Structure, function and mechanisms of bacterial protein Hfq

doi:10.3969/j.issn.1000-2006.2016.05.025

FAN Ben, CHEN Sheng, LI Yulong

Journal of Nanjing Forestry University (Natural Sciences Edition） ›› 2016, Vol. 40 ›› Issue (05) : 155-162.

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Journal of Nanjing Forestry University (Natural Sciences Edition） ›› 2016, Vol. 40 ›› Issue (05) : 155-162. DOI: 10.3969/j.issn.1000-2006.2016.05.025

Structure, function and mechanisms of bacterial protein Hfq

FAN Ben, CHEN Sheng, LI Yulong

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Abstract

Bacterial small RNAs(sRNAs)have been one of the important research subjects in microbiology in last decade. They mainly act as a group of regulators controlling bacterial gene expression at post-transcriptional level. Most sRNAs regulate their mRNA targets involved by Hfq, which can facilitate base-paring of sRNA-mRNA and further affect mRNA stability or translation process. In this work the structure of Hfq, the molecular mechanisms of Hfq in sRNA regulation, and its influences detected in various bacterial species are reviewed. As a small chaperon protein ubiquitously present in many bacteria, the homohexamer form of Hfq possesses two unequivocal facets which can bind different types RNAs and promote their interaction. Such a structure provides a basis for its functional roles in mediating sRNA-mRNA interaction. While the hitherto studies on Hfq are mainly restricted in Gram-negative bacteria, its roles in some Gram-positive bacteria remain elusive. Moreover, the mechanisms underlying the impacts of Hfq on many important bacterial species have been still not clear. In future, it is necessary to further investigate the fine structure of Hfq with regard to its function as well as the detailed mechanism of the diverse bacterial phenotype affected by Hfq.

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FAN Ben, CHEN Sheng, LI Yulong. Structure, function and mechanisms of bacterial protein Hfq[J]. Journal of Nanjing Forestry University (Natural Sciences Edition）. 2016, 40(05): 155-162 https://doi.org/10.3969/j.issn.1000-2006.2016.05.025

References

[1] Franze de Fernandez M T, Eoyang L, August J T. Factor fraction required for the synthesis of bacteriophage Qbeta-RNA[J]. Nature, 1968, 219(5154):588-590.
[2] Carmichael G G, Weber K, Niveleau A, et al. The host factor required for RNA phage Qp RNA replication in vitro[J]. J Biol Chem, 1975, 250:3607-3612.
[3] Vogel J, Luisi B F. Hfq and its constellation of RNA[J]. Nat Rev Microbiol, 2011, 9(8):578-589. Doi:10.1038/nrmicro2615.
[4] Waters L S, Storz G. Regulatory RNAs in bacteria[J]. Cell, 2009, 136(4):615-628. Doi:10.1016/j.cell.2009.01.043.
[5] Gottesman S. Micros for microbes: non-coding regulatory RNAs in bacteria[J]. Trends Genet, 2005, 21(7):399-404. Doi:10.1016/j.tig.2005.05.008.
[6] Sobrero P, Valverde C. The bacterial protein Hfq: much more than a mere RNA-binding factor[J]. Critical Reviews in Microbiology, 2012, 38:276-299. Doi:10.3109/1040841x.2012.664540.
[7] Schumacher M A, Pearson R F, Mueller T, et al. Structure of the pleiotropic translational regulator Hfq and an Hfq-RNA complex:a bacterial Sm-like protein[J]. EMBO J, 2002, 21:3546-3556. Doi:10.1093/emboj/cdf322.
[8] Dondrup M, Albaum S P, Griebel T, et al. EMMA 2--a MAGE-compliant system for the collaborative analysis and integration of microarray data[J]. BMC Bioinformatics, 2009, 10:50. Doi:10.1186/1471-2105-10-50.
[9] Beich-Frandsen M, Vec^ˇerek B, Konarev P V, et al. Structural insights into the dynamics and function of the C-terminus of the E. coli RNA chaperone Hfq[J]. Nucleic Acids Research, 2011, 39(11):4900-4915. Doi:10.1093/nar/gkq1346.
