Bacterial RNA Chaperones and Chaperone-like Riboregulators: Behind the Scenes of RNA-mediated Regulation of Cellular Metabolism

Overview

Journal RNA Biol

Specialty Molecular Biology

Date 2022 Apr 19

PMID 35438047

Authors

Kai Katsuya-Gaviria

Giulia Paris

Tom Dendooven

Katarzyna J Bandyra

Affiliations

Soon will be listed here.

Abstract

In all domains of life, RNA chaperones safeguard and guide the fate of the cellular RNA pool. RNA chaperones comprise structurally diverse proteins that ensure proper folding, stability, and ribonuclease resistance of RNA, and they support regulatory activities mediated by RNA. RNA chaperones constitute a topologically diverse group of proteins that often present an unstructured region and bind RNA with limited nucleotide sequence preferences. In bacteria, three main proteins - Hfq, ProQ, and CsrA - have been shown to regulate numerous complex processes, including bacterial growth, stress response and virulence. Hfq and ProQ have well-studied activities as global chaperones with pleiotropic impact, while CsrA has a chaperone-like role with more defined riboregulatory function. Here, we describe relevant novel insights into their common features, including RNA binding properties, unstructured domains, and interplay with other proteins important to RNA metabolism.

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References

Otaka H, Ishikawa H, Morita T, Aiba H . PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action. Proc Natl Acad Sci U S A. 2011; 108(32):13059-64. PMC: 3156202. DOI: 10.1073/pnas.1107050108. View

Dimastrogiovanni D, Frohlich K, Bandyra K, Bruce H, Hohensee S, Vogel J . Recognition of the small regulatory RNA RydC by the bacterial Hfq protein. Elife. 2015; 3. PMC: 4337610. DOI: 10.7554/eLife.05375. View

Kay E, Dubuis C, Haas D . Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc Natl Acad Sci U S A. 2005; 102(47):17136-41. PMC: 1287983. DOI: 10.1073/pnas.0505673102. View

Frohlich K, Velasco Gomariz M . RNA-controlled regulation in Caulobacter crescentus. Curr Opin Microbiol. 2021; 60:1-7. DOI: 10.1016/j.mib.2021.01.002. View

Zhang A, Schu D, Tjaden B, Storz G, Gottesman S . Mutations in interaction surfaces differentially impact E. coli Hfq association with small RNAs and their mRNA targets. J Mol Biol. 2013; 425(19):3678-97. PMC: 3640674. DOI: 10.1016/j.jmb.2013.01.006. View

Berndt V, Beckstette M, Volk M, Dersch P, Bronstrup M . Metabolome and transcriptome-wide effects of the carbon storage regulator A in enteropathogenic Escherichia coli. Sci Rep. 2019; 9(1):138. PMC: 6333774. DOI: 10.1038/s41598-018-36932-w. View

McQuail J, Carpousis A, Wigneshweraraj S . The association between Hfq and RNase E in long-term nitrogen-starved Escherichia coli. Mol Microbiol. 2021; 117(1):54-66. DOI: 10.1111/mmi.14782. View

Parker A, Cureoglu S, De Lay N, Majdalani N, Gottesman S . Alternative pathways for Escherichia coli biofilm formation revealed by sRNA overproduction. Mol Microbiol. 2017; 105(2):309-325. PMC: 5510166. DOI: 10.1111/mmi.13702. View

Rife C, Schwarzenbacher R, McMullan D, Abdubek P, Ambing E, Axelrod H . Crystal structure of the global regulatory protein CsrA from Pseudomonas putida at 2.05 A resolution reveals a new fold. Proteins. 2005; 61(2):449-53. DOI: 10.1002/prot.20502. View

10.

Duss O, Michel E, Yulikov M, Schubert M, Jeschke G, Allain F . Structural basis of the non-coding RNA RsmZ acting as a protein sponge. Nature. 2014; 509(7502):588-92. DOI: 10.1038/nature13271. View

11.

Pei X, Dendooven T, Sonnleitner E, Chen S, Blasi U, Luisi B . Architectural principles for Hfq/Crc-mediated regulation of gene expression. Elife. 2019; 8. PMC: 6422490. DOI: 10.7554/eLife.43158. View

12.

Santiago-Frangos A, Frohlich K, Jeliazkov J, Malecka E, Marino G, Gray J . Hfq structure reveals a conserved mechanism of RNA annealing regulation. Proc Natl Acad Sci U S A. 2019; 116(22):10978-10987. PMC: 6561178. DOI: 10.1073/pnas.1814428116. View

13.

Rizvanovic A, Kjellin J, Soderbom F, Holmqvist E . Saturation mutagenesis charts the functional landscape of Salmonella ProQ and reveals a gene regulatory function of its C-terminal domain. Nucleic Acids Res. 2021; 49(17):9992-10006. PMC: 8464044. DOI: 10.1093/nar/gkab721. View

14.

Dendooven T, Sinha D, Roeselova A, Cameron T, De Lay N, Luisi B . A cooperative PNPase-Hfq-RNA carrier complex facilitates bacterial riboregulation. Mol Cell. 2021; 81(14):2901-2913.e5. PMC: 8294330. DOI: 10.1016/j.molcel.2021.05.032. View

15.

Smirnov A, Forstner K, Holmqvist E, Otto A, Gunster R, Becher D . Grad-seq guides the discovery of ProQ as a major small RNA-binding protein. Proc Natl Acad Sci U S A. 2016; 113(41):11591-11596. PMC: 5068311. DOI: 10.1073/pnas.1609981113. View

16.

Callaghan A, Marcaida M, Stead J, McDowall K, Scott W, Luisi B . Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature. 2005; 437(7062):1187-91. DOI: 10.1038/nature04084. View

17.

Karlinsey J, Tanaka S, Bettenworth V, Yamaguchi S, Boos W, Aizawa S . Completion of the hook-basal body complex of the Salmonella typhimurium flagellum is coupled to FlgM secretion and fliC transcription. Mol Microbiol. 2000; 37(5):1220-31. DOI: 10.1046/j.1365-2958.2000.02081.x. View

18.

Kutsukake K, Ohya Y, Iino T . Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J Bacteriol. 1990; 172(2):741-7. PMC: 208501. DOI: 10.1128/jb.172.2.741-747.1990. View

19.

Tauber D, Tauber G, Parker R . Mechanisms and Regulation of RNA Condensation in RNP Granule Formation. Trends Biochem Sci. 2020; 45(9):764-778. PMC: 7211619. DOI: 10.1016/j.tibs.2020.05.002. View

20.

Mercante J, Edwards A, Dubey A, Babitzke P, Romeo T . Molecular geometry of CsrA (RsmA) binding to RNA and its implications for regulated expression. J Mol Biol. 2009; 392(2):511-28. PMC: 2735826. DOI: 10.1016/j.jmb.2009.07.034. View