Skip to main content

Transcriptional and Post-transcriptional Regulatory Mechanisms Controlling Type III Secretion

  • Chapter
  • First Online:
Bacterial Type III Protein Secretion Systems

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 427))

Abstract

Type III secretion systems (T3SSs) are utilized by numerous Gram-negative bacteria to efficiently interact with host cells and manipulate their function. Appropriate expression of type III secretion genes is achieved through the integration of multiple control elements and regulatory pathways that ultimately coordinate the activity of a central transcriptional activator usually belonging to the AraC/XylS family. Although several regulatory elements are conserved between different species and families, each pathogen uses a unique set of control factors and mechanisms to adjust and optimize T3SS gene expression to the need and lifestyle of the pathogen. This is reflected by the complex set of sensory systems and diverse transcriptional, post-transcriptional and post-translational control strategies modulating T3SS expression in response to environmental and intrinsic cues. Whereas some pathways regulate solely the T3SS, others coordinately control expression of one or multiple T3SSs together with other virulence factors and fitness traits on a global scale. Over the past years, several common regulatory themes emerged, e.g., environmental control by two-component systems and carbon metabolism regulators or coupling of T3SS induction with host cell contact/translocon-effector secretion. One of the remaining challenges is to resolve the understudied post-transcriptional regulation of T3SS and the dynamics of the control process.

Marcel Volk and Ines Vollmer contributed equally

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 139.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ahuja U, Shokeen B, Cheng N, Cho Y, Blum C, Coppola G et al (2016) 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 113(9):2341–2348. https://doi.org/10.1073/pnas.1600320113. PubMed PMID: 26884180; PubMed Central PMCID: PMCPMC4780644

  • Altier C, Suyemoto M, Lawhon SD (2000) Regulation of Salmonella enterica serovar typhimurium invasion genes by csrA. Infect Immun 68(12):6790–6797. PubMed PMID: 11083797

    Google Scholar 

  • Anderson DM, Schneewind O (1999) Yersinia enterocolitica type III secretion: an mRNA signal that couples translation and secretion of YopQ. Mol Microbiol 31(4):1139–1148. PubMed PMID: 10096081

    Google Scholar 

  • Anderson DM, Ramamurthi KS, Tam C, Schneewind O (2002) YopD and LcrH regulate expression of Yersinia enterocolitica YopQ by a posttranscriptional mechanism and bind to yopQ RNA. J Bacteriol 184(5):1287–1295. PubMed PMID: 11844757; PubMed Central PMCID: PMC134855

    Google Scholar 

  • Bent ZW, Poorey K, Brazel DM, LaBauve AE, Sinha A, Curtis DJ et al (2015) Transcriptomic analysis of Yersinia enterocolitica Biovar 1B infecting murine macrophages reveals new mechanisms of extracellular and intracellular survival. Infect Immun 83(7):2672–2685. https://doi.org/10.1128/iai.02922-14. PubMed PMID: 25895974; PubMed Central PMCID: PMCPMC4468540

  • Bhatt S, Edwards AN, Nguyen HT, Merlin D, Romeo T, Kalman D (2009) The RNA binding protein CsrA is a pleiotropic regulator of the locus of enterocyte effacement pathogenicity island of enteropathogenic Escherichia coli. Infect Immun 77(9):3552–3568. https://doi.org/10.1128/iai.00418-09. PubMed PMID: 19581394; PubMed Central PMCID: PMCPMC2737987

  • Bhatt S, Egan M, Jenkins V, Muche S, El-Fenej J (2016) The Tip of the iceberg: on the roles of regulatory small RNAs in the virulence of enterohemorrhagic and enteropathogenic Escherichia coli. Front Cell Infect Microbiol 6:105. https://doi.org/10.3389/fcimb.2016.00105. PubMed PMID: 27709103; PubMed Central PMCID: PMCPMC5030294

  • Böhme K, Steinmann R, Kortmann J, Seekircher S, Heroven AK, Berger E et al (2012) Concerted actions of a thermo-labile regulator and a unique intergenic RNA thermosensor control Yersinia virulence. PLoS Pathog 8(2):e1002518. Epub 2012/02/24. https://doi.org/10.1371/journal.ppat.1002518. PubMed PMID: 22359501; PubMed Central PMCID: PMC3280987

