Comparative Integrated Omics Analysis of the Hfq Regulon in Bordetella pertussis
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
19-12338S
Grantová Agentura České Republiky
MSM200201702
Akademie Věd České Republiky
PubMed
31238496
PubMed Central
PMC6627887
DOI
10.3390/ijms20123073
PII: ijms20123073
Knihovny.cz E-zdroje
- Klíčová slova
- Bordetella pertussis, Hfq, T3SS, omics analysis, serum resistance, solute-binding proteins,
- MeSH
- Bordetella pertussis genetika metabolismus MeSH
- chromatografie kapalinová MeSH
- genová ontologie MeSH
- lidé MeSH
- protein hostitelského faktoru 1 genetika metabolismus MeSH
- proteom MeSH
- proteomika * metody MeSH
- regulace genové exprese u bakterií * MeSH
- regulon * MeSH
- sekreční systém typu III genetika metabolismus MeSH
- stanovení celkové genové exprese * metody MeSH
- tandemová hmotnostní spektrometrie MeSH
- transkriptom MeSH
- výpočetní biologie metody MeSH
- vysoce účinné nukleotidové sekvenování MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- protein hostitelského faktoru 1 MeSH
- proteom MeSH
- sekreční systém typu III MeSH
Bordetella pertussis is a Gram-negative strictly human pathogen of the respiratory tract and the etiological agent of whooping cough (pertussis). Previously, we have shown that RNA chaperone Hfq is required for virulence of B. pertussis. Furthermore, microarray analysis revealed that a large number of genes are affected by the lack of Hfq. This study represents the first attempt to characterize the Hfq regulon in bacterial pathogen using an integrative omics approach. Gene expression profiles were analyzed by RNA-seq and protein amounts in cell-associated and cell-free fractions were determined by LC-MS/MS technique. Comparative analysis of transcriptomic and proteomic data revealed solid correlation (r2 = 0.4) considering the role of Hfq in post-transcriptional control of gene expression. Importantly, our study confirms and further enlightens the role of Hfq in pathogenicity of B. pertussis as it shows that Δhfq strain displays strongly impaired secretion of substrates of Type III secretion system (T3SS) and substantially reduced resistance to serum killing. On the other hand, significantly increased production of proteins implicated in transport of important metabolites and essential nutrients observed in the mutant seems to compensate for the physiological defect introduced by the deletion of the hfq gene.
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Mattoo S., Cherry J.D. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to bordetella pertussis and other bordetella subspecies. Clin. Microbiol. Rev. 2005;18:326–382. doi: 10.1128/CMR.18.2.326-382.2005. PubMed DOI PMC
World Health Organization (WHO) Vaccine preventable deaths and the global immunization vision and strategy, 2006–2015. MMWR Morb. Mortal. Wkly. Rep. 2006;55:511–515. PubMed
Raguckas S.E., VandenBussche H.L., Jacobs C., Klepser M.E. Pertussis resurgence: Diagnosis, treatment, prevention, and beyond. Pharmacotherapy. 2007;27:41–52. doi: 10.1592/phco.27.1.41. PubMed DOI
Cherry J.D. The present and future control of pertussis. Clin. Infect. Dis. 2010;51:663–667. doi: 10.1086/655826. PubMed DOI
