RNase Y in Bacillus subtilis: A natively disordered protein that is the functional equivalent of RNase E from Escherichia coli

Journal of Bacteriology

Volumn 193, Issue 19, 2011, Pages 5431-5441

  Lehnik Habrink, Martin ^a   Newman, Joseph ^b   Rothe, Fabian M ^a   Solovyova, Alexandra S ^b   Rodrigues, Cecilia ^b   Herzberg, Christina ^a   Commichau, Fabian M ^a   Lewis, Richard J ^b   Stülke, Jörg ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ENOLASE; EXORIBONUCLEASE; MESSENGER RNA; RIBONUCLEASE; RIBONUCLEASE E; RNA HELICASE; RNA HELICASE CSHA; RNASE Y; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BIOINFORMATICS; CONTROLLED STUDY; ENZYME LOCALIZATION; ESCHERICHIA COLI; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; RNA DEGRADATION; RNA PROCESSING; RNA STABILITY;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; ENDORIBONUCLEASES; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA HELICASES; SEQUENCE HOMOLOGY, AMINO ACID; TWO-HYBRID SYSTEM TECHNIQUES;

BACILLUS SUBTILIS; ESCHERICHIA COLI;

EID: 80053594659     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.05500-11     Document Type: Article

References (63)

1. Arraiano, C. M., et al. 2010. The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol. Rev. 34: 883-923.
2. Bernstein, J. A., P. H. Lin, S. N. Cohen, and S. Lin-Chao. 2004. Global analysis of Escherichia coli RNA degradosome function using DNA microarrays. Proc. Natl. Acad. Sci. U. S. A. 101:2758-2763.
3. Burkhard, P., J. Stetefeld, and S. V. Strelkov. 2001. Coiled coils: a highly versatile protein folding motif. Trends Cell Biol. 11:82-88.
4. Callaghan, A. J., et al. 2003. Quaternary structure and catalytic activity of the Escherichia coli RNase E amino-terminal catalytic domain. Biochemistry 42:13848-13855.
5. Callaghan, A. J., et al. 2005. Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature 437:1187-1191.
6. Carpousis, A. J. 2007. The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol. 61:71-87.
7. Carpousis, A. J., B. F. Luisi, and K. J. McDowall. 2009. Endonucleolytic initiation of mRNA decay in Escherichia coli. Prog. Mol. Biol. Transl. Sci. 85:91-135.
8. Celesnik, H., A. Deana, and J. G. Belasco. 2007. Initiation of RNA decay in Escherichia coli by 5' pyrophosphate removal. Mol. Cell 27:79-90.
9. Claessen, D., et al. 2008. Control of the cell elongation-division cycle by shuttling of PBP1 protein in Bacillus subtilis. Mol. Microbiol. 68:1029-1046.
10. Commichau, F. M., et al. 2009. Novel activities of glycolytic enzymes in Bacillus subtilis: interactions with essential proteins involved in mRNA processing. Mol. Cell. Proteomics 8:1350-1360.
11. Condon, C. 2003. RNA processing and degradation in Bacillus subtilis. Microbiol. Mol. Biol. Rev. 67:157-174.
12. Dunker, A. K., et al. 2001. Intrinsically disordered protein. J. Mol. Graph. Model. 19:26-59.
13. Dyson, H. J., and P. E. Wright. 2005. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6:197-208.
14. Evguenieva-Hackenberg, E., V. Roppelt, C. Lassek, and G. Klug. 2011. Subcellular localization of RNA degrading proteins and protein complexes in prokaryotes. RNA Biol. 8:49-54.
15. Fieulaine, S., et al. 2002. X-ray structure of a bifunctional protein kinase in complex with its protein substrate HPr. Proc. Natl. Acad. Sci. U. S. A. 99:13437-13441.
16. Fong, J. H., B. A. Shoemaker, S. O. Garbuzynskiy, M. Y. Lobanov, and A. R. Pancheko. 2009. Intrinsic disorder in protein interactions: insights from a comprehensive structural analysis. PLoS Comput. Biol. 5:e1000316.
17. Grigoryan, G., and A. E. Keating. 2008. Structural specificity in coiled-coil interactions. Curr. Opin. Struct. Biol. 18:477-483.
