The Escherichia coli RNA processing and degradation machinery is compartmentalized within an organized cellular network

Biochemical Journal

Volumn 458, Issue 1, 2014, Pages 11-22

  Taghbalout, Aziz ^a   Yang, Qingfen ^a   Arluison, Véronique ^b  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Cellular compartmentalization; Cellular organization; Macromolecular assembly; Membrane association; RNA degradosome; RNA processing and degradation

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL RNA; CHAPERONE; CYTOPLASM PROTEIN; CYTOSKELETON PROTEIN; ELONGATION FACTOR EF; ELONGATION FACTOR HA; ELONGATION FACTOR TU; FLAG PROTEIN; HFQ PROTEIN; MESSENGER RNA; ORN PROTEIN; PAP I PROTEIN; RIBONUCLEASE; RIBONUCLEASE E; RIBONUCLEASE II; RIBONUCLEASE III; RPPH PROTEIN; RRAA PROTEIN; RRAB PROTEIN; UNCLASSIFIED DRUG; YFP PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL STRUCTURE; CELLULAR DISTRIBUTION; CHROMOSOME; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ESCHERICHIA COLI; IMMUNOHISTOCHEMISTRY; MESSENGER RNA SYNTHESIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RNA DEGRADATION; RNA PROCESSING; RNA SYNTHESIS;

BLOTTING, WESTERN; CELL COMPARTMENTATION; ESCHERICHIA COLI; PROTEOLYSIS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, BACTERIAL;

EID: 84892918629     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20131287     Document Type: Article

References (63)