Cherry J.D. Pertussis: Challenges today and for the future. PLoS Pathog. 2013;9:e1003418. doi: 10.1371/journal.ppat.1003418. PubMed DOI PMC
Mooi F.R., Van Der Maas N.A., De Melker H.E. Pertussis resurgence: Waning immunity and pathogen adaptation—Two sides of the same coin. Epidemiol. Infect. 2014;142:685–694. doi: 10.1017/S0950268813000071. PubMed DOI PMC
Sealey K.L., Belcher T., Preston A. Bordetella pertussis epidemiology and evolution in the light of pertussis resurgence. Infect. Genet. Evol. 2016;40:136–143. doi: 10.1016/j.meegid.2016.02.032. PubMed DOI
Burdin N., Handy L.K., Plotkin S.A. What is wrong with pertussis vaccine immunity? The problem of waning effectiveness of pertussis vaccines. Cold Spring Harb. Perspect. Biol. 2017;9 doi: 10.1101/cshperspect.a029454. PubMed DOI PMC
Hewlett E.L., Burns D.L., Cotter P.A., Harvill E.T., Merkel T.J., Quinn C.P., Stibitz E.S. Pertussis pathogenesis—What we know and what we don’t know. J. Infect. Dis. 2014;209:982–985. doi: 10.1093/infdis/jit639. PubMed DOI PMC
The Periscope Consortium Periscope: Road towards effective control of pertussis. Lancet Infect. Dis. 2019;19:179–186. doi: 10.1016/S1473-3099(18)30646-7. PubMed DOI
Chao Y., Vogel J. The role of hfq in bacterial pathogens. Curr. Opin. Microbiol. 2010;13:24–33. doi: 10.1016/j.mib.2010.01.001. PubMed DOI
Feliciano J.R., Grilo A.M., Guerreiro S.I., Sousa S.A., Leitao J.H. Hfq: A multifaceted rna chaperone involved in virulence. Fut. Microbiol. 2016;11:137–151. doi: 10.2217/fmb.15.128. PubMed DOI
Papenfort K., Vogel J. Regulatory rna in bacterial pathogens. Cell Host Microbe. 2010;8:116–127. doi: 10.1016/j.chom.2010.06.008. PubMed DOI
Vogel J., Luisi B.F. Hfq and its constellation of rna. Nat. Rev. Microbiol. 2011;9:578–589. doi: 10.1038/nrmicro2615. PubMed DOI PMC
Vecerek B., Rajkowitsch L., Sonnleitner E., Schroeder R., Blasi U. The c-terminal domain of escherichia coli hfq is required for regulation. Nucleic Acids Res. 2008;36:133–143. doi: 10.1093/nar/gkm985. PubMed DOI PMC
Updegrove T.B., Zhang A., Storz G. Hfq: The flexible rna matchmaker. Curr. Opin. Microbiol. 2016;30:133–138. doi: 10.1016/j.mib.2016.02.003. PubMed DOI PMC
Brennan R.G., Link T.M. Hfq structure, function and ligand binding. Curr. Opin. Microbiol. 2007;10:125–133. doi: 10.1016/j.mib.2007.03.015. PubMed DOI
Bibova I., Skopova K., Masin J., Cerny O., Hot D., Sebo P., Vecerek B. The rna chaperone hfq is required for virulence of bordetella pertussis. Infect. Immun. 2013;81:4081–4090. doi: 10.1128/IAI.00345-13. PubMed DOI PMC
Bibova I., Hot D., Keidel K., Amman F., Slupek S., Cerny O., Gross R., Vecerek B. Transcriptional profiling of bordetella pertussis reveals requirement of rna chaperone hfq for type iii secretion system functionality. RNA Biol. 2015;12:175–185. doi: 10.1080/15476286.2015.1017237. PubMed DOI PMC
de Sousa Abreu R., Penalva L.O., Marcotte E.M., Vogel C. Global signatures of protein and mrna expression levels. Mol. Biosyst. 2009;5:1512–1526. doi: 10.1039/b908315d. PubMed DOI PMC
Kumar D., Bansal G., Narang A., Basak T., Abbas T., Dash D. Integrating transcriptome and proteome profiling: Strategies and applications. Proteomics. 2016;16:2533–2544. doi: 10.1002/pmic.201600140. PubMed DOI