[10] Beich-Frandsen M, Vec^ˇerek B, Sjöblom B, et al. Structural analysis of full-length Hfq from Escherichia coli[J]. Acta Crystallogr Sect F Struct Biol Cryst Commun, 2011, 67(Pt 5):536-540. Doi:10.1107/S174430911100786X.
[11] Ishikawa H, Otaka H, Maki K, et al. double or single hairpin preceded by a U-rich sequence and followed the functional Hfq-binding module of bacterial sRNAs consists of a by a 3' poly(U)tail[J]. RNA, 2012, 18(5):1062-1074. Doi:10.1261/rna.031575.111.
[12] Otaka H, Ishikawaa H, Moritab T, et al. PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action[J]. Proc Natl Acad Sci USA, 2011, 108:13059-13064. Doi:10.1073/pnas.1107050108.
[13] Sauer E, Schmidt S, Weichenrieder O. Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(24):9396-9401. Doi:10.1073/pnas.1202521109.
[14] Mikulecky P J, Kaw M K, Brescia C C, et al. Escherichia coli Hfq has distinct interaction surfaces for DsrA,rpoS and poly(A)RNAs[J]. Nat Struct Mol Biol, 2004, 11:1206-1214. Doi:10.1038/nsmb858.
[15] Zhang A, Schu D J, Tjaden B C, et al. Mutations in interaction surfaces differentially impact E. coli Hfq association with small RNAs and their mRNA targets[J]. J Mol Biol, 2013, 425:3678-3697. Doi:10.1016/j.jmb.2013.01.006.
[16] Soper T J, Woodson S A. The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA[J]. RNA, 2008, 14(9):1907-1917. Doi:10.1261/rna.1110608.
[17] Salim N N, Feig A L. An upstream Hfq binding site in the fhlA mRNA leader region facilitates the OxyS-fhlA interaction[J]. PLoS ONE, 2010, 5(9):e13028. Doi:10.1371/journal.pone.0013028.
[18] Salim N N, Faner M A, Philip J A, et al. Requirement of upstream Hfq-binding(ARN)x elements in glmS and the Hfq C-terminal region for GlmS upregulation by sRNAs GlmZ and GlmY[J]. Nucleic Acids Res, 2012, 40(16):8021-8032. Doi:10.1093/nar/gks392.
[19] Liang H, Zhao Y T, Zhang J Q, et al. Identification and functional characterization of small non-coding RNAs in Xanthomonas oryzae pathovar oryzae[J]. BMC Genomics, 2011, 12:87. Doi:10.1186/1471-2164-12-87.
[20] Fender A, Elf J, Hampel K, et al. RNAs actively cycle on the Sm-like protein Hfq[J]. Genes Dev, 2010, 24(23):2621-2626. Doi:10.1101/gad.591310.
[21] Moon K, Gottesman S. Competition among Hfq-binding small RNAs in Escherichia coli[J]. Molecular Microbiology, 2011, 82:1545-1562. Doi:10.1111/j.1365-2958.2011.07907.x.
[22] Olejniczak M. Despite similar binding to the Hfq protein regulatory RNAs widely differ in their competition performance[J]. Biochemistry, 2011, 50:4427-4440. Doi:10.1021/bi102043f.
[23] Hussein R, Lim H N. Disruption of small RNA signaling caused by competition for Hfq[J]. Proc Natl Acad Sci USA, 2010, 108(3):1110-1115. Doi:10.1073/pnas.1010082108.
[24] Sonnleitner E, Hagens S, Rosenau F, et al. Reduced virulence of a hfq mutant of Pseudomonas aeruginosa O1[J]. Microbial Pathogenesis, 2003, 35(5):217-228. Doi:10.1016/S0882-4010(03)00149-9.
[25] Ding Y, Davis B M, Waldor M K. Hfq is essential for Vibrio cholerae virulence and downregulates sigma expression[J]. Molecular Microbiology, 2004, 53(1):345-54. Doi:10.1111/j.1365-2958.2004.04142.x.
