Viral Interference of the Bacterial RNA Metabolism Machinery

Overview

Journal RNA Biol

Specialty Molecular Biology

Date 2016 Nov 12

PMID 27834591

Citations 6

Authors

Tom Dendooven

An Van den Bossche

Hanne Hendrix

Pieter-Jan Ceyssens

Marleen Voet

K J Bandyra

Marc De Maeyer

Abram Aertsen

Jean-Paul Noben

Steven W Hardwick

Ben F Luisi

Rob Lavigne

Affiliations

Soon will be listed here.

Abstract

In a recent publication, we reported a unique interaction between a protein encoded by the giant myovirus phiKZ and the Pseudomonas aeruginosa RNA degradosome. Crystallography, site-directed mutagenesis and interactomics approaches revealed this 'degradosome interacting protein' or Dip, to adopt an 'open-claw' dimeric structure that presents acidic patches on its outer surface which hijack 2 conserved RNA binding sites on the scaffold domain of the RNase E component of the RNA degradosome. This interaction prevents substrate RNAs from being bound and degraded by the RNA degradosome during the virus infection cycle. In this commentary, we provide a perspective into the biological role of Dip, its structural analysis and its mysterious evolutionary origin, and we suggest some therapeutic and biotechnological applications of this distinctive viral protein.

Citing Articles

Interaction between Phage T4 Protein RIII and Host Ribosomal Protein S1 Inhibits Endoribonuclease RegB Activation.

Juskauskas A, Zajanckauskaite A, Meskys R, Ger M, Kaupinis A, Valius M Int J Mol Sci. 2022; 23(16).

PMID: 36012768 PMC: 9409239. DOI: 10.3390/ijms23169483.

The world of ribonucleases from pseudomonads: a short trip through the main features and singularities.

Apura P, Goncalves L, Viegas S, Arraiano C Microb Biotechnol. 2021; 14(6):2316-2333.

PMID: 34427985 PMC: 8601179. DOI: 10.1111/1751-7915.13890.

A Grad-seq View of RNA and Protein Complexes in Pseudomonas aeruginosa under Standard and Bacteriophage Predation Conditions.

Gerovac M, Wicke L, Chihara K, Schneider C, Lavigne R, Vogel J mBio. 2021; 12(1).

PMID: 33563827 PMC: 8545117. DOI: 10.1128/mBio.03454-20.

RNase E and the High-Fidelity Orchestration of RNA Metabolism.

Bandyra K, Luisi B Microbiol Spectr. 2018; 6(2).

PMID: 29676248 PMC: 11633573. DOI: 10.1128/microbiolspec.RWR-0008-2017.

Phage or foe: an insight into the impact of viral predation on microbial communities.

Fernandez L, Rodriguez A, Garcia P ISME J. 2018; 12(5):1171-1179.

PMID: 29371652 PMC: 5932045. DOI: 10.1038/s41396-018-0049-5.

References

Breidenstein E, de la Fuente-Nunez C, Hancock R . Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol. 2011; 19(8):419-26. DOI: 10.1016/j.tim.2011.04.005. View

Brussow H . What is needed for phage therapy to become a reality in Western medicine?. Virology. 2012; 434(2):138-42. DOI: 10.1016/j.virol.2012.09.015. View

Bandyra K, Bouvier M, Carpousis A, Luisi B . The social fabric of the RNA degradosome. Biochim Biophys Acta. 2013; 1829(6-7):514-22. PMC: 3991390. DOI: 10.1016/j.bbagrm.2013.02.011. View

Deutscher M . Degradation of stable RNA in bacteria. J Biol Chem. 2003; 278(46):45041-4. DOI: 10.1074/jbc.R300031200. View

Bassetti M, Merelli M, Temperoni C, Astilean A . New antibiotics for bad bugs: where are we?. Ann Clin Microbiol Antimicrob. 2013; 12:22. PMC: 3846448. DOI: 10.1186/1476-0711-12-22. View