Gygi S.P., Rochon Y., Franza B.R., Aebersold R. Correlation between protein and mrna abundance in yeast. Mol. Cell Biol. 1999;19:1720–1730. doi: 10.1128/MCB.19.3.1720. PubMed DOI PMC
Greenbaum D., Colangelo C., Williams K., Gerstein M. Comparing protein abundance and mrna expression levels on a genomic scale. Genome Biol. 2003;4:117. doi: 10.1186/gb-2003-4-9-117. PubMed DOI PMC
Ghazalpour A., Bennett B., Petyuk V.A., Orozco L., Hagopian R., Mungrue I.N., Farber C.R., Sinsheimer J., Kang H.M., Furlotte N., et al. Comparative analysis of proteome and transcriptome variation in mouse. PLoS Genet. 2011;7:e1001393. doi: 10.1371/journal.pgen.1001393. PubMed DOI PMC
Maier T., Guell M., Serrano L. Correlation of mrna and protein in complex biological samples. FEBS Lett. 2009;583:3966–3973. doi: 10.1016/j.febslet.2009.10.036. PubMed DOI
Manzoni C., Kia D.A., Vandrovcova J., Hardy J., Wood N.W., Lewis P.A., Ferrari R. Genome, transcriptome and proteome: The rise of omics data and their integration in biomedical sciences. Brief Bioinform. 2018;19:286–302. doi: 10.1093/bib/bbw114. PubMed DOI PMC
Nie L., Wu G., Zhang W. Correlation of mrna expression and protein abundance affected by multiple sequence features related to translational efficiency in desulfovibrio vulgaris: A quantitative analysis. Genetics. 2006;174:2229–2243. doi: 10.1534/genetics.106.065862. PubMed DOI PMC
Arraiano C.M., Andrade J.M., Domingues S., Guinote I.B., Malecki M., Matos R.G., Moreira R.N., Pobre V., Reis F.P., Saramago M., et al. The critical role of rna processing and degradation in the control of gene expression. FEMS Microbiol. Rev. 2010;34:883–923. doi: 10.1111/j.1574-6976.2010.00242.x. PubMed DOI
Kudla G., Murray A.W., Tollervey D., Plotkin J.B. Coding-sequence determinants of gene expression in escherichia coli. Science. 2009;324:255–258. doi: 10.1126/science.1170160. PubMed DOI PMC
Grenga L., Chandra G., Saalbach G., Galmozzi C.V., Kramer G., Malone J.G. Analyzing the complex regulatory landscape of hfq—An integrative, multi-omics approach. Front. Microbiol. 2017;8:1784. doi: 10.3389/fmicb.2017.01784. PubMed DOI PMC
Delgado-Ortega M., Marc D., Dupont J., Trapp S., Berri M., Meurens F. Socs proteins in infectious diseases of mammals. Vet. Immunol. Immunopathol. 2013;151:1–19. doi: 10.1016/j.vetimm.2012.11.008. PubMed DOI PMC
Marr N., Shah N.R., Lee R., Kim E.J., Fernandez R.C. Bordetella pertussis autotransporter vag8 binds human c1 esterase inhibitor and confers serum resistance. PLoS ONE. 2011;6:e20585. doi: 10.1371/journal.pone.0020585. PubMed DOI PMC
Hovingh E.S., van den Broek B., Kuipers B., Pinelli E., Rooijakkers S.H.M., Jongerius I. Acquisition of c1 inhibitor by bordetella pertussis virulence associated gene 8 results in c2 and c4 consumption away from the bacterial surface. PLoS Pathog. 2017;13:e1006531. doi: 10.1371/journal.ppat.1006531. PubMed DOI PMC
Brookes C., Freire-Martin I., Cavell B., Alexander F., Taylor S., Persaud R., Fry N., Preston A., Diavatopoulos D., Gorringe A. Bordetella pertussis isolates vary in their interactions with human complement components. Emerg. Microbes Infect. 2018;7:81. doi: 10.1038/s41426-018-0084-3. PubMed DOI PMC