18. Gunka, K. 2011. Der Einfluss der Glutamatdehydrogenasen auf die Verknüpfung des Kohlenstoff- und Stickstoffstoffwechsels in Bacillus subtilis. Ph.D. thesis. University of Göttingen, Göttingen, Germany.
19. Hahne, H., S. Wolff, M. Hecker, and D. Becher. 2008. From complementarity to comprehensiveness-targeting the membrane proteome of growing Bacillus subtilis by divergent approaches. Proteomics 8:4123-4136.
20. Hardwick, S. W., V. S. Y. Chan, R. W. Broadhurst, and B. Luisi. 2010. An RNA degradosome assembly in Caulobacter crescentus. Nucleic Acids Res. 39:1449-1459.
21. Herzberg, C., et al. 2007. SPINE: a method for the rapid detection and analysis of protein-protein interactions in vivo. Proteomics 7:4032-4035.
22. Homuth, G., A. Mogk, and W. Schumann. 1999. Post-transcriptional regulation of the Bacillus subtilis dnaK operon. Mol. Microbiol. 32:1183-1197.
23. Hunt, A., J. P. Rawlins, H. B. Thomaides, and J. Errington. 2006. Functional analysis of 11 putative essential genes in Bacillus subtilis. Microbiology 152: 2895-2907.
24. Ishida, T., and K. Kinoshita. 2008. Prediction of disordered regions in proteins based on the meta approach. Bioinformatics 24:1344-1348.
25. Kaberdin, V. R., et al. 1998. The endonucleolytic 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. 95:11637-11642.
26. Kaberdin, V. R., D. Singh, and S. Lin-Chao. 2011. Composition and conservation of the mRNA-degrading machinery in bacteria. J. Biomed. Sci. 18:23.
27. Kang, S. O., M. G. Caparon, and K. H. Cho. 2010. Virulence gene regulation by CvfA, a putative RNase: the CvfA-enolase complex in Streptococcus pyogenes links nutritional stress, growth-phase control, and virulence gene expression. Infect. Immun. 78:2754-2767.
28. Karimova, G., J. Pidoux, A. Ullmann, and D. Ladant. 1998. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. U. S. A. 95:5752-5756.
29. Khemici, V., L. Poljak, B. F. Luisi, and A. J. Carpousis. 2008. The RNase E of Escherichia coli is a membrane binding protein. Mol. Microbiol. 70:799-813.
30. Kunst, F., and G. Rapoport. 1995. Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis. J. Bacteriol. 177: 2403-2407.
31. Kushner, S. R. 2002. mRNA decay in Escherichia coli comes of age. J. Bacteriol. 184:4658-4665.
32. Laue, T., B. Shah, T. Ridgeway, and S. Pelletier. 1992. Computer-aided interpretation of analytical sedimentation data for proteins. In S. Harding, A. Rowe, and J. Horton (ed.). Royal Society of Chemistry, Cambridge, United Kingdom.
33. Lehnik-Habrink, M., et al. 2010. The RNA degradosome in Bacillus subtilis: identification of CshA as the major RNA helicase in the multi-protein complex. Mol. Microbiol. 77:958-971.
34. Lehnik-Habrink, M., et al. RNA processing in Bacillus subtilis: identification of targets of the essential RNase Y. Mol. Microbiol., in press. doi:10.1111/ j.1365-2011.07777.x.
35. Levin, P. A., I. G. Kurtser, and A. D. Grossman. 1999. Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 96:9642-9647.
36. Lewis, P. J., S. D. Thaker, and J. Errington. 2000. Compartmentalization of transcription and translation in Bacillus subtilis. EMBO J. 19:710-718.
37. Liou, G. G., W. N. Jane, S. N. Cohen, N. S. Lin, and S. Lin-Chao. 2001. RNA degradosomes exist in vivo in Escherichia coli as multicomponent complexes associated with the cytoplasmic membrane via the N-terminal region of RNase E. Proc. Natl. Acad. Sci. U. S. A. 98:63-68.
38. Ludwig, H., et al. 2001. Transcription of glycolytic genes and operons in Bacillus subtilis: evidence for the presence of multiple levels of control of the gapA operon. Mol. Microbiol. 41:409-422.
39. Lupas, A., M. van Dyke, and J. Stock. 1991. Predicting coiled coils from protein sequences. Science 252:1162-1164.