  • Brutinel ED, Yahr TL (2008) Control of gene expression by type III secretory activity. Curr Opin Microbiol 11(2):128–133. https://doi.org/10.1016/j.mib.2008.02.010. Epub 2008/04/09. doi:S1369-5274(08)00021-0 [pii]. PubMed PMID: 18396449; PubMed Central PMCID: PMC2387186

  • Brutinel ED, Vakulskas CA, Yahr TL (2010) ExsD inhibits expression of the Pseudomonas aeruginosa type III secretion system by disrupting ExsA self-association and DNA binding activity. J Bacteriol 192(6):1479–1486. https://doi.org/10.1128/jb.01457-09. PubMed PMID: 20008065; PubMed Central PMCID: PMC2832532

  • Bustos SA, Schleif RF (1993) Functional domains of the AraC protein. Proc Natl Acad Sci USA 90(12):5638–5642. PubMed PMID: 8516313; PubMed Central PMCID: PMCPMC46776

    Google Scholar 

  • Büttner D (2012) Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol Mol Biol Rev 76(2):262–310. https://doi.org/10.1128/mmbr.05017-11. PubMed PMID: 22688814; PubMed Central PMCID: PMCPMC3372255

  • Cambronne ED, Schneewind O (2002) Yersinia enterocolitica type III secretion: yscM1 and yscM2 regulate yop gene expression by a posttranscriptional mechanism that targets the 5′ untranslated region of yop mRNA. J Bacteriol 184(21):5880–5893. PubMed PMID: 12374821; PubMed Central PMCID: PMC135404

    Google Scholar 

  • Chakravarty S, Melton CN, Bailin A, Yahr TL, Anderson GG (2017) Pseudomonas aeruginosa magnesium transporter MgtE inhibits type III secretion system gene expression by stimulating rsmYZ transcription. J Bacteriol 199(23). https://doi.org/10.1128/jb.00268-17. PubMed PMID: 28847924; PubMed Central PMCID: PMCPMC5686585

  • Chao Y, Papenfort K, Reinhardt R, Sharma CM, Vogel J (2012) An atlas of Hfq-bound transcripts reveals 3’ UTRs as a genomic reservoir of regulatory small RNAs. EMBO J 31(20):4005–4019. https://doi.org/10.1038/emboj.2012.229. PubMed PMID: 22922465; PubMed Central PMCID: PMCPMC3474919

  • Chen Y, Anderson DM (2011) Expression hierarchy in the Yersinia type III secretion system established through YopD recognition of RNA. Mol Microbiol 80(4):966–980. https://doi.org/10.1111/j.1365-2958.2011.07623.x. Epub 2011/04/13. PubMed PMID: 21481017

  • Chevance FF, Hughes KT (2017) Coupling of flagellar gene expression with assembly in Salmonella enterica. Methods Mol Biol 1593:47–71. https://doi.org/10.1007/978-1-4939-6927-2_4. PubMed PMID: 28389944

  • Choi SM, Jeong JH, Choy HE, Shin M (2016)Amino acid residues in the Ler protein critical for derepression of the LEE5 promoter in enteropathogenic E. coli. J Microbiol 54(8):559–564. https://doi.org/10.1007/s12275-016-6027-6. PubMed PMID: 27480636

  • Dasgupta N, Lykken GL, Wolfgang MC, Yahr TL (2004) A novel anti-anti-activator mechanism regulates expression of the Pseudomonas aeruginosa type III secretion system. Mol Microbiol 53(1):297–308. https://doi.org/10.1111/j.1365-2958.2004.04128.x. PubMed PMID: 15225323

  • Dasgupta N, Ashare A, Hunninghake GW, Yahr TL (2006) Transcriptional induction of the Pseudomonas aeruginosa type III secretion system by low Ca2+ and host cell contact proceeds through two distinct signaling pathways. Infect Immun 74(6):3334–3341. https://doi.org/10.1128/iai.00090-06. PubMed PMID: 16714561; PubMed Central PMCID: PMCPMC1479281