Marioni J.C., Mason C.E., Mane S.M., Stephens M., Gilad Y. Rna-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 2008;18:1509–1517. doi: 10.1101/gr.079558.108. PubMed DOI PMC
Zhao S., Fung-Leung W.P., Bittner A., Ngo K., Liu X. Comparison of rna-seq and microarray in transcriptome profiling of activated t cells. PLoS ONE. 2014;9:e78644. doi: 10.1371/journal.pone.0078644. PubMed DOI PMC
Basler M., Linhartova I., Halada P., Novotna J., Bezouskova S., Osicka R., Weiser J., Vohradsky J., Sebo P. The iron-regulated transcriptome and proteome of neisseria meningitidis serogroup c. Proteomics. 2006;6:6194–6206. doi: 10.1002/pmic.200600312. PubMed DOI
Yuk M.H., Harvill E.T., Miller J.F. The bvgas virulence control system regulates type iii secretion in bordetella bronchiseptica. Mol. Microbiol. 1998;28:945–959. doi: 10.1046/j.1365-2958.1998.00850.x. PubMed DOI
Ahuja U., Shokeen B., Cheng N., Cho Y., Blum C., Coppola G., Miller J.F. Differential regulation of type iii secretion and virulence genes in bordetella pertussis and bordetella bronchiseptica by a secreted anti-sigma factor. Proc. Natl. Acad. Sci. USA. 2016;113:2341–2348. doi: 10.1073/pnas.1600320113. PubMed DOI PMC
Mattoo S., Yuk M.H., Huang L.L., Miller J.F. Regulation of type iii secretion in bordetella. Mol. Microbiol. 2004;52:1201–1214. doi: 10.1111/j.1365-2958.2004.04053.x. PubMed DOI
Kurushima J., Kuwae A., Abe A. The type iii secreted protein bspr regulates the virulence genes in bordetella bronchiseptica. PLoS ONE. 2012;7:e38925. doi: 10.1371/journal.pone.0038925. PubMed DOI PMC
Fennelly N.K., Sisti F., Higgins S.C., Ross P.J., van der Heide H., Mooi F.R., Boyd A., Mills K.H. Bordetella pertussis expresses a functional type iii secretion system that subverts protective innate and adaptive immune responses. Infect. Immun. 2008;76:1257–1266. doi: 10.1128/IAI.00836-07. PubMed DOI PMC
Gaillard M.E., Bottero D., Castuma C.E., Basile L.A., Hozbor D. Laboratory adaptation of bordetella pertussis is associated with the loss of type three secretion system functionality. Infect. Immun. 2011;79:3677–3682. doi: 10.1128/IAI.00136-11. PubMed DOI PMC
Brickman T.J., Cummings C.A., Liew S.Y., Relman D.A., Armstrong S.K. Transcriptional profiling of the iron starvation response in bordetella pertussis provides new insights into siderophore utilization and virulence gene expression. J. Bacteriol. 2011;193:4798–4812. doi: 10.1128/JB.05136-11. PubMed DOI PMC
Hanawa T., Kamachi K., Yonezawa H., Fukutomi T., Kawakami H., Kamiya S. Glutamate limitation, bvgas activation, and (p)ppgpp regulate the expression of the bordetella pertussis type 3 secretion system. J. Bacteriol. 2016;198:343–351. doi: 10.1128/JB.00596-15. PubMed DOI PMC
Fantappie L., Metruccio M.M., Seib K.L., Oriente F., Cartocci E., Ferlicca F., Giuliani M.M., Scarlato V., Delany I. The rna chaperone hfq is involved in stress response and virulence in neisseria meningitidis and is a pleiotropic regulator of protein expression. Infect. Immun. 2009;77:1842–1853. doi: 10.1128/IAI.01216-08. PubMed DOI PMC
Barnes M.G., Weiss A.A. Brka protein of bordetella pertussis inhibits the classical pathway of complement after c1 deposition. Infect. Immun. 2001;69:3067–3072. doi: 10.1128/IAI.69.5.3067-3072.2001. PubMed DOI PMC
