Membrane Recognition and Dynamics of the RNA Degradosome
Recent discoveries that two ribonucleases with major roles in mRNA degradation, RNase E of Escherichia coli and RNase Y of Bacillus subtilis, are localized to the inner cytoplasmic membrane suggest that spatial separation of transcription and mRNA degradation are general features of the bacterial cell. Here we show that RNase E rapidly diffuses over the entire inner membrane forming short-lived foci. Results of molecular dynamics simulations lead us to suggest that RNase E interacts with the lipid membrane by a novel mechanism permitting a high degree of translational freedom. We show that RNA substrate is necessary for the formation of RNase E foci and that formation of foci correlates with constraints on the diffusion of RNase E. We therefore propose that foci are degradation bodies in which several RNase E molecules engage an RNA substrate. The sequestration of the mRNA degradation machinery to the inner cytoplasmic membrane has important consequences for mRNA turnover. This organization likely favors formation of polyribosomes on nascent transcripts before they are exposed to the degradation machinery. Rapid diffusion of RNase E on the inner cytoplasmic membrane could be part of a scanning mechanism that facilitates recognition of cytoplasmic polyribosomes and cooperative degradation of mRNA.
Vyšlo v časopise:
Membrane Recognition and Dynamics of the RNA Degradosome. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1004961
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004961
Souhrn
Recent discoveries that two ribonucleases with major roles in mRNA degradation, RNase E of Escherichia coli and RNase Y of Bacillus subtilis, are localized to the inner cytoplasmic membrane suggest that spatial separation of transcription and mRNA degradation are general features of the bacterial cell. Here we show that RNase E rapidly diffuses over the entire inner membrane forming short-lived foci. Results of molecular dynamics simulations lead us to suggest that RNase E interacts with the lipid membrane by a novel mechanism permitting a high degree of translational freedom. We show that RNA substrate is necessary for the formation of RNase E foci and that formation of foci correlates with constraints on the diffusion of RNase E. We therefore propose that foci are degradation bodies in which several RNase E molecules engage an RNA substrate. The sequestration of the mRNA degradation machinery to the inner cytoplasmic membrane has important consequences for mRNA turnover. This organization likely favors formation of polyribosomes on nascent transcripts before they are exposed to the degradation machinery. Rapid diffusion of RNase E on the inner cytoplasmic membrane could be part of a scanning mechanism that facilitates recognition of cytoplasmic polyribosomes and cooperative degradation of mRNA.
Zdroje
1. Gorna MW, Carpousis AJ, Luisi BF (2012) From conformational chaos to robust regulation: the structure and function of the multi-enzyme RNA degradosome. Q Rev Biophys 45: 105–145. doi: 10.1017/S003358351100014X 22169164
2. Bandyra KJ, Bouvier M, Carpousis AJ, Luisi BF (2013) The social fabric of the RNA degradosome. Biochim Biophys Acta 1829: 514–522. doi: 10.1016/j.bbagrm.2013.02.011 23459248
3. Waters LS, Storz G (2009) Regulatory RNAs in bacteria. Cell 136: 615–628. doi: 10.1016/j.cell.2009.01.043 19239884
4. Beisel CL, Storz G (2010) Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 34: 866–882. doi: 10.1111/j.1574-6976.2010.00241.x 20662934
5. Carpousis AJ (2007) The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu Rev Microbiol 61: 71–87. doi: 10.1146/annurev.micro.61.080706.093440 17447862