Stover C, Pham X, Erwin A, Mizoguchi S, Warrener P, Hickey M . Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature. 2000; 406(6799):959-64. DOI: 10.1038/35023079. View

Sulthana S, Basturea G, Deutscher M . Elucidation of pathways of ribosomal RNA degradation: an essential role for RNase E. RNA. 2016; 22(8):1163-71. PMC: 4931109. DOI: 10.1261/rna.056275.116. View

Hauser R, Blasche S, Dokland T, Haggard-Ljungquist E, von Brunn A, Salas M . Bacteriophage protein-protein interactions. Adv Virus Res. 2012; 83:219-98. PMC: 3461333. DOI: 10.1016/B978-0-12-394438-2.00006-2. View

Gorna M, Carpousis A, Luisi B . From conformational chaos to robust regulation: the structure and function of the multi-enzyme RNA degradosome. Q Rev Biophys. 2011; 45(2):105-45. DOI: 10.1017/S003358351100014X. View

10.

Miczak A, Kaberdin V, Wei C, Lin-Chao S . Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc Natl Acad Sci U S A. 1996; 93(9):3865-9. PMC: 39450. DOI: 10.1073/pnas.93.9.3865. View

11.

Deutscher M . Degradation of RNA in bacteria: comparison of mRNA and stable RNA. Nucleic Acids Res. 2006; 34(2):659-66. PMC: 1360286. DOI: 10.1093/nar/gkj472. View

12.

Van den Bossche A, Ceyssens P, De Smet J, Hendrix H, Bellon H, Leimer N . Systematic identification of hypothetical bacteriophage proteins targeting key protein complexes of Pseudomonas aeruginosa. J Proteome Res. 2014; 13(10):4446-56. DOI: 10.1021/pr500796n. View

13.

Kime L, Vincent H, Gendoo D, Jourdan S, Fishwick C, Callaghan A . The first small-molecule inhibitors of members of the ribonuclease E family. Sci Rep. 2015; 5:8028. PMC: 4306137. DOI: 10.1038/srep08028. View

14.

Endersen L, OMahony J, Hill C, Ross R, McAuliffe O, Coffey A . Phage therapy in the food industry. Annu Rev Food Sci Technol. 2014; 5:327-49. DOI: 10.1146/annurev-food-030713-092415. View

15.

Bandyra K, Luisi B . Licensing and due process in the turnover of bacterial RNA. RNA Biol. 2013; 10(4):627-35. PMC: 3710370. DOI: 10.4161/rna.24393. View

16.

Liu J, Dehbi M, Moeck G, Arhin F, Bauda P, Bergeron D . Antimicrobial drug discovery through bacteriophage genomics. Nat Biotechnol. 2004; 22(2):185-91. DOI: 10.1038/nbt932. View

17.

Walkinshaw M, Taylor P, Sturrock S, Atanasiu C, Berge T, Henderson R . Structure of Ocr from bacteriophage T7, a protein that mimics B-form DNA. Mol Cell. 2002; 9(1):187-94. DOI: 10.1016/s1097-2765(02)00435-5. View

18.

Ceyssens P, Minakhin L, Van den Bossche A, Yakunina M, Klimuk E, Blasdel B . Development of giant bacteriophage ϕKZ is independent of the host transcription apparatus. J Virol. 2014; 88(18):10501-10. PMC: 4178840. DOI: 10.1128/JVI.01347-14. View

19.

Gao J, Lee K, Zhao M, Qiu J, Zhan X, Saxena A . Differential modulation of E. coli mRNA abundance by inhibitory proteins that alter the composition of the degradosome. Mol Microbiol. 2006; 61(2):394-406. DOI: 10.1111/j.1365-2958.2006.05246.x. View

20.

Mackie G . RNase E: at the interface of bacterial RNA processing and decay. Nat Rev Microbiol. 2012; 11(1):45-57. DOI: 10.1038/nrmicro2930. View