Structure and RNA-binding Properties of the Bacterial LSm Protein Hfq

Overview

Journal RNA Biol

Specialty Molecular Biology

Date 2013 Mar 29

PMID 23535768

Citations 42

Authors

Evelyn Sauer

Affiliations

Soon will be listed here.

Abstract

Over the past years, small non-coding RNAs (sRNAs) emerged as important modulators of gene expression in bacteria. Guided by partial sequence complementarity, these sRNAs interact with target mRNAs and eventually affect transcript stability and translation. The physiological function of sRNAs depends on the protein Hfq, which binds sRNAs in the cell and promotes the interaction with their mRNA targets. This important physiological function of Hfq as a central hub of sRNA-mediated regulation made it one of the most intensely studied proteins in bacteria. Recently, a new model for sRNA binding by Hfq has been proposed that involves the direct recognition of the sRNA 3' end and interactions of the sRNA body with the lateral RNA-binding surface of Hfq. This review summarizes the current understanding of the RNA binding properties of Hfq and its (s)RNA complexes. Moreover, the implications of the new binding model for sRNA-mediated regulation are discussed.

Citing Articles

HP-Bodies - Ancestral Condensates that Regulate RNA Turnover and Protein Translation in Bacteria.

Guan J, Hurto R, Rai A, Azaldegui C, Ortiz-Rodriguez L, Biteen J bioRxiv. 2025; .

PMID: 39975000 PMC: 11839049. DOI: 10.1101/2025.02.06.636932.

Two temperature-responsive RNAs act in concert: the small RNA CyaR and the mRNA ompX.

Guanzon D, Pienkoss S, Brandenburg V, Roder J, Scheller D, Dietze A Nucleic Acids Res. 2025; 53(3).

PMID: 39907110 PMC: 11795201. DOI: 10.1093/nar/gkaf041.

An sRNA overexpression library reveals AbnZ as a negative regulator of an essential translocation module in Caulobacter crescentus.

Velasco-Gomariz M, Sulzer J, Faber F, Frohlich K Nucleic Acids Res. 2024; 53(1.

PMID: 39657128 PMC: 11724286. DOI: 10.1093/nar/gkae1139.

RNA compaction and iterative scanning for small RNA targets by the Hfq chaperone.

Malecka E, Woodson S Nat Commun. 2024; 15(1):2069.

PMID: 38453956 PMC: 10920880. DOI: 10.1038/s41467-024-46316-6.

Insights into the complementation potential of the extreme acidophile's orthologue in replacing Escherichia coli hfq gene-particularly in bacterial resistance to environmental stress.

Hu W, Huo X, Bai H, Chen Z, Zhang J, Yang H World J Microbiol Biotechnol. 2024; 40(4):105.

PMID: 38386219 DOI: 10.1007/s11274-024-03924-0.

References

Schumacher M, Pearson R, Moller T, Valentin-Hansen P, Brennan R . Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. EMBO J. 2002; 21(13):3546-56. PMC: 126077. DOI: 10.1093/emboj/cdf322. View

Collins B, Harrop S, Kornfeld G, Dawes I, Curmi P, Mabbutt B . Crystal structure of a heptameric Sm-like protein complex from archaea: implications for the structure and evolution of snRNPs. J Mol Biol. 2001; 309(4):915-23. DOI: 10.1006/jmbi.2001.4693. View

Hopkins J, Panja S, McNeil S, Woodson S . Effect of salt and RNA structure on annealing and strand displacement by Hfq. Nucleic Acids Res. 2009; 37(18):6205-13. PMC: 2764445. DOI: 10.1093/nar/gkp646. View

Sittka A, Lucchini S, Papenfort K, Sharma C, Rolle K, Binnewies T . Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet. 2008; 4(8):e1000163. PMC: 2515195. DOI: 10.1371/journal.pgen.1000163. View

Das D, Kozbial P, Axelrod H, Miller M, McMullan D, Sri Krishna S . Crystal structure of a novel Sm-like protein of putative cyanophage origin at 2.60 A resolution. Proteins. 2009; 75(2):296-307. PMC: 2785455. DOI: 10.1002/prot.22360. View