[26] Kulesus R R, Diaz-Perez K, Slechta E S, et al. Impact of the RNA chaperone Hfq on the fitness and virulence potential of uropathogenic Escherichia coli[J]. Infect Immun, 2008, 76(7):3019-3026. Doi:10.1128/IAI.00022-08.
[27] Kakoschke T, Kakoschke S, Magistro G, et al. The RNA chaperone Hfq impacts growth, metabolism and production of virulence factors in Yersinia enterocolitica[J]. PLoS One, 2014, 9(1):e86113. Doi:10.1371/journal.pone.0086113.
[28] Sittka A, Pfeiffer V, Tedin K, et al. The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium[J]. Mol Microbiol, 2007, 63(1):193-217. Doi:10.1111/j.1365-2958.2006.05489.x.
[29] Geng J, Song Y, Yang L, et al. Involvement of the post-transcriptional regulator Hfq in Yersinia pestis virulence[J]. PLoS ONE, 2009, 4(7):e6213. Doi:10.1371/journal.pone.0006213.
[30] Liu Y, Wu N, Dong J, et al. Hfq is a global regulator that controls the pathogenicity of Staphylococcus aureus[J]. PLoS ONE, 2010, 5(9):e013069. Doi:10.1371/journal.pone.0013069.
[31] Cui M, Wang T, Xu J, et al. Impact of Hfq on global gene expression and intracellular survival in Brucella melitensis[J]. PLoS One, 2013, 8(8):e71933. Doi:10.1371/journal.pone.0071933.
[32] Sittka A, Pfeiffer V, Tedin K, et al. The rna chaperone hfq is essential for the virulence of salmonella typhimurium[J]. Molecular Microbiology, 2007, 63(1):192-217.
[33] Wang M C, Chien H F, Tsai Y L, et al. The RNA chaperone Hfq is involved in stress tolerance and virulence in uropathogenic Proteus mirabilis[J]. PLoS One, 2014, 9(1):e85626. Doi:10.1371/journal.pone.0085626.
[34] Kim S, Hwang H, Kim K P, et al. The hfq plays important roles in virulence and stress adaptation in Cronobacter sakazakii ATCC 29544[J]. Infection and Immunity, 2015, 2015(9):03161-14. Doi:10.1128/IAI.03161-14.
[35] Nakao H, Watanabe H, Nakayama S, et al. yst gene expression in Yersinia enterocolitica is positively regulated by a chromosomal region that is highly homologous to Escherichia coli host factor 1 gene(hfq)[J]. Mol Microbiol, 1995, 18(5):859-865. Doi:10.1111/j.1365-2958.1995.18050859.x.
[36] Christiansen J K, Larsen M H, Ingmer H, et al. The RNA-binding protein Hfq of Listeria monocytogenes: role in stress tolerance and virulence[J]. J Bacteriol, 2004, 186(11):3355-3362. Doi:10.1128/JB.186.11.3355-3362.2004.
[37] Wilms I, Moller P, Stock A M, et al. Hfq influences multiple transport systems and virulence in the plant pathogen Agrobacterium tumefaciens[J]. J Bacteriol, 2012, 194(19):5209-5217. Doi:10.1128/JB.00510-12.
[38] Bibova I, Skopova K, Masin J, et al. The RNA chaperone Hfq is required for virulence of Bordetella pertussis[J]. Infect Immun, 2013, 81(11):4081-4090. Doi:10.1128/IAI.00345-13.
[39] Sousa S A, Ramos C G, Moreira L M, et al. The hfq gene is required for stress resistance and full virulence of Burkholderia cepacia to the nematode Caenorhabditis elegans[J]. Microbiology, 2010, 156(Pt 3):896-908. Doi:10.1099/mic.0.035139-0.
[40] Zeng Q, McNally R R, Sundin G W. Global small RNA chaperone Hfq and regulatory small RNAs are important virulence regulators in Erwinia amylovora[J]. J Bacteriol, 2013, 195(8):1706-1717. Doi:10.1128/JB.02056-12.