  • Deng W, Marshall NC, Rowland JL, McCoy JM, Worrall LJ, Santos AS et al (2017) Assembly, structure, function and regulation of type III secretion systems. Nat Rev Microbiol 15(6):323–337. https://doi.org/10.1038/nrmicro.2017.20. PubMed PMID: 28392566

  • Diepold A, Wagner S (2014) Assembly of the bacterial type III secretion machinery. FEMS Microbiol Rev 38(4):802–822. https://doi.org/10.1111/1574-6976.12061. PubMed PMID: 24484471

  • Dorman CJ (2007) H-NS, the genome sentinel. Nat Rev Microbiol 5(2):157–161. https://doi.org/10.1038/nrmicro1598. Epub 2006/12/28. doi:nrmicro1598 [pii]. PubMed PMID: 17191074

  • Dubey AK, Baker CS, Romeo T, Babitzke P (2005) RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. RNA 11(10):1579–1587. https://doi.org/10.1261/rna.2990205. PubMed PMID: 16131593; PubMed Central PMCID: PMCPMC1370842

  • Ellermeier JR, Slauch JM (2007) Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr Opin Microbiol 10(1):24–29. https://doi.org/10.1016/j.mib.2006.12.002. PubMed PMID: 17208038

  • Ellermeier JR, Slauch JM (2008) Fur regulates expression of the Salmonella pathogenicity island 1 type III secretion system through HilD. J Bacteriol 190(2):476–486. https://doi.org/10.1128/jb.00926-07. PubMed PMID: 17993530; PubMed Central PMCID: PMC2223717

  • Ellermeier CD, Ellermeier JR, Slauch JM (2005) HilD, HilC and RtsA constitute a feed forward loop that controls expression of the SPI1 type three secretion system regulator hilA in Salmonella enterica serovar Typhimurium. Mol Microbiol 57(3):691–705. https://doi.org/10.1111/j.1365-2958.2005.04737.x. PubMed PMID: 16045614

  • Erhardt M, Dersch P (2015) Regulatory principles governing Salmonella and Yersinia virulence. Front Microbiol 6:949. https://doi.org/10.3389/fmicb.2015.00949. PubMed PMID: 26441883; PubMed Central PMCID: PMCPMC4563271

  • Francis MS, Wolf-Watz H, Forsberg A (2002) Regulation of type III secretion systems. Curr Opin Microbiol 5(2):166–172. PubMed PMID: 11934613

    Google Scholar 

  • Galan JE, Lara-Tejero M, Marlovits TC, Wagner S (2014) Bacterial type III secretion systems: specialized nanomachines for protein delivery into target cells. Annu Rev Microbiol 68:415–438. https://doi.org/10.1146/annurev-micro-092412-155725. PubMed PMID: 25002086; PubMed Central PMCID: PMCPMC4388319

  • Golubeva YA, Ellermeier JR, Cott Chubiz JE, Slauch JM (2016). Intestinal long-chain fatty acids act as a direct signal to modulate expression of the Salmonella Pathogenicity Island 1 type III secretion system. MBio 7(1):e02170–e02175. https://doi.org/10.1128/mbio.02170-15. PubMed PMID: 26884427; PubMed Central PMCID: PMCPMC4752608

  • Görke B, Stülke J (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6(8):613–624. https://doi.org/10.1038/nrmicro1932. PubMed PMID: 18628769

  • Gruber CC, Sperandio V (2014) Posttranscriptional control of microbe-induced rearrangement of host cell actin. MBio 5(1):e01025-13. https://doi.org/10.1128/mbio.01025-13. PubMed PMID: 24425733; PubMed Central PMCID: PMCPMC3903284

  • Gruber CC, Sperandio V (2015) Global analysis of posttranscriptional regulation by GlmY and GlmZ in enterohemorrhagic Escherichia coli O157:H7. Infect Immun 83(4):1286–1295. https://doi.org/10.1128/iai.02918-14. PubMed PMID: 25605763; PubMed Central PMCID: PMCPMC4363437

  • Heroven A, Bohme K, Rohde M, Dersch P (2008) A Csr-type regulatory system, including small non-coding RNAs, regulates the global virulence regulator RovA of Yersinia pseudotuberculosis through RovM. Mol Microbiol 68(5):1179–1195. https://doi.org/10.1111/j.1365-2958.2008.06218.x. Epub 2008/04/24. doi:MMI6218 [pii] . PubMed PMID: 18430141