FRANZE DE FERNANDEZ M, Hayward W, August J . Bacterial proteins required for replication of phage Q ribonucleic acid. Pruification and properties of host factor I, a ribonucleic acid-binding protein. J Biol Chem. 1972; 247(3):824-31. View

Sauter C, Basquin J, Suck D . Sm-like proteins in Eubacteria: the crystal structure of the Hfq protein from Escherichia coli. Nucleic Acids Res. 2003; 31(14):4091-8. PMC: 167641. DOI: 10.1093/nar/gkg480. View

Morita T, Aiba H . RNase E action at a distance: degradation of target mRNAs mediated by an Hfq-binding small RNA in bacteria. Genes Dev. 2011; 25(4):294-8. PMC: 3042153. DOI: 10.1101/gad.2030311. View

Sittka A, Pfeiffer V, Tedin K, Vogel J . The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol Microbiol. 2006; 63(1):193-217. PMC: 1810395. DOI: 10.1111/j.1365-2958.2006.05489.x. View

10.

Soper T, Doxzen K, Woodson S . Major role for mRNA binding and restructuring in sRNA recruitment by Hfq. RNA. 2011; 17(8):1544-50. PMC: 3153977. DOI: 10.1261/rna.2767211. View

11.

Mura C, Cascio D, Sawaya M, Eisenberg D . The crystal structure of a heptameric archaeal Sm protein: Implications for the eukaryotic snRNP core. Proc Natl Acad Sci U S A. 2001; 98(10):5532-7. PMC: 33247. DOI: 10.1073/pnas.091102298. View

12.

Tsui H, Feng G, Winkler M . Negative regulation of mutS and mutH repair gene expression by the Hfq and RpoS global regulators of Escherichia coli K-12. J Bacteriol. 1997; 179(23):7476-87. PMC: 179700. DOI: 10.1128/jb.179.23.7476-7487.1997. View

13.

Papenfort K, Bouvier M, Mika F, Sharma C, Vogel J . Evidence for an autonomous 5' target recognition domain in an Hfq-associated small RNA. Proc Natl Acad Sci U S A. 2010; 107(47):20435-40. PMC: 2996696. DOI: 10.1073/pnas.1009784107. View

14.

Pomeranz Krummel D, Oubridge C, Leung A, Li J, Nagai K . Crystal structure of human spliceosomal U1 snRNP at 5.5 A resolution. Nature. 2009; 458(7237):475-80. PMC: 2673513. DOI: 10.1038/nature07851. View

15.

Hajnsdorf E, Regnier P . Host factor Hfq of Escherichia coli stimulates elongation of poly(A) tails by poly(A) polymerase I. Proc Natl Acad Sci U S A. 2000; 97(4):1501-5. PMC: 26463. DOI: 10.1073/pnas.040549897. View

16.

Bayer T, Booth L, Knudsen S, Ellington A . Arginine-rich motifs present multiple interfaces for specific binding by RNA. RNA. 2005; 11(12):1848-57. PMC: 1370873. DOI: 10.1261/rna.2167605. View

17.

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

18.

Miranda G, Schuppli D, Barrera I, Hausherr C, Sogo J, Weber H . Recognition of bacteriophage Qbeta plus strand RNA as a template by Qbeta replicase: role of RNA interactions mediated by ribosomal proteins S1 and host factor. J Mol Biol. 1997; 267(5):1089-103. DOI: 10.1006/jmbi.1997.0939. View

19.

Folichon M, Arluison V, Pellegrini O, Huntzinger E, Regnier P, Hajnsdorf E . The poly(A) binding protein Hfq protects RNA from RNase E and exoribonucleolytic degradation. Nucleic Acids Res. 2003; 31(24):7302-10. PMC: 291859. DOI: 10.1093/nar/gkg915. View

20.

Panja S, Woodson S . Hexamer to monomer equilibrium of E. coli Hfq in solution and its impact on RNA annealing. J Mol Biol. 2012; 417(5):406-12. PMC: 3303956. DOI: 10.1016/j.jmb.2012.02.009. View