[41] Meibom K L, Forslund A L, Kuoppa K, et al. Hfq, a novel pleiotropic regulator of virulence-associated genes in Francisella tularensis[J]. Infection and Immunity, 2009, 77(5):1866-1880. Doi:10.1128/IAI.01496-08.
[42] Gangaiah D, Labandeira-Rey M, Zhang X, et al. Haemophilus ducreyi Hfq contributes to virulence gene regulation as cells enter stationary phase[J]. M Bio, 2014, 5(1):e01081-13. Doi:10.1128/mBio.01081-13.
[43] Chiang M K, Lu M C, Liu L C, et al. Impact of Hfq on global gene expression and virulence in Klebsiella pneumoniae[J]. PLoS One, 2011, 6(7):e22248. Doi:10.1371/journal.pone.0022248.
[44] Dietrich M, Munke R, Gottschald M, et al. The effect of hfq on global gene expression and virulence in Neisseria gonorrhoeae[J]. FEBS J, 2009, 276(19):5507-5520. Doi:10.1111/j.1742-4658.2009.07234.x.
[45] Fantappie L, Metruccio M M, Seib K L, et al. The RNA chaperone Hfq is involved in stress response and virulence in Neisseria meningitidis and is a pleiotropic regulator of protein expression[J]. Infect Immun, 2009, 77(5):1842-1853. Doi:10.1128/IAI.01216-08.
[46] Sharma A K, Payne S M. Induction of expression of hfq by DksA is essential for Shigella flexneri virulence[J]. Mol Microbiol, 2006, 62(2):469-79. Doi:10.1111/j.1365-2958.2006.05376.x.
[47]Tsui H C, Leung H C, Winkler M E. Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12[J]. Molecular Microbiology, 1994, 13(1):35-49. Doi:10.1111/j.1365-2958.1994.tb00400.x.
[48] Chambers J R, Bender K S. The RNA chaperone Hfq is important for growth and stress tolerance in Francisella novicida[J]. PLoS One, 2011, 6(5):e19797. Doi:10.1371/journal.pone.0019797.
[49] Berghoff B A, Glaeser J, Sharma C M, et al. Contribution of Hfq to photooxidative stress resistance and global regulation in Rhodobacter sphaeroides[J]. Mol Microbiol, 2011, 80(6):1479-1495. Doi:10.1111/j.1365-2958.2011.07658.x.
[50] Brennan C M, Keane M L, Hunt T M, et al. Shewanella oneidensis Hfq promotes exponential phase growth, stationary phase culture density, and cell survival[J]. BMC Microbiol, 2013, 13:33. Doi:10.1186/1471-2180-13-33.
[51] Yang S, Pelletier D A, Lu T Y, et al. The Zymomonas mobilis regulator hfq contributes to tolerance against multiple lignocellulosic pretreatment inhibitors[J]. BMC Microbiol, 2010, 10:135. Doi:10.1186/1471-2180-10-135.
[52] Subashchandrabose S, Leveque R M, Kirkwood R N, et al. The RNA chaperone Hfq promotes fitness of Actinobacillus pleuropneumoniae during porcine pleuropneumonia[J]. Infect Immun, 2013, 81(8):2952-2961. Doi:10.1128/IAI.00392-13.
[53] Fantappie L, Oriente F, Muzzi A, et al. A novel Hfq-dependent sRNA that is under FNR control and is synthesized in oxygen limitation in Neisseria meningitidis[J]. Mol Microbiol, 2011, 80(2):507-523. Doi:10.1111/j.1365-2958.2011.07592.x.
[54] Barra-Bily L, Fontenelle C, Jan G, et al. Proteomic alterations explain phenotypic changes in Sinorhizobium meliloti lacking the RNA chaperone Hfq[J]. J Bacteriol, 2010, 192(6):1719-1729. Doi:10.1128/JB.01429-09.