  • Hoe NP, Goguen JD (1993) Temperature sensing in Yersinia pestis: translation of the LcrF activator protein is thermally regulated. J Bacteriol 175(24):7901–7909. PubMed PMID: 7504666

    Google Scholar 

  • Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62(2):379–433

    Google Scholar 

  • Intile PJ, Diaz MR, Urbanowski ML, Wolfgang MC, Yahr TL (2014) The AlgZR two-component system recalibrates the RsmAYZ posttranscriptional regulatory system to inhibit expression of the Pseudomonas aeruginosa type III secretion system. J Bacteriol 196(2):357–366. https://doi.org/10.1128/jb.01199-13. PubMed PMID: 24187093; PubMed Central PMCID: PMCPMC3911257

  • Intile PJ, Balzer GJ, Wolfgang MC, Yahr TL (2015) The RNA Helicase DeaD stimulates ExsA translation to promote expression of the Pseudomonas aeruginosa type III secretion system. J Bacteriol 197(16):2664–2674. https://doi.org/10.1128/jb.00231-15. PubMed PMID: 26055113; PubMed Central PMCID: PMCPMC4507347

  • Jackson M, Silva-Herzog E, Plano GV (2004) The ATP-dependent ClpXP and Lon proteases regulate expression of the Yersinia pestis type III secretion system via regulated proteolysis of YmoA, a small histone-like protein. Mol Microbiol 54(5):1364–1378. https://doi.org/10.1111/j.1365-2958.2004.04353.x. Epub 2004/11/24. doi:MMI4353 [pii]. PubMed PMID: 15554975

  • Kakoschke T, Kakoschke S, Magistro G, Schubert S, Borath M, Heesemann J et al (2014) The RNA chaperone Hfq impacts growth, metabolism and production of virulence factors in Yersinia enterocolitica. PLoS One 9(1):e86113. https://doi.org/10.1371/journal.pone.0086113. PubMed PMID: 24454955; PubMed Central PMCID: PMCPMC3893282

  • Kakoschke TK, Kakoschke SC, Zeuzem C, Bouabe H, Adler K, Heesemann J et al (2016) The RNA chaperone Hfq is essential for virulence and modulates the expression of four adhesins in Yersinia enterocolitica. Sci Rep 6:29275. https://doi.org/10.1038/srep29275. PubMed PMID: 27387855; PubMed Central PMCID: PMCPMC4937351

  • Katsowich N, Elbaz N, Pal RR, Mills E, Kobi S, Kahan T et al (2017) Host cell attachment elicits posttranscriptional regulation in infecting enteropathogenic bacteria. Science 355(6326):735–739. https://doi.org/10.1126/science.aah4886. PubMed PMID: 28209897

  • King JM, Schesser Bartra S, Plano G, Yahr TL (2013) ExsA and LcrF recognize similar consensus binding sites, but differences in their oligomeric state influence interactions with promoter DNA. J Bacteriol 195(24):5639–5650. https://doi.org/10.1128/jb.00990-13. PubMed PMID: 24142246; PubMed Central PMCID: PMC3889609

  • Kopaskie KS, Ligtenberg KG, Schneewind O (2013) Translational regulation of Yersinia enterocolitica mRNA encoding a type III secretion substrate. J Biol Chem 288(49):35478–35488. https://doi.org/10.1074/jbc.m113.504811. PubMed PMID: 24158443; PubMed Central PMCID: PMC3853294

  • Kusmierek M, Dersch P (2017) Regulation of host-pathogen interactions via the post-transcriptional Csr/Rsm system. Curr Opin Microbiol 41:58–67. https://doi.org/10.1016/j.mib.2017.11.022. PubMed PMID: 29207313

  • Laaberki MH, Janabi N, Oswald E, Repoila F (2006) Concert of regulators to switch on LEE expression in enterohemorrhagic Escherichia coli O157:H7: interplay between Ler, GrlA, HNS and RpoS. Int J Med Microbiol 296(4–5):197–210. https://doi.org/10.1016/j.ijmm.2006.02.017. PubMed PMID: 16618552