40. Mackie, G. A. 1998. RNase E is a 5″-end-dependent endonuclease. Nature 395:720-723.
41. Mäder, U., L. Zig, J. Kretschmer, G. Homuth, and H. Putzer. 2008. mRNA processing by RNases J1 and J2 affects Bacillus subtilis gene expression on a global scale. Mol. Microbiol. 70:183-196.
42. Martin-Verstraete, I., M. Débarbouillé, A. Klier, and G. Rapoport. 1994. Interaction of wild-type truncated LevR of Bacillus subtilis with the upstream activating sequence of the levanase operon. J. Mol. Biol. 241:178-192.
43. Meinken, C., H. M. Blencke, H. Ludwig, and J. Stülke. 2003. Expression of the glycolytic gapA operon in Bacillus subtilis: differential syntheses of proteins encoded by the operon. Microbiology 149:751-761.
44. Meyer, F. M., et al. 2011. Physical interactions between tricarboxylic acid cycle enzymes in Bacillus subtilis: evidence for a metabolon. Metab. Eng. 13:18-27.
45. Miczak, A., R. A. Srivastava, and D. Apirion. 1991. Location of the RNAprocessing enzymes RNase III, RNase E and RNase P in the Escherichia coli cell. Mol. Microbiol. 5:1801-1810.
46. Miczak, A., V. R. Kaberdin, C. L. Wei, and S. Lin-Chao. 1996. Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc. Natl. Acad. Sci. U. S. A. 93:3865-3869.
47. Montero Llopis, P., et al. 2010. Spatial organization of the flow of genetic information in bacteria. Nature 466:77-81.
48. Nevo-Dinur, K., A. Nussbaum-Schochat, S. Ben-Yehuda, and O. Amster-Choder. 2011. Translation-independent localization of mRNA in E. coli. Science 331:1081-1084.
49. Nurmohamed, S., et al. 2011. Polynucleotide phosphorylase activity may be modulated by metabolites in Escherichia coli. J. Biol. Chem. 286:14315-14323.
50. Rigden, M. D., et al. 2008. Identification of the coiled-coil domains of Enterococcus faecalis DivIVA that mediate oligomerization and their importance for biological function. J. Biochem. 144:63-76.
51. Roppelt, V., et al. 2010. The archaeal exosome localizes to the membrane. FEBS Lett. 584:2791-2795.
52. Roux, C. M., J. P. DeMuth, and P. M. Dunman. 2011. Characterization of components of the Staphylococcus aureus mRNA degradosome holoenzymelike complex. J. Bacteriol. 193:5520-5526.
53. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
54. Schuck, P. 2000. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78:1606-1619.
55. Shahbabian, K., A. Jamalli, L. Zig, and H. Putzer. 2009. RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J. 28:3523-3533.
56. Shi, Z., W. Z. Yang, S. Lin-Chao, K. F. Chak, and H. S. Yuan. 2008. Crystal structure of Escherichia coli PNPase: central channel residues are involved in processive RNA degradation. RNA 14:2361-2371.
57. Tjalsma, H., et al. 2004. Proteomics of protein secretion by Bacillus subtilis: separating the "secrets" of the secretome. Microbiol. Mol. Biol. Rev. 68: 207-233.
58. Tjalsma, H., and J. M. van Dijl. 2005. Proteomics-based consensus prediction of protein retention in a bacterial membrane. Proteomics 5:4472-4482.
59. Uversky, V. N., J. R. Gillespie, and A. L. Fink. 2000. Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41: 415-427.
60. Wach, A. 1996. PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae. Yeast 12:259-265.
61. Xue, B., R. L. DunBrack, R. W. Williams, A. K. Dunker, and V. N. Uversky. 2010. PONDR-Fit: a meta-predictor of intrinsically disordered amino acids. Biochim. Biophys. Acta 1804:996-1010.
62. Yao, S., and D. H. Bechhofer. 2010. Initiation of decay of Bacillus subtilis rpsO mRNA by endoribonuclease RNase Y. J. Bacteriol. 192:3279-3286.
63. Zweers, J. C., T. Wiegert, and J. M. van Dijl. 2009. Stress-responsive systems set specific limits to the overproduction of membrane proteins in Bacillus subtilis. Appl. Environ. Microbiol. 75:7356-7364.