherichia coli RNA degradosome component enolase. J. Mol. Biol. 313:2001;583-592
43. Symmons M.F., Jones G.H., Luisi B.F. A duplicate fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity, and regulation. Struct. Fold Des. 8:2000;1215-1226
44. 70 and Rsd protein. Structure. 12:2004;269-275
45. Kaberdin V.R., Walsh A.P., Jakobsen T., McDowall K.J., von Gabain A. Enhanced cleavage of RNA mediated by an interaction between substrate and arginine rich domain of E. coli ribonuclease E. J. Mol. Biol. 301:2000;257-264
46. Leroy A., Vanzo N.F., Sousa S., Dreyfus M., Carpoussis A.J. Function in Escherichia coli of the non-catalytic part of RNase E: role in the degradation of ribosome-free mRNA. Mol. Microbiol. 45:2002;1231-1243
47. Ser. Science. 263:1994;1404-1410
48. Liou G.-G., Chang H.-Y., Lin C.-S., Lin-Chao S. DEAD box Rh1B RNA helicase physically associates with exoribonuclease PNPase to degrade double-stranded RNA independent of the degradosome assembly. J. Biol. Chem. 277:2002;41157-41162
49. Carpousis A.J. The Escherichia coli RNA degradosome: structure, function and relationship to other ribonucleotic multienzyme complexes. Biochem. Soc. Trans. 30:2002;150-155
50. Jäger S., Fuhrmann O., Heck C., Hebermehl M., Schiltz E., Rauhut R., Klug G. An mRNA degrading complex in Rhodobacter capsulatus. Nucl. Acids Res. 29:2001;4581-4588
51. 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. 48:2003;349-360
52. Rauhut R., Klug G. mRNA degradation in bacteria. FEMS Microbiol. Rev. 23:1999;353-370
53. Kido M., Yamanaka K., Mitani T., Niki H., Ogura T., Hiraga S. RNase E polypeptides lacking a carboxy-terminal half suppress a mukB mutation in Escherichia coli. J. Bacteriol. 178:1996;1925-3917
54. Bernstein J.A., Lin P., Cohen S.N., Lin-Chao S. Global analysis of Escherichia coli RNA degradosome function using DNA microarrays. Proc. Natl Acad. Sci. USA. 101:2004;2758-2763
55. Aurikko, J.P., (2003) Structural studies of the C-terminal domain of RNase E: a scaffold for the Escherichia coli degradosome. M.Phil. thesis, University of Cambridge.
56. Semenyuk A.V., Svergun D.I. GNOM - a program package for small-angle scattering data processing. J. Appl. Crystallog. 22:1991;537-540
57. Sobott F., Hernandez H., McCammon M.G., Tito M.A., Robinson C.V. A tandem mass spectrometer for improved transmission and analysis of large macromolecular assemblies. Anal. Chem. 74:2002;1402-1407
58. Goodstadt L., Ponting C.P. CHROMA: consensus-based colouring of multiple alignments for publication. Bioinform. Appl. Note. 17:2001;845-846