  • Lapouge K, Perozzo R, Iwaszkiewicz J, Bertelli C, Zoete V, Michielin O et al (2013) RNA pentaloop structures as effective targets of regulators belonging to the RsmA/CsrA protein family. RNA Biol 10(6):1031–1041. https://doi.org/10.4161/rna.24771. PubMed PMID: 23635605; PubMed Central PMCID: PMCPMC4111731

  • Leskinen K, Varjosalo M, Skurnik M (2015) Absence of YbeY RNase compromises the growth and enhances the virulence plasmid gene expression of Yersinia enterocolitica O:3. Microbiology 161(Pt 2):285–299. https://doi.org/10.1099/mic.0.083097-0. PubMed PMID: 25416689

  • Li L, Yan H, Feng L, Li Y, Lu P, Hu Y et al (2014) LcrQ blocks the role of LcrF in regulating the Ysc-Yop type III secretion genes in Yersinia pseudotuberculosis. PLoS One 9(3):e92243. https://doi.org/10.1371/journal.pone.0092243. PubMed PMID: 24658611; PubMed Central PMCID: PMCPMC3962397

  • Lodato PB, Hsieh PK, Belasco JG, Kaper JB (2012) The ribosome binding site of a mini-ORF protects a T3SS mRNA from degradation by RNase E. Mol Microbiol 86(5):1167–1182. https://doi.org/10.1111/mmi.12050. PubMed PMID: 23043360; PubMed Central PMCID: PMCPMC3537511

  • Lodato PB, Thuraisamy T, Richards J, Belasco JG (2017) Effect of RNase E deficiency on translocon protein synthesis in an RNase E-inducible strain of enterohemorrhagic Escherichia coli O157:H7. FEMS Microbiol Lett 364(13). https://doi.org/10.1093/femsle/fnx131. PubMed PMID: 28854682

  • Lopez-Garrido J, Puerta-Fernandez E, Casadesus J (2014) A eukaryotic-like 3’ untranslated region in Salmonella enterica hilD mRNA. Nucleic Acids Res 42(9):5894–5906. https://doi.org/10.1093/nar/gku222. PubMed PMID: 24682814; PubMed Central PMCID: PMC4027200

  • Madrid C, Nieto JM, Juarez A (2002) Role of the Hha/YmoA family of proteins in the thermoregulation of the expression of virulence factors. Int J Med Microbiol 291(6–7):425–432. PubMed PMID: 11890540

    Google Scholar 

  • Madrid C, Balsalobre C, Garcia J, Juarez A (2007) The novel Hha/YmoA family of nucleoid-associated proteins: use of structural mimicry to modulate the activity of the H-NS family of proteins. Mol Microbiol 63(1):7–14. PubMed PMID: 17116239

    Google Scholar 

  • Martinez LC, Yakhnin H, Camacho MI, Georgellis D, Babitzke P, Puente JL et al (2011) Integration of a complex regulatory cascade involving the SirA/BarA and Csr global regulatory systems that controls expression of the Salmonella SPI-1 and SPI-2 virulence regulons through HilD. Mol Microbiol 80(6):1637–1656. https://doi.org/10.1111/j.1365-2958.2011.07674.x. PubMed PMID: 21518393; PubMed Central PMCID: PMC3116662

  • McCaw ML, Lykken GL, Singh PK, Yahr TL (2002) ExsD is a negative regulator of the Pseudomonas aeruginosa type III secretion regulon. Mol Microbiol 46(4):1123–1133. PubMed PMID: 12421316

    Google Scholar 

  • Mercante J, Edwards AN, Dubey AK, Babitzke P, Romeo T (2009) Molecular geometry of CsrA (RsmA) binding to RNA and its implications for regulated expression. J Mol Biol 392(2):511–528. https://doi.org/10.1016/j.jmb.2009.07.034. PubMed PMID: 19619561; PubMed Central PMCID: PMC2735826

  • Miller HK, Kwuan L, Schwiesow L, Bernick DL, Mettert E, Ramirez HA et al (2014) IscR is essential for Yersinia pseudotuberculosis type III secretion and virulence. PLoS Pathog 10(6):e1004194. https://doi.org/10.1371/journal.ppat.1004194. PubMed PMID: 24945271; PubMed Central PMCID: PMC4055776