Berggard K., Johnsson E., Mooi F.R., Lindahl G. Bordetella pertussis binds the human complement regulator c4bp: Role of filamentous hemagglutinin. Infect. Immun. 1997;65:3638–3643. PubMed PMC
Noofeli M., Bokhari H., Blackburn P., Roberts M., Coote J.G., Parton R. Bapc autotransporter protein is a virulence determinant of bordetella pertussis. Microb. Pathog. 2011;51:169–177. doi: 10.1016/j.micpath.2011.04.004. PubMed DOI
Rosa L.T., Bianconi M.E., Thomas G.H., Kelly D.J. Tripartite atp-independent periplasmic (trap) transporters and tripartite tricarboxylate transporters (ttt): From uptake to pathogenicity. Front. Cell Infect. Microbiol. 2018;8:33. doi: 10.3389/fcimb.2018.00033. PubMed DOI PMC
Antoine R., Jacob-Dubuisson F., Drobecq H., Willery E., Lesjean S., Locht C. Overrepresentation of a gene family encoding extracytoplasmic solute receptors in bordetella. J. Bacteriol. 2003;185:1470–1474. doi: 10.1128/JB.185.4.1470-1474.2003. PubMed DOI PMC
Huvent I., Belrhali H., Antoine R., Bompard C., Locht C., Jacob-Dubuisson F., Villeret V. Crystal structure of bordetella pertussis bugd solute receptor unveils the basis of ligand binding in a new family of periplasmic binding proteins. J. Mol. Biol. 2006;356:1014–1026. doi: 10.1016/j.jmb.2005.11.096. PubMed DOI
Huvent I., Belrhali H., Antoine R., Bompard C., Locht C., Jacob-Dubuisson F., Villeret V. Structural analysis of bordetella pertussis buge solute receptor in a bound conformation. Acta Crystallogr. D Biol. Crystallogr. 2006;62:1375–1381. doi: 10.1107/S0907444906032653. PubMed DOI
Carbonetti N.H. Contribution of pertussis toxin to the pathogenesis of pertussis disease. Pathog. Dis. 2015;73:ftv073. doi: 10.1093/femspd/ftv073. PubMed DOI PMC
Brown L., Elliott T. Efficient translation of the rpos sigma factor in salmonella typhimurium requires host factor i, an rna-binding protein encoded by the hfq gene. J. Bacteriol. 1996;178:3763–3770. doi: 10.1128/jb.178.13.3763-3770.1996. PubMed DOI PMC
Muffler A., Fischer D., Hengge-Aronis R. The rna-binding protein hf-i, known as a host factor for phage qbeta rna replication, is essential for rpos translation in escherichia coli. Genes Dev. 1996;10:1143–1151. doi: 10.1101/gad.10.9.1143. PubMed DOI
Ding Y., Davis B.M., Waldor M.K. Hfq is essential for vibrio cholerae virulence and downregulates sigma expression. Mol. Microbiol. 2004;53:345–354. doi: 10.1111/j.1365-2958.2004.04142.x. PubMed DOI
Figueroa-Bossi N., Lemire S., Maloriol D., Balbontin R., Casadesus J., Bossi L. Loss of hfq activates the sigmae-dependent envelope stress response in salmonella enterica. Mol. Microbiol. 2006;62:838–852. doi: 10.1111/j.1365-2958.2006.05413.x. PubMed DOI
Keidel K., Amman F., Bibova I., Drzmisek J., Benes V., Hot D., Vecerek B. Signal transduction-dependent small regulatory rna is involved in glutamate metabolism of the human pathogen bordetella pertussis. RNA. 2018;24:1530–1541. doi: 10.1261/rna.067306.118. PubMed DOI PMC
Amman F., D’Halluin A., Antoine R., Huot L., Bibova I., Keidel K., Slupek S., Bouquet P., Coutte L., Caboche S., et al. Primary transcriptome analysis reveals importance of is elements for the shaping of the transcriptional landscape of bordetella pertussis. RNA Biol. 2018;15:967–975. doi: 10.1080/15476286.2018.1462655. PubMed DOI PMC