6. Khemici V, Poljak L, Luisi BF, Carpousis AJ (2008) The RNase E of Escherichia coli is a membrane-binding protein. Mol Microbiol 70: 799–813. 18976283
7. Taghbalout A, 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. doi: 10.1073/pnas.0610491104 17242352
8. Papanastasiou M, Orfanoudaki G, Koukaki M, Kountourakis N, Sardis MF, et al. (2013) The Escherichia coli peripheral inner membrane proteome. Mol Cell Proteomics 12: 599–610. doi: 10.1074/mcp.M112.024711 23230279
9. Lopez-Campistrous A, Semchuk P, Burke L, Palmer-Stone T, Brokx SJ, et al. (2005) Localization, annotation, and comparison of the Escherichia coli K-12 proteome under two states of growth. Mol Cell Proteomics 4: 1205–1209. doi: 10.1074/mcp.D500006-MCP200 15911532
10. Mackie GA (2013) RNase E: at the interface of bacterial RNA processing and decay. Nat Rev Microbiol 11: 45–57. doi: 10.1038/nrmicro2930 23241849
11. Shahbabian K, Jamalli A, Zig L, Putzer H (2009) RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J 28: 3523–3533. doi: 10.1038/emboj.2009.283 19779461
12. Taghbalout A, 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. doi: 10.1074/jbc.M709118200 18337249
13. Taghbalout A, Yang Q, Arluison V (2014) The Escherichia coli RNA processing and degradation machinery is compartmentalized within an organized cellular network. Biochem J 458: 11–22. doi: 10.1042/BJ20131287 24266791
14. Worrall JA, Howe FS, McKay AR, Robinson CV, Luisi BF (2008) Allosteric activation of the ATPase activity of the Escherichia coli RhlB RNA helicase. J Biol Chem 283: 5567–5576. doi: 10.1074/jbc.M708620200 18165229
15. Ait-Bara S, Carpousis AJ (2010) Characterization of the RNA degradosome of Pseudoalteromonas haloplanktis: conservation of the RNase E-RhlB interaction in the {gamma}-Proteobacteria. J Bacteriol. doi: 10.1128/JB.00592-10 20729366
16. Soupene E, van Heeswijk WC, Plumbridge J, Stewart V, Bertenthal D, et al. (2003) Physiological studies of Escherichia coli strain MG1655: growth defects and apparent cross-regulation of gene expression. J Bacteriol 185: 5611–5626. doi: 10.1128/JB.185.18.5611-5626.2003 12949114
17. Bouvier M, Carpousis AJ (2011) A tale of two mRNA degradation pathways mediated by RNase E. Mol Microbiol 82: 1305–1310. doi: 10.1111/j.1365-2958.2011.07894.x 22074454
18. Sweetman G, Trinei M, Modha J, Kusel J, Freestone P, et al. (1996) Electrospray ionization mass spectrometric analysis of phospholipids of Escherichia coli. Mol Microbiol 20: 233–238. doi: 10.1111/j.1365-2958.1996.tb02504.x 8861220
19. Oursel D, Loutelier-Bourhis C, Orange N, Chevalier S, Norris V, et al. (2007) Lipid composition of membranes of Escherichia coli by liquid chromatography/tandem mass spectrometry using negative electrospray ionization. Rapid Commun Mass Spectrom 21: 1721–1728. doi: 10.1002/rcm.3013 17477452
20. Strahl H, Hamoen LW (2012) Finding the corners in a cell. Curr Opin Microbiol 15: 731–736. doi: 10.1016/j.mib.2012.10.006 23182676
21. Strahl H, Burmann F, Hamoen LW (2014) The actin homologue MreB organizes the bacterial cell membrane. Nat Commun 5: 3442. doi: 10.1038/ncomms4442 24603761
22. Knight JD, Lerner MG, Marcano-Velazquez JG, Pastor RW, Falke JJ (2010) Single molecule diffusion of membrane-bound proteins: window into lipid contacts and bilayer dynamics. Biophys J 99: 2879–2887. doi: 10.1016/j.bpj.2010.08.046 21044585
23. Garner EC, Bernard R, Wang W, Zhuang X, Rudner DZ, et al. (2011) Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333: 222–225. doi: 10.1126/science.1203285
24. Dominguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Soldner R, et al. (2011) Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333: 225–228. doi: 10.1126/science.1203466 21636744