  • Mohanty BK, Kushner SR (2016)Regulation of mRNA decay in bacteria. Annu Rev Microbiol 70:25–44. https://doi.org/10.1146/annurev-micro-091014-104515. PubMed PMID: 27297126

  • Navarre WW, Porwollik S, Wang Y, McClelland M, Rosen H, Libby SJ et al (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313(5784):236–238. PubMed PMID: 16763111

    Google Scholar 

  • Nuss AM, Beckstette M, Pimenova M, Schmühl C, Opitz W, Pisano F et al (2017) Tissue dual RNA-seq: a fast discovery path for infection-specific functions and riboregulators shaping host-pathogen transcriptomes. Proc Natl Acad Sci USA 114(5):E791–E800

    Google Scholar 

  • Okan NA, Bliska JB, Karzai AW (2006) A Role for the SmpB-SsrA system in Yersinia pseudotuberculosis pathogenesis. PLoS Pathog 2(1):e6. https://doi.org/10.1371/journal.ppat.0020006. Epub 2006/02/02. PubMed PMID: 16450010; PubMed Central PMCID: PMC1358943

  • Olekhnovich IN, Kadner RJ (2007) Role of nucleoid-associated proteins Hha and H-NS in expression of Salmonella enterica activators HilD, HilC, and RtsA required for cell invasion. J Bacteriol 89(19):6882–6890. https://doi.org/10.1128/jb.00905-07. PubMed PMID: 17675384; PubMed Central PMCID: PMC2045230

  • Ozturk G, LeGrand K, Zheng Y, Young GM (2017) Yersinia enterocolitica CsrA regulates expression of the Ysa and Ysc type 3 secretion system in unique ways. FEMS Microbiol Lett 364(20). https://doi.org/10.1093/femsle/fnx204. PubMed PMID: 29044402

  • Parsot C, Ageron E, Penno C, Mavris M, Jamoussi K, d’Hauteville H et al (2005) A secreted anti-activator, OspD1, and its chaperone, Spa15, are involved in the control of transcription by the type III secretion apparatus activity in Shigella flexneri. Mol Microbiol 56(6):1627–1635. https://doi.org/10.1111/j.1365-2958.2005.04645.x. PubMed PMID: 15916611

  • Pettersson J, Nordfelth R, Dubinina E, Bergman T, Gustafsson M, Magnusson KE et al (1996) Modulation of virulence factor expression by pathogen target cell contact. Science 273(5279):1231–1233

    Google Scholar 

  • Poncet S, Milohanic E, Maze A, Abdallah JN, Ake FML et al (2009) Correlations between carbon metabolism and virulence in bacteria. Contrib Microbiol 16:88–102

    Google Scholar 

  • Portaliou AG, Tsolis KC, Loos MS, Zorzini V, Economou A (2016) Type III secretion: building and operating a remarkable nanomachine. Trends Biochem Sci 41(2):175–189. https://doi.org/10.1016/j.tibs.2015.09.005. PubMed PMID: 26520801

  • Ren B, Shen H, Lu ZJ, Liu H, Xu Y (2014) The phzA2-G2 transcript exhibits direct RsmA-mediated activation in Pseudomonas aeruginosa M18. PLoS One 9(2):e89653. https://doi.org/10.1371/journal.pone.0089653. PubMed PMID: 24586939; PubMed Central PMCID: PMCPMC3933668

  • Rhigetti F, Nuss AM, Twittenhoff C, Beele S, Urban K, Will S et al (2016) Temperature-responsive in vitro RNA structurome of Yersinia pseudotuberculosis. Proc Natl Acad Sci 113(26):7237–7242

    Google Scholar 

  • Rietsch A, Vallet-Gely I, Dove SL, Mekalanos JJ (2005) ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 102(22):8006–8011. https://doi.org/10.1073/pnas.0503005102. PubMed PMID: 15911752; PubMed Central PMCID: PMCPMC1142391

  • Rosenzweig JA, Chopra AK (2013) The exoribonuclease polynucleotide phosphorylase influences the virulence and stress responses of yersiniae and many other pathogens. Front Cell Infect Microbiol 3:81. https://doi.org/10.3389/fcimb.2013.00081. PubMed PMID: 24312901; PubMed Central PMCID: PMCPMC3832800

