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Hfq and its constellation of RNA

Key Points

  • Hfq is a conserved bacterial RNA-binding protein with complex roles in post-transcriptional gene regulation. Although studies of Hfq are rapidly advancing through the insights provided from crystal structures and from studies of mutant phenotypes and genetic responses, many aspects remain poorly understood.

  • At the level of protein structure, Hfq has a simple fold, with small protomers of 11 kDa forming a ring-like quaternary architecture that presents two distinct surfaces which can bind RNA. Homologues of Hfq that have a similar ring-like quaternary structure occur in the archaea and eukaryotes. Recent X-ray crystal structures and solution data provide insight into how Hfq binds RNA, with its two RNA-binding surfaces having distinct sequence preferences.

  • At the level of phenotype and gene expression, compelling data show a role for Hfq in mediating complex processes, such as quorum sensing and invasive virulence of pathogens.

  • One key function of bacterial Hfq is to mediate the activity of small non-coding RNAs (sRNAs) in the modulation of mRNA translation. Hfq seems to display in vivo specificity towards certain sRNAs and mRNAs.

  • Depending on its RNA partner and the context, Hfq can mediate either silencing or activation of gene expression at the post-transcriptional level. Although some aspects of these processes may be interpreted based on the available crystallographic and biochemical data, the current understanding is not sufficiently advanced to make robust predictions for the outcome of a given Hfq–RNA interaction.

  • Hfq cooperates with protein partners, such as ribonuclease E (RNase E) and the transcription termination factor Rho, for its biological activity. The association of Hfq with RNase E seems to trigger degradation of certain mRNAs that are recognized through sRNA partners.

  • Although Hfq is an abundant protein, it seems to be present at limiting concentrations for its binding partners. Thus, it is difficult to understand how an sRNA binds to Hfq to become an efficient mediator of gene regulation, and how Hfq contributes to fast-acting regulatory responses.

Abstract

Hfq is an RNA-binding protein that is common to diverse bacterial lineages and has key roles in the control of gene expression. By facilitating the pairing of small RNAs with their target mRNAs, Hfq affects the translation and turnover rates of specific transcripts and contributes to complex post-transcriptional networks. These functions of Hfq can be attributed to its ring-like oligomeric architecture, which presents two non-equivalent binding surfaces that are capable of multiple interactions with RNA molecules. Distant homologues of Hfq occur in archaea and eukaryotes, reflecting an ancient origin for the protein family and hinting at shared functions. In this Review, we describe the salient structural and functional features of Hfq and discuss possible mechanisms by which this protein can promote RNA interactions to catalyse specific and rapid regulatory responses in vivo.

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Figure 1: Widely accepted modes of Hfq activity.
Figure 2: The structure of Hfq and its interactions with RNA.
Figure 3: A typical Hfq-associated small RNA.
Figure 4: A three-body problem involving Hfq, small RNA and mRNA.
Figure 5: A model for RNA exchange on Hfq.

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Acknowledgements

We thank J. Steitz, K. Weber, A. Callaghan, H. Vincent, K. Bandyra and many other colleagues for stimulating discussions about Hfq–RNA interactions and about their work. We are indebted to O. Weichenrieder for help with figure 3b. We thank K. Lipkow and S. Andrews for discussion about intracellular diffusion rates in bacteria. Work in the Vogel laboratory is supported by the National Genome Reseach Network Plus (NGFN+) grant RNomics of Infectious diseases (funded by the German Federal Ministry of Education and Research (BMBF)), and by German Research Foundation (DFG) Priority Programme SPP1258 Sensory and Regulatory RNAs in Prokaryotes (Grants VO8751/2-4). The Luisi laboratory is supported by the Wellcome Trust.

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Structural data for Hfq and Sm-like proteins. (PDF 158 kb)

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Glossary

Chaperones

Protective carriers for a meta-stable state of a macromolecule; for proteins, chaperones assist protein folding, and in the context used here, a chaperone confers protection to RNA species that are vulnerable to chemical or enzymatic attack.

RNA decoys

Cellular RNAs that inactivate regulatory RNAs by mimicry of their actual targets.

Protomers

Subunits of an oligomeric assembly.

Hetero-oligomers

Protein assemblies in which the subunits are not chemically identical.

Spliceosome

The series of multicomponent assemblies that dynamically remodel and cleave introns from eukaryotic mRNAs.

Trans-actions

Regulatory base-pairing of a small RNA with a trans-encoded target mRNA.

Rho-independent transcription terminator

A stable secondary RNA structure followed by a short poly(U) stretch that destabilizes the RNA–DNA duplex during transcription so that the RNA polymerase falls off.

Aptamer

An oligonucleotide that is selected in vitro from a large population of combinatorial variants for a targeted property, such as binding to a defined protein.

Pseudoknot

A structure that is formed when duplex-forming regions are interwoven, so that half of one duplex is intercalated between the two halves of another duplex.

Poly(A) polymerase

An important enzyme that catalyses the addition of adenosine to the 3′ end of mRNA and thereby accelerates RNA turnover in vivo.

On rate

In classical reaction kinetics, the rate of complex formation, with dimensions of concentration per unit time for simple binary associations.

Polynucleotide phosphorylase

(PNPase). An exoribonuclease that uses phosphate as an attacking group to sequentially liberate nucleoside 5′-diphosphates from the 3′ end of an RNA.

Degradosome

A multi-enzyme assembly that was first identified in Escherichia coli and is found in many other bacterial lineages. In E. coli, the canonical components are ribonuclease E and polynucleotide phosphorylase, as well as a DEAD-box RNA helicase and the glycolytic enzyme enolase.

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Vogel, J., Luisi, B. Hfq and its constellation of RNA. Nat Rev Microbiol 9, 578–589 (2011). https://doi.org/10.1038/nrmicro2615

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