1. Carpousis, A. J. (2007) The RNA degradosome of Escherichia coli: An mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol. 61, 71-87
2. Worrall, J. A. and Luisi, B. F. (2007) Information available at cut rates: Structure and mechanism of ribonucleases. Curr. Opin. Struct. Biol. 17, 128-137
3. Vogel, J. and Luisi, B. F. (2011) Hfq and its constellation of RNA. Nature Rev. 9, 578-589
4. Arraiano, C. M., Andrade, J. M., Domingues, S., Guinote, I. B., Malecki, M., Matos, R. G., Moreira, R. N., Pobre, V., Reis, F. P., Saramago, M. et al. (2010) The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol. Rev. 34, 883-923
5. Taghbalout, A. and Rothfield, L. (2008) RNaseE and RNA helicase B play central roles in the cytoskeletal organization of the RNA degradosome. J. Biol. Chem. 283, 13850-13855
6. Taghbalout, A. and Rothfield, L. (2007) RNaseE and the other constituents of the RNA degradosome are components of the bacterial cytoskeleton. Proc. Natl. Acad. Sci. U.S.A. 104, 1667-1672
7. Lu, F. and Taghbalout, A. (2013) Membrane association via an amino-terminal amphipathic helix is required for the cellular organization and function of RNase II. J. Biol. Chem. 288, 7241-7251
8. Maniatis, T., Fritsch, E. F. and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor
9. Shih, Y. L., Fu, X., King, G. F., Le, T. and Rothfield, L. (2002) Division site placement in E. coli: Mutations that prevent formation of the MinE ring lead to loss of the normal midcell arrest of growth of polar MinD membrane domains. EMBO J. 21, 3347-3357
10. Datsenko, K. A. and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97, 6640-6645
11. Uzzau, S., Figueroa-Bossi, N., Rubino, S. and Bossi, L. (2001) Epitope tagging of chromosomal genes in Salmonella . Proc. Natl. Acad. Sci. U.S.A. 98, 15264-15269
12. Cherepanov, P. P. and Wackernagel, W. (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158, 9-14
13. Miller, J. H. (1992) A Short Course on Bacterial Genetics, Cold Spring Harbor Laboratory Press, Cold Spring Harbor
14. Justice, S. S., Garcia-Lara, J. and Rothfield, L. I. (2000) Cell division inhibitors SulA and MinC/MinD block septum formation at different steps in the assembly of the Escherichia coli division machinery. Mol. Microbiol. 37, 410-423
15. Rowland, S. L., Fu, X., Sayed, M. A., Zhang, Y., Cook, W. R. and Rothfield, L. I. (2000) Membrane redistribution of the Escherichia coli MinD protein induced by MinE. J. Bacteriol. 182, 613-619
16. Soper, T., Mandin, P., Majdalani, N., Gottesman, S. and Woodson, S. A. (2010) Positive regulation by small RNAs and the role of Hfq. Proc. Natl. Acad. Sci. U.S.A. 107, 9602-9607
17. Hwang, W., Arluison, V. and Hohng, S. (2011) Dynamic competition of DsrA and rpoS fragments for the proximal binding site of Hfq as a means for efficient annealing. Nucleic Acids Res. 39, 5131-5139
18. Raynal, L. C., Krisch, H. M. and Carpousis, A. J. (1996) Bacterial poly(A) polymerase: An enzyme that modulates RNA stability. Biochimie 78, 390-398
19. Richet, E., Davidson, A. L. and Joly, N. (2012) The ABC transporter MalFGK2 sequesters the MalT transcription factor at the membrane in the absence of cognate substrate. Mol. Microbiol. 85, 632-647
20. Pichoff, S. and Lutkenhaus, J. (2005) Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol. Microbiol. 55, 1722-1734
21. Taghbalout, A., Ma, L. and Rothfield, L. (2006) Role of MinD-membrane association in Min protein interactions. J. Bacteriol. 188, 2993-3001
22. Defeu Soufo, H. J., Reimold, C., Linne, U., Knust, T., Gescher, J. and Graumann, P. L. (2010) Bacterial translation elongation factor EF-Tu interacts and colocalizes with actin-like MreB protein. Proc. Natl. Acad. Sci. U.S.A. 107, 3163-3168
23. Landgraf, D., Okumus, B., Chien, P., Baker, T. A. and Paulsson, J. (2012) Segregation of molecules at cell division reveals native protein localization. Nat. Methods 9, 480-482
24. Sun, Q. and Margolin, W. (1998) FtsZ dynamics during the division cycle of live Escherichia coli cells. J. Bacteriol. 180, 2050-2056
25. Shih, Y. L., Le, T. and Rothfield, L. (2003) Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles. Proc. Natl. Acad. Sci. U.S.A. 100, 7865-7870
26. Hu, Z. and Lutkenhaus, J. (2003) A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol. Microbiol. 47, 345-355
27. Szeto, T. H., Rowland, S. L., Rothfield, L. I. and King, G. F. (2002) Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts. Proc. Natl. Acad. Sci. U.S.A. 99, 15693-15698
28. 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
29. Mohanty, B. K., Maples, V. F. and Kushner, S. R. (2004) The Sm-like protein Hfq regulates polyadenylation dependent mRNA decay in Escherichia coli. Mol. Microbiol. 54, 905-920
30. 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
31. 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. U.S.A. 101, 2758-2763
32. Nierlich, D. P. and Murakawa, G. J. (1996) The decay of bacterial messenger RNA. Prog. Nucleic Acid Res. Mol. Biol. 52, 153-216
33. Montero Llopis, P., Jackson, A. F., Sliusarenko, O., Surovtsev, I., Heinritz, J., Emonet, T. and Jacobs-Wagner, C. (2010) Spatial organization of the flow of genetic information in bacteria. Nature 466, 77-81
34. Berlatzky, I. A., Rouvinski, A. and Ben-Yehuda, S. (2008) Spatial organization of a replicating bacterial chromosome. Proc. Natl. Acad. Sci. U.S.A. 105, 14136-14140