[55] Yamada J, Yamasaki S, Hirakawa H, et al. Impact of the RNA chaperone Hfq on multidrug resistance in Escherichia coli[J]. J Antimicrob Chemother, 2010, 65(5):853-858. Doi:10.1093/jac/dkq067.
[56] Hayashi-Nishino M, Fukushima A, Nishino K. Impact of hfq on the intrinsic drug resistance of Salmonella enterica serovar typhimurium[J]. Front Microbiol, 2012, 3:205. Doi:10.3389/fmicb.2012.00205.
[57] Maharjan R, McKenzie C, Yeung A, et al. The basis of antagonistic pleiotropy in Hfq mutations that have opposite effects on fitness at slow and fast growth rates[J]. Heredity(Edinb), 2013, 110(1):10-18. Doi:10.1038/hdy.2012.46.
[58] Brennan C M, Mazzucca N Q, Mezoian T, et al. Reduced heme levels underlie the exponential growth defect of the Shewanella oneidensis hfq mutant[J]. PLoS One, 2014, 9(10):e109879. Doi:PONE-D-14-27358[pii].
[59] Wu X G, Duan H M, Tian T, et al. Effect of the hfq gene on 2,4-diacetylphloroglucinol production and the PcoI/PcoR quorum-sensing system in Pseudomonas fluorescens 2P24[J]. FEMS Microbiol Lett, 2010, 309(1):16-24. Doi:10.1111/j.1574-6968.2010.02009.x.
[60] Gao M, Tang M, Guerich L, et al. Modulation of Sinorhizobium meliloti quorum sensing by Hfq-mediated post-transcriptional regulation of ExpR[J]. Environ Microbiol Rep, 2015, 7(1):148-154. Doi:10.1111/1758-2229.12235.
[61] Bardill J P, Zhao X, Hammer B K. The Vibrio cholerae quorum sensing response is mediated by Hfq-dependent sRNA/mRNA base pairing interactions[J]. Mol Microbiol, 2011, 80(5):1381-1394. Doi:10.1111/j.1365-2958.2011.07655.x.
[62] Lenz D H, Mok K C, Lilley B N, et al. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae[J]. Cell, 2004, 118(1):69-82. Doi:10.1016/j.cell.2004.06.009.
[63] Monteiro C, Papenfort K, Hentrich K, et al. Hfq and Hfq-dependent small RNAs are major contributors to multicellular development in Salmonella enterica serovar Typhimurium[J]. RNA Biology, 2012, 9(4):489-502. Doi:10.4161/rna.19682.
[64] Rempe K A, Hinz A K, Vadyvaloo V. Hfq regulates biofilm gut blockage that facilitates flea-borne transmission of Yersinia pestis[J]. J Bacteriol, 2012, 194(8):2036-2040. Doi:10.1128/JB.06568-11.
[65] Moller P, Overloper A, Forstner K U, et al. Profound impact of Hfq on nutrient acquisition, metabolism and motility in the plant pathogen Agrobacterium tumefaciens[J]. PLoS One, 2014, 9(10):e110427. Doi:10.1371/journal.pone.0110427.
[66] Dienst D, Duhring U, Mollenkopf H J, et al. The cyanobacterial homologue of the RNA chaperone Hfq is essential for motility of Synechocystis sp. PCC 6803[J]. Microbiology, 2008, 154(Pt 10):3134-3143. Doi:10.1099/mic.0.2008/020222-0.
[67] Puerta-Fernandez E, Vioque A. Hfq is required for optimal nitrate assimilation in the Cyanobacterium anabaena sp. strain PCC 7120[J]. J Bacteriol, 2011, 193(14):3546-3555. Doi:10.1128/JB.00254-11.
[68] Gao M, Barnett M J, Long S R, et al. Role of the Sinorhizobium meliloti global regulator Hfq in gene regulation and symbiosis[J]. Mol Plant Microbe Interact, 2010, 23(4):355-365. Doi:10.1094/MPMI-23-4-0355.