Kasuga T., Nakase Y., Ukishima K., Takatsu K. Studies on haemophilis pertussis. Iii. Some properties of each phase of h. Pertussis. Kitasato Arch. Exp. Med. 1954;27:37–47. PubMed
Stainer D.W., Scholte M.J. A simple chemically defined medium for the production of phase i bordetella pertussis. J. Gen. Microbiol. 1970;63:211–220. doi: 10.1099/00221287-63-2-211. PubMed DOI
Bolger A.M., Lohse M., Usadel B. Trimmomatic: A flexible trimmer for illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC
Hoffmann S., Otto C., Kurtz S., Sharma C.M., Khaitovich P., Vogel J., Stadler P.F., Hackermuller J. Fast mapping of short sequences with mismatches, insertions and deletions using index structures. PLoS Comput. Biol. 2009;5:e1000502. doi: 10.1371/journal.pcbi.1000502. PubMed DOI PMC
Anders S., Pyl P.T., Huber W. Htseq—A python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31:166–169. doi: 10.1093/bioinformatics/btu638. PubMed DOI PMC
Love M.I., Huber W., Anders S. Moderated estimation of fold change and dispersion for rna-seq data with deseq2. Genome Biol. 2014;15:550. doi: 10.1186/s13059-014-0550-8. PubMed DOI PMC
Benjamini Y., Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. B. 1995;57:289–300. doi: 10.1111/j.2517-6161.1995.tb02031.x. DOI
Masuda T., Tomita M., Ishihama Y. Phase transfer surfactant-aided trypsin digestion for membrane proteome analysis. J. Proteome Res. 2008;7:731–740. doi: 10.1021/pr700658q. PubMed DOI
Hebert A.S., Richards A.L., Bailey D.J., Ulbrich A., Coughlin E.E., Westphall M.S., Coon J.J. The one hour yeast proteome. Mol. Cell Proteom. 2014;13:339–347. doi: 10.1074/mcp.M113.034769. PubMed DOI PMC
Cox J., Mann M. Maxquant enables high peptide identification rates, individualized p.P.B.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008;26:1367–1372. doi: 10.1038/nbt.1511. PubMed DOI
Cox J., Neuhauser N., Michalski A., Scheltema R.A., Olsen J.V., Mann M. Andromeda: A peptide search engine integrated into the maxquant environment. J. Proteome Res. 2011;10:1794–1805. doi: 10.1021/pr101065j. PubMed DOI
Cox J., Hein M.Y., Luber C.A., Paron I., Nagaraj N., Mann M. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed maxlfq. Mol. Cell Proteom. 2014;13:2513–2526. doi: 10.1074/mcp.M113.031591. PubMed DOI PMC
Tyanova S., Temu T., Sinitcyn P., Carlson A., Hein M.Y., Geiger T., Mann M., Cox J. The perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods. 2016;13:731–740. doi: 10.1038/nmeth.3901. PubMed DOI
Perez-Riverol Y., Csordas A., Bai J., Bernal-Llinares M., Hewapathirana S., Kundu D.J., Inuganti A., Griss J., Mayer G., Eisenacher M., et al. The pride database and related tools and resources in 2019: Improving support for quantification data. Nucleic Acids Res. 2019;47:D442–D450. doi: 10.1093/nar/gky1106. PubMed DOI PMC
Conesa A., Gotz S., Garcia-Gomez J.M., Terol J., Talon M., Robles M. Blast2go: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21:3674–3676. doi: 10.1093/bioinformatics/bti610. PubMed DOI
Supek F., Bosnjak M., Skunca N., Smuc T. Revigo summarizes and visualizes long lists of gene ontology terms. PLoS ONE. 2011;6:e21800. doi: 10.1371/journal.pone.0021800. PubMed DOI PMC
Bordetella Type III Secretion Injectosome and Effector Proteins