35. Cook, W. R. and Rothfield, L. I. (1999) Nucleoid-independent identification of cell division sites in Escherichia coli. J. Bacteriol. 181, 1900-1905
36. Hardwick, S. W., Chan, V. S., Broadhurst, R. W. and Luisi, B. F. (2011) An RNA degradosome assembly in Caulobacter crescentus. Nucleic Acids Res. 39, 1449-1459
37. Shih, Y. L., Kawagishi, I. and Rothfield, L. (2005) The MreB and Min cytoskeletal-like systems play independent roles in prokaryotic polar differentiation. Mol. Microbiol. 58, 917-928
38. Garner, E. C., Bernard, R., Wang, W., Zhuang, X., Rudner, D. Z. and Mitchison, T. (2011) Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333, 222-225
39. White, C. L., Kitich, A. and Gober, J. W. (2010) Positioning cell wall synthetic complexes by the bacterial morphogenetic proteins MreB and MreD. Mol. Microbiol. 76, 616-633
40. Dye, N. A., Pincus, Z., Theriot, J. A., Shapiro, L. and Gitai, Z. (2005) Two independent spiral structures control cell shape in Caulobacter . Proc. Natl. Acad. Sci. U.S.A. 102, 18608-18613
41. Divakaruni, A. V., Loo, R. R., Xie, Y., Loo, J. A. and Gober, J. W. (2005) The cell-shape protein MreC interacts with extracytoplasmic proteins including cell wall assembly complexes in Caulobacter crescentus. Proc. Natl. Acad. Sci. U.S.A. 102, 18602-18607
42. Dominguez-Escobar, J., Chastanet, A., Crevenna, A. H., Fromion, V., Wedlich-Soldner, R. and Carballido-Lopez, R. (2011) Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333, 225-228
43. van Teeffelen, S., Wang, S., Furchtgott, L., Huang, K. C., Wingreen, N. S., Shaevitz, J. W. and Gitai, Z. (2011) The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. Proc. Natl. Acad. Sci. U.S.A. 108, 15822-15827
44. Vats, P., Shih, Y. and Rothfield, L. (2009) Assembly of the MreB-associated cytoskeletal ring of Escherichia coli. Mol. Microbiol. 72, 170-182
45. Raynal, L. C. and Carpousis, A. J. (1999) Poly(A) polymerase I of Escherichia coli: Characterization of the catalytic domain, an RNA binding site and regions for the interaction with proteins involved in mRNA degradation. Mol. Microbiol. 32, 765-775
46. Gorna, M. W., Pietras, Z., Tsai, Y. C., Callaghan, A. J., Hernandez, 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
47. Lee, K., Zhan, X., Gao, J., Qiu, J., Feng, Y., Meganathan, R., Cohen, S. N. and Georgiou, G. (2003) RraA. a protein inhibitor of RNase E activity that globally modulates RNA abundance in E. coli. Cell 114, 623-634
48. Gao, J., Lee, K., Zhao, M., Qiu, J., Zhan, X., Saxena, A., Moore, C. J., Cohen, S. N. and Georgiou, G. (2006) Differential modulation of E. coli mRNA abundance by inhibitory proteins that alter the composition of the degradosome. Mol. Microbiol. 61, 394-406
49. Lopez, D. and Kolter, R. (2010) Functional microdomains in bacterial membranes. Genes Dev. 24, 1893-1902
50. Matsumoto, K., Kusaka, J., Nishibori, A. and Hara, H. (2006) Lipid domains in bacterial membranes. Mol. Microbiol. 61, 1110-1117
51. Figge, R. M., Divakaruni, A. V. and Gober, J. W. (2004) MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol. Microbiol. 51, 1321-1332
52. Jones, L. J., Carballido-Lopez, R. and Errington, J. (2001) Control of cell shape in bacteria: Helical, actin-like filaments in Bacillus subtilis. Cell 104, 913-922
53. Swulius, M. T. and Jensen, G. J. (2012) The helical MreB cytoskeleton in Escherichia coli MC1000/pLE7 is an artifact of the N-terminal yellow fluorescent protein tag. J. Bacteriol. 194, 6382-6386
54. Diestra, E., Cayrol, B., Arluison, V. and Risco, C. (2009) Cellular electron microscopy imaging reveals the localization of the Hfq protein close to the bacterial membrane. PLoS ONE 4, e8301
55. Azam, T. A., Hiraga, S. and Ishihama, A. (2000) Two types of localization of the DNA-binding proteins within the Escherichia coli nucleoid. Genes Cells 5, 613-626
56. Jasiecki, J. and Wegrzyn, G. (2005) Localization of Escherichia coli poly(A) polymerase I in cellular membrane. Biochem. Biophys. Res. Commun. 329, 598-602
57. Carabetta, V. J., Mohanty, B. K., Kushner, S. R. and Silhavy, T. J. (2009) The response regulator SprE (RssB) modulates polyadenylation and mRNA stability in Escherichia coli. J. Bacteriol. 191, 6812-6821
58. Miczak, A., Srivastava, R. A. and Apirion, D. (1991) Location of the RNA-processing enzymes RNase III, RNase E and RNase P in the Escherichia coli cell. Mol. Microbiol. 5, 1801-1810
59. Russell, J. H. and Keiler, K. C. (2009) Subcellular localization of a bacterial regulatory RNA. Proc. Natl. Acad. Sci. U.S.A. 106, 16405-16409
60. Gorna, M. W., Carpousis, A. J. and Luisi, B. F. (2012) From conformational chaos to robust regulation: The structure and function of the multi-enzyme RNA degradosome. Q. Rev. Biophys. 45, 105-145
61. de Boer, P. A., Crossley, R. E. and Rothfield, L. I. (1988) Isolation and properties of minB, a complex genetic locus involved in correct placement of the division site in Escherichiacoli. J. Bacteriol. 170, 2106-2112
62. Wachi, M., Doi, M., Tamaki, S., Park, W., Nakajima-Iijima, S. and Matsuhashi, M. (1987) Mutant isolation and molecular cloning of mre genes, which determine cell shape, sensitivity to mecillinam, and amount of penicillin-binding proteins in Escherichia coli. J. Bacteriol. 169, 4935-4940
63. Vanzo, N. F., Li, Y. S., Py, B., Blum, E., Higgins, C. F., Raynal, L. C., Krisch, H. M. and Carpousis, A. J. (1998) Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev. 12, 2770-2781