[69] Barra-Bily L, Pandey S P, Trautwetter A, et al. The Sinorhizobium meliloti RNA chaperone Hfq mediates symbiosis of S. meliloti and alfalfa[J]. J Bacteriol, 2010, 192(6):1710-1718. Doi:10.1128/JB.01427-09.
[70] Torres-Quesada O, Oruezabal R I, Peregrina A, et al. The Sinorhizobium meliloti RNA chaperone Hfq influences central carbon metabolism and the symbiotic interaction with alfalfa[J]. BMC Microbiol, 2010, 10:71. Doi:10.1186/1471-2180-10-71.
[71] Bibova I, Hot D, Keidel K, et al. Transcriptional profiling of Bordetella pertussis reveals requirement of RNA chaperone Hfq for type III secretion system functionality[J]. RNA Biol, 2015, 12(2):175-185. Doi:10.1080/15476286.2015.1017237.
[72] Shakhnovich E A, Davis B M, Waldor M K. Hfq negatively regulates type III secretion in EHEC and several other pathogens[J]. Molecular Microbiology, 2009, 74(2):347-363. Doi:10.1111/j.1365-2958.2009.06856.x.
[73] Niemann G S, Brown R N, Mushamiri I T, et al. RNA type III secretion signals that require Hfq[J]. J Bacteriol, 2013, 195(10):2119-2125. Doi:10.1128/JB.00024-13.
[74] Xu G, Zhao Y, Du L, et al. Hfq regulates antibacterial antibiotic biosynthesis and extracellular lytic-enzyme production in Lysobacter enzymogenes OH11[J]. Microb Biotechnol, 2015, 8(3):499-509. Doi:10.1111/1751-7915.12246.
[75] Wang G, Huang X, Li S, et al. The RNA chaperone Hfq regulates antibiotic biosynthesis in the rhizobacterium Pseudomonas aeruginosa M18[J]. J Bacteriol, 2012, 194(10):2443-2457. Doi:10.1128/JB.00029-12.
[76] Matilla M A, Leeper F J, Salmond G P. Biosynthesis of the antifungal haterumalide, oocydin A, in Serratia, and its regulation by quorum sensing, RpoS and Hfq[J]. Environmental Microbiology, 2015, 2015(6):1462-2920. Doi:10.1111/1462-2920.12839.
[77] Zhou M, Gao K, Zeng J, et al. Role of the RNA-binding protein Hfq in Serratia plymuthica[J]. Front Biosci(Elite Ed), 2012, 4:1263-1275. Doi:10.2741/e457.
[78] Zhang Y, Hong G. Evidences of Hfq associates with tryptophanase and affects extracellular indole levels[J]. Acta Biochim Biophys Sin(Shanghai), 2009, 41(8):709-717. Doi:0.1093/abbs/ gmp059.
[79] Cech G M, Pakula B, Kamrowska D, et al. Hfq protein deficiency in Escherichia coli affects ColE1-like but not lambda plasmid DNA replication[J]. Plasmid, 2014, 73:10-15. Doi:10.1016/j.plasmid.2014.04.005.
[80] Ross J A, Trussler R S, Black M D, et al. Tn5 transposition in Escherichia coli is repressed by Hfq and activated by over-expression of the small non-coding RNA SgrS[J]. Mob DNA, 2014, 5(1):27. Doi:10.1186/s13100-014-0027-z.
[81] Hess W R, Berghoff B A, Wilde A, et al. Riboregulators and the role of Hfq in photosynthetic bacteria[J]. RNA Biol, 2014, 11(5):413-426. Doi:10.4161/rna.28035.
[82] Allam U S, Krishna M G, Lahiri A, et al. Salmonella enterica serovar Typhimurium lacking hfq gene confers protective immunity against murine typhoid[J]. PLoS One, 2011, 6(2):e16667. Doi:10.1371/journal.pone.0016667.
[83] Schuergers N, Ruppert U, Watanabe S, et al. Binding of the RNA chaperone Hfq to the type IV pilus base is crucial for its function in Synechocystis sp. PCC 6803[J]. Molecular Microbiology, 2014, 92(4):840-852. Doi:10.1111/mmi.12595.