  • Rosenzweig JA, Weltman G, Plano GV, Schesser K (2005) Modulation of Yersinia type three secretion system by the S1 domain of polynucleotide phosphorylase. J Biol Chem 280(1):156–163. https://doi.org/10.1074/jbc.m405662200. PubMed PMID: 15509583

  • Rosenzweig JA, Chromy B, Echeverry A, Yang J, Adkins B, Plano GV et al (2007) Polynucleotide phosphorylase independently controls virulence factor expression levels and export in Yersinia spp. FEMS Microbiol Lett 270(2):255–264. https://doi.org/10.1111/j.1574-6968.2007.00689.x. PubMed PMID: 17391372

  • Schiano CA, Bellows LE, Lathem WW (2010) The small RNA chaperone Hfq is required for the virulence of Yersinia pseudotuberculosis. Infect Immun 78(5):2034–2044. https://doi.org/10.1128/iai.01046-09. PubMed PMID: 20231416; PubMed Central PMCID: PMC2863511

  • Schiano CA, Koo JT, Schipma MJ, Caulfield AJ, Jafari N, Lathem WW (2014) Genome-wide analysis of small RNAs expressed by Yersinia pestis identifies a regulator of the Yop-Ysc type III secretion system. J Bacteriol 196(9):1659–1670. Epub 2014/02/18. https://doi.org/10.1128/jb.01456-13. PubMed PMID: 24532772; PubMed Central PMCID: PMC3993326

  • Schleif R (2010) AraC protein, regulation of the l-arabinose operon in Escherichia coli, and the light switch mechanism of AraC action. FEMS Microbiol Rev 34(5):779–796. https://doi.org/10.1111/j.1574-6976.2010.00226.x. PubMed PMID: 20491933

  • Schulmeyer KH, Yahr TL (2017) Post-transcriptional regulation of type III secretion in plant and animal pathogens. Curr Opin Microbiol 36:30–36. https://doi.org/10.1016/j.mib.2017.01.009. PubMed PMID: 28189908; PubMed Central PMCID: PMCPMC5534366

  • Schwiesow L, Lam H, Dersch P, Auerbuch V (2015) Yersinia type III secretion system master regulator LcrF. J Bacteriol 198(4):604–614. https://doi.org/10.1128/jb.00686-15. PubMed PMID: 26644429; PubMed Central PMCID: PMCPMC4751813

  • Shimizu T, Ichimura K, Noda M (2015) The surface sensor NlpE of enterohemorrhagic Escherichia coli contributes to regulation of the type III secretion system and flagella by the Cpx response to adhesion. Infect Immun 84(2):537–549. https://doi.org/10.1128/iai.00881-15. PubMed PMID: 26644384; PubMed Central PMCID: PMCPMC4730559

  • Sittka A, Pfeiffer V, Tedin K, Vogel J (2007) The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol Microbiol 63(1):193–217. https://doi.org/10.1111/j.1365-2958.2006.05489.x. PubMed PMID: 17163975; PubMed Central PMCID: PMCPMC1810395

  • Standish AJ, Teh MY, Tran ENH, Doyle MT, Baker PJ, Morona R (2016) Unprecedented abundance of protein tyrosine phosphorylation modulates Shigella flexneri virulence. J Mol Biol 428(20):4197–4208. https://doi.org/10.1016/j.jmb.2016.06.016. PubMed PMID: 27380737

  • Tanabe T, Miyamoto K, Tsujibo H, Yamamoto S, Funahashi T (2015) The small RNA Spot 42 regulates the expression of the type III secretion system 1 (T3SS1) chaperone protein VP1682 in Vibrio parahaemolyticus. FEMS Microbiol Lett 362(21). https://doi.org/10.1093/femsle/fnv173. PubMed PMID: 26394644

  • Teixido L, Carrasco B, Alonso JC, Barbe J, Campoy S (2011) Fur activates the expression of Salmonella enterica pathogenicity island 1 by directly interacting with the hilD operator in vivo and in vitro. PLoS One 6(5):e19711. https://doi.org/10.1371/journal.pone.0019711. PubMed PMID: 21573071; PubMed Central PMCID: PMC3089636