25. van Teeffelen S, Wang S, Furchtgott L, Huang KC, Wingreen NS, et al. (2011) The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. Proc Natl Acad Sci U S A 108: 15822–15827. doi: 10.1073/pnas.1108999108 21903929
26. Lopez PJ, Iost I, Dreyfus M (1994) The use of a tRNA as a transcriptional reporter: the T7 late promoter is extremely efficient in Escherichia coli but its transcripts are poorly expressed. Nucleic Acids Res 22: 2434. doi: 10.1093/nar/22.7.1186 8036178
27. Iost I, Dreyfus M (1995) The stability of Escherichia coli lacZ mRNA depends upon the simultaneity of its synthesis and translation. EMBO J 14: 3252–3261. 7542588
28. Ow MC, Kushner SR (2002) Initiation of tRNA maturation by RNase E is essential for cell viability in E. coli. Genes Dev 16: 1102–1115. doi: 10.1101/gad.983502
29. Jain C, Belasco JG (1995) RNase E autoregulates its synthesis by controlling the degradation rate of its own mRNA in Escherichia coli: unusual sensitivity of the rne transcript to RNase E activity. Genes Dev 9: 84–96. doi: 10.1101/gad.9.1.84 7530223
30. Leroy A, Vanzo NF, Sousa S, Dreyfus M, Carpousis AJ (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. doi: 10.1046/j.1365-2958.2002.03104.x 12207692
31. Shaner NC, Steinbach PA, Tsien RY (2005) A guide to choosing fluorescent proteins. Nat Methods 2: 905–909. doi: 10.1038/nmeth819 16299475
32. Bakshi S, Siryaporn A, Goulian M, Weisshaar JC (2012) Superresolution imaging of ribosomes and RNA polymerase in live Escherichia coli cells. Mol Microbiol 85: 21–38. doi: 10.1111/j.1365-2958.2012.08081.x 22624875
33. Parry BR, Surovtsev IV, Cabeen MT, O’Hern CS, Dufresne ER, et al. (2014) The bacterial cytoplasm has glass-like properties and is fluidized by metabolic activity. Cell 156: 183–194. doi: 10.1016/j.cell.2013.11.028 24361104
34. Hunter CA, Anderson HL (2009) What is cooperativity? Angew Chem Int Ed Engl 48: 7488–7499. doi: 10.1002/anie.200902490 19746372
35. Carpousis AJ, Leroy A, Vanzo N, Khemici V (2001) Escherichia coli RNA degradosome. Methods Enzymol 342: 333–345. doi: 10.1016/S0076-6879(01)42556-0 11586906
36. Decker CJ, Parker R (2012) P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harb Perspect Biol 4: a012286. doi: 10.1101/cshperspect.a012286 22763747
37. Stoecklin G, Kedersha N (2013) Relationship of GW/P-bodies with stress granules. Adv Exp Med Biol 768: 197–211. doi: 10.1007/978-1-4614-5107-5_12 23224972
38. Shao Y, Feng L, Rutherford ST, Papenfort K, Bassler BL (2013) Functional determinants of the quorum-sensing non-coding RNAs and their roles in target regulation. EMBO J 32: 2158–2171. doi: 10.1038/emboj.2013.155 23838640
39. Tsai YC, Du D, Dominguez-Malfavon L, Dimastrogiovanni D, Cross J, et al. (2012) Recognition of the 70S ribosome and polysome by the RNA degradosome in Escherichia coli. Nucleic Acids Res 40: 10417–10431. doi: 10.1093/nar/gks739 22923520
40. Morita T, Maki K, Aiba H (2005) RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev 19: 2176–2186. doi: 10.1101/gad.1330405 16166379
41. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, et al. (2005) GROMACS: fast, flexible, and free. J Comput Chem 26: 1701–1718. doi: 10.1002/jcc.20291 16211538
42. Poger D, Mark AE (2009) On the Validation of Molecular Dynamics Simulations of Saturated and cis-Monounsaturated Phosphatidylcholine Lipid Bilayers: A Comparison with Experiment. J Chem Theory Comput 6: 325–336. doi: 10.1021/ct900487a
43. Poger D, Van Gunsteren WF, Mark AE (2010) A new force field for simulating phosphatidylcholine bilayers. J Comput Chem 31: 1117–1125. doi: 10.1002/jcc.21396 19827145
44. Berendsen H, Postma J, van Gunsteren W, Hermans J (1981) Interaction Models for Water in Relation to Protein Hydration. In: Pullman B, editor. Intermolecular Forces. Dordrecht, The Netherlands: Reidel Publishing Company.