[84] Nielsen J S, Lei L K, Ebersbach T, et al. Defining a role for Hfq in Gram-positive bacteria: evidence for Hfq-dependent antisense regulation in Listeria monocytogenes[J]. Nucleic Acids Res, 2010, 38(3):907-919. Doi:10.1093/nar/gkp1081.
[85] Rochat T, Delumeau O, Figueroa-Bossi N, et al. Tracking the elusive function of Bacillus subtilis Hfq[J]. PLoS One, 2015, 10(4):e0124977. Doi:10.1371/journal.pone.0124977.
[86] Sun X, Zhulin I, Wartell R M. Predicted structure and phyletic distribution of the RNA-binding protein Hfq[J]. Nucleic Acids Res, 2002, 30(17):3662-3671. Doi:10.1093/nar/gkf508.
[87] Bohn C, Rigoulay C, Bouloc P. No detectable effect of RNA-binding protein Hfq absence in Staphylococcus aureus[J]. BMC Microbiology, 2007, 7(10):10. Doi:10.1186/1471-2180-7-10.
[88] Dambach M, Irnov I, Winkler W C. Association of RNAs with Bacillus subtilis Hfq[J]. PLoS One, 2013, 8(2):e55156. Doi:10.1371/journal.pone.0055156.
[89] Hammerle H, Amman F, Vecerek B, et al. Impact of Hfq on the Bacillus subtilis transcriptome[J]. PLoS One, 2014, 9(6):e98661. Doi:10.1371/journal.pone.0098661.
[90] Fortas E, Piccirilli F, Malabirade A, et al. New insight into the structure and function of Hfq C-terminus[J]. Biosci Rep, 2015, 35(2):e00190. Doi:10.1042/BSR20140128.
[91] Brennan R G, Link T M. Hfq structure, function and ligand binding[J]. Curr Opin Microbiol, 2007, 10(2):125-133. Doi:10.1016/j.mib.2007.03.015.
[92] Murina V, Lekontseva N, Nikulin A. Hfq binds ribonucleotides in three different RNA-binding sites[J]. Acta Crystallogr D Biol Crystallogr, 2013, 69(Pt 8):1504-1513. Doi:10.1107/S090744491301010X.
[93] Schulz E C, Barabas O. Structure of an Escherichia coli Hfq:RNA complex at 0.97 a resolution[J]. Acta Crystallogr F Struct Biol Commun, 2014, 70(Pt 11):1492-1497. Doi:10.1107/S2053230X14020044.
[94] Obregon K A, Hoch C T, Sukhodolets M V. Sm-like protein Hfq: Composition of the native complex, modifications, and interactions[J]. Biochim Biophys Acta, 2015, 1854(8):950-966. Doi:10.1016/j.bbapap.2015.03.016.
[95] Peng Y, Curtis J E, Fang X, et al. Structural model of an mRNA in complex with the bacterial chaperone Hfq[J]. Proc Natl Acad Sci U S A, 2014, 111(48):17134-17139. Doi:10.1073/pnas.1410114111.
[96] Zeng Q, Sundin G W. Genome-wide identification of Hfq-regulated small RNAs in the fire blight pathogen Erwinia amylovora discovered small RNAs with virulence regulatory function[J]. BMC Genomics, 2014, 15(414):414. Doi:10.1186/1471-2164-15-414.
[97] Lenco J, Tambor V, Link M, et al. Changes in proteome of the Deltahfq strain derived from Francisella tularensis LVS correspond with its attenuated phenotype[J]. Proteomics, 2014, 14(21-22):2400-2409. Doi:10.1002/pmic.201400198.
[98] Liu H, Wang Q, Liu Q, et al. Roles of Hfq in the stress adaptation and virulence in fish pathogen Vibrio alginolyticus and its potential application as a target for live attenuated vaccine[J]. Appl Microbiol Biotechnol, 2011, 91(2):353-364. Doi:10.1007/s00253-011-3286-3.

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