  • Tobe T, Yen H, Takahashi H, Kagayama Y, Ogasawara N, Oshima T (2014 )Antisense transcription regulates the expression of the enterohemorrhagic Escherichia coli virulence regulatory gene ler in response to the intracellular iron concentration. PLoS One 9(7):e101582. https://doi.org/10.1371/journal.pone.0101582. PubMed PMID: 25006810; PubMed Central PMCID: PMCPMC4090186

  • Urbanowski ML, Lykken GL, Yahr TL (2005) A secreted regulatory protein couples transcription to the secretory activity of the Pseudomonas aeruginosa type III secretion system. Proc Natl Acad Sci USA 102(28):9930–9935. https://doi.org/10.1073/pnas.0504405102. PubMed PMID: 15985546; PubMed Central PMCID: PMC1175016

  • Vakulskas CA, Brady KM, Yahr TL (2009) Mechanism of transcriptional activation by Pseudomonas aeruginosa ExsA. J Bacteriol 191(21):6654–6664. https://doi.org/10.1128/jb.00902-09. PubMed PMID: 19717612; PubMed Central PMCID: PMC2795306

  • Vakulskas CA, Potts AH, Babitzke P, Ahmer BM, Romeo T (2015) Regulation of bacterial virulence by Csr (Rsm) systems. Microbiol Mol Biol Rev 79(2):193–224. https://doi.org/10.1128/mmbr.00052-14. PubMed PMID: 25833324

  • Vergnes A, Viala JP, Ouadah-Tsabet R, Pocachard B, Loiseau L, Meresse S et al (2017) The iron-sulfur cluster sensor IscR is a negative regulator of Spi1 type III secretion system in Salmonella enterica. Cell Microbiol 19(4). https://doi.org/10.1111/cmi.12680. PubMed PMID: 27704705

  • Wang H, Avican K, Fahlgren A, Erttmann SF, Nuss AM, Dersch P et al (2016) Increased plasmid copy number is essential for Yersinia T3SS function and virulence. Science 353(6298):492–495. https://doi.org/10.1126/science.aaf7501. PubMed PMID: 27365311

  • Yakhnin AV, Baker CS, Vakulskas CA, Yakhnin H, Berezin I, Romeo T et al (2013) CsrA activates flhDC expression by protecting flhDC mRNA from RNase E-mediated cleavage. Mol Microbiol 87(4):851–866. https://doi.org/10.1111/mmi.12136. PubMed PMID: 23305111; PubMed Central PMCID: PMCPMC3567230

  • Yang J, Jain C, Schesser K (2008) RNase E regulates the Yersinia type 3 secretion system. J Bacteriol 190(10):3774–3778. https://doi.org/10.1128/jb.00147-08. PubMed PMID: 18359811; PubMed Central PMCID: PMCPMC2395017

  • Zheng Z, Chen G, Joshi S, Brutinel ED, Yahr TL, Chen L (2007) Biochemical characterization of a regulatory cascade controlling transcription of the Pseudomonas aeruginosa type III secretion system. J Biol Chem 282(9):6136–6142. https://doi.org/10.1074/jbc.m611664200. PubMed PMID: 17197437

  • Zhou X, Konkel ME, Call DR (2010) Regulation of type III secretion system 1 gene expression in Vibrio parahaemolyticus is dependent on interactions between ExsA, ExsC, and ExsD. Virulence 1(4):260–272. https://doi.org/10.4161/viru.1.4.12318. PubMed PMID: 21178451; PubMed Central PMCID: PMCPMC3073295

  • Zierler MK, Galan JE (1995) Contact with cultured epithelial cells stimulates secretion of Salmonella typhimurium invasion protein InvJ. Infect Immun 63(10):4024–4028

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Petra Dersch .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Volk, M., Vollmer, I., Heroven, A.K., Dersch, P. (2019). Transcriptional and Post-transcriptional Regulatory Mechanisms Controlling Type III Secretion. In: Wagner, S., Galan, J. (eds) Bacterial Type III Protein Secretion Systems. Current Topics in Microbiology and Immunology, vol 427. Springer, Cham. https://doi.org/10.1007/82_2019_168

Download citation

Publish with us

Policies and ethics