45. Nose S (1984) A molecular dynamics method for simulations in the canonical ensemble. Mol Phys 52: 255–268. doi: 10.1080/00268978400101201
46. Hoover WG (1985) Canonical dynamics: Equilibrium phase-space distributions. Phys Rev A 31: 1695–1697. doi: 10.1103/PhysRevA.31.1695 9895674
47. Parrinello M, Rahman AJ (1981) J Appl Phys 52: 7182–7190. doi: 10.1063/1.328693
48. Hess B, Bekker H, Berendsen HJC, Fraaije J (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18: 1463–1472. doi: 10.1002/(SICI)1096-987X(199709)18:12%3C1463::AID-JCC4%3E3.3.CO;2-L
49. Bond PJ, Sansom MS (2006) Insertion and assembly of membrane proteins via simulation. J Am Chem Soc 128: 2697–2704. doi: 10.1021/ja0569104 16492056
50. Bond PJ, Holyoake J, Ivetac A, Khalid S, Sansom MS (2007) Coarse-grained molecular dynamics simulations of membrane proteins and peptides. J Struct Biol 157: 593–605. doi: 10.1016/j.jsb.2006.10.004 17116404
51. Berendsen HJC, Postma JMP, van Gunsteren WF, DiNola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81: 3684–3690. doi: 10.1063/1.448118
52. Datsenko KA, Wanner BL (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. doi: 10.1073/pnas.120163297 10829079
53. Uzzau S, Figueroa-Bossi N, Rubino S, Bossi L (2001) Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci U S A 98: 15264–15269. doi: 10.1073/pnas.261348198 11742086
54. Carpousis AJ, Khemici V, Ait-Bara S, Poljak L (2008) Co-immunopurification of multiprotein complexes containing RNA-degrading enzymes. Methods Enzymol 447: 65–82. doi: 10.1016/S0076-6879(08)02204-0 19161838
55. Khemici V, Carpousis AJ (2004) The RNA degradosome and poly(A) polymerase of Escherichia coli are required in vivo for the degradation of small mRNA decay intermediates containing REP-stabilizers. Mol Microbiol 51: 777–790. doi: 10.1046/j.1365-2958.2003.03862.x 14731278
56. Neidhardt FC, Bloch PL, Smith DF (1974) Culture medium for enterobacteria. J Bacteriol 119: 736–747. 4604283
57. Strahl H, Hamoen LW (2010) Membrane potential is important for bacterial cell division. Proc Natl Acad Sci U S A 107: 12281–12286. doi: 10.1073/pnas.1005485107 20566861
58. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675. doi: 10.1038/nmeth.2089 22930834
59. Collins TJ (2007) ImageJ for microscopy. Biotechniques 43: 25–30. doi: 10.2144/000112517 17936939
60. Vanzo NF, Li YS, Py B, Blum E, Higgins CF, et al. (1998) Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev 12: 2770–2781. doi: 10.1101/gad.12.17.2770 9732274
61. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567–1572. doi: 10.1038/nbt1037
62. Ah-Seng Y, Rech J, Lane D, Bouet JY (2013) Defining the role of ATP hydrolysis in mitotic segregation of bacterial plasmids. PLoS Genet 9: e1003956. doi: 10.1371/journal.pgen.1003956 24367270
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2015 Číslo 2
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Genomic Selection and Association Mapping in Rice (): Effect of Trait Genetic Architecture, Training Population Composition, Marker Number and Statistical Model on Accuracy of Rice Genomic Selection in Elite, Tropical Rice Breeding Lines
- Discovery of Transcription Factors and Regulatory Regions Driving Tumor Development by ATAC-seq and FAIRE-seq Open Chromatin Profiling
- Evolutionary Signatures amongst Disease Genes Permit Novel Methods for Gene Prioritization and Construction of Informative Gene-Based Networks
- Proteotoxic Stress Induces Phosphorylation of p62/SQSTM1 by ULK1 to Regulate Selective Autophagic Clearance of Protein Aggregates