Roles of the Tol-Pal System in the Type III Secretion System and Flagella-mediated Virulence in Enterohemorrhagic Escherichia Coli

Overview

Journal Sci Rep

Specialty Science

Date 2020 Sep 24

PMID 32968151

Citations 14

Authors

Hidetada Hirakawa

Kazutomo Suzue

Ayako Takita

Chikako Awazu

Jun Kurushima

Haruyoshi Tomita

Affiliations

Soon will be listed here.

Abstract

The Tol-Pal system is a protein complex that is highly conserved in many gram-negative bacteria. We show here that the Tol-Pal system is associated with the enteric pathogenesis of enterohemorrhagic E. coli (EHEC). Deletion of tolB, which is required for the Tol-Pal system decreased motility, secretion of the Type III secretion system proteins EspA/B, and the ability of bacteria to adhere to and to form attaching and effacing (A/E) lesions in host cells, but the expression level of LEE genes, including espA/B that encode Type III secretion system proteins were not affected. The Citrobacter rodentium, tolB mutant, that is traditionally used to estimate Type III secretion system associated virulence in mice did not cause lethality in mice while it induced anti-bacterial immunity. We also found that the pal mutant, which lacks activity of the Tol-Pal system, exhibited lower motility and EspA/B secretion than the wild-type parent. These combined results indicate that the Tol-Pal system contributes to the virulence of EHEC associated with the Type III secretion system and flagellar activity for infection at enteric sites. This finding provides evidence that the Tol-Pal system may be an effective target for the treatment of infectious diseases caused by pathogenic E. coli.

Citing Articles

subsp. requires a genus-specific outer membrane protein and TolB to coordinate cell membrane integrity and virulence.

Wu L, Zhu X, Long H, Huang X, Zhu S, Xue Q Microbiol Spectr. 2025; 13(2):e0252124.

PMID: 39817731 PMC: 11792487. DOI: 10.1128/spectrum.02521-24.

AlgU mediates hyperosmotic tolerance in SN15-2 by regulating membrane stability, ROS scavenging, and osmolyte synthesis.

Wang J, Wang Y, Lu S, Lou H, Wang X, Wang W Appl Environ Microbiol. 2024; 90(8):e0059624.

PMID: 39023265 PMC: 11337839. DOI: 10.1128/aem.00596-24.

Attenuated mutants of Typhimurium mediate melanoma regression via an immune response.

Jorge G, Gontijo M, Floro E Silva M, Goes I, Jaimes-Florez Y, Coser L Exp Biol Med (Maywood). 2024; 249:10081.

PMID: 38974834 PMC: 11224151. DOI: 10.3389/ebm.2024.10081.

Construction and application of the conditionally essential gene knockdown library in to screen potential antimicrobial targets and virulence genes via Mobile-CRISPRi-seq.

Zhu Q, Lin Q, Jiang Y, Chen S, Tian J, Yang S Appl Environ Microbiol. 2023; 89(10):e0095623.

PMID: 37815340 PMC: 10617577. DOI: 10.1128/aem.00956-23.

The Tol-Pal system of Acinetobacter baumannii is important for cell morphology, antibiotic resistance and virulence.

Hubloher J, van der Sande L, Schaudinn C, Muller V, Averhoff B Int Microbiol. 2023; 26(3):543-550.

PMID: 36648597 PMC: 10397113. DOI: 10.1007/s10123-022-00319-9.

References

Karmali M . Infection by verocytotoxin-producing Escherichia coli. Clin Microbiol Rev. 1989; 2(1):15-38. PMC: 358098. DOI: 10.1128/CMR.2.1.15. View

Tarr P, Gordon C, Chandler W . Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet. 2005; 365(9464):1073-86. DOI: 10.1016/S0140-6736(05)71144-2. View

Hueck C . Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev. 1998; 62(2):379-433. PMC: 98920. DOI: 10.1128/MMBR.62.2.379-433.1998. View

Nataro J, Kaper J . Diarrheagenic Escherichia coli. Clin Microbiol Rev. 1998; 11(1):142-201. PMC: 121379. DOI: 10.1128/CMR.11.1.142. View

Sandvig K, van Deurs B . Entry of ricin and Shiga toxin into cells: molecular mechanisms and medical perspectives. EMBO J. 2000; 19(22):5943-50. PMC: 305844. DOI: 10.1093/emboj/19.22.5943. View

Galan J, Wolf-Watz H . Protein delivery into eukaryotic cells by type III secretion machines. Nature. 2006; 444(7119):567-73. DOI: 10.1038/nature05272. View

Kenny B, DeVinney R, Stein M, Reinscheid D, Frey E, Finlay B . Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell. 1997; 91(4):511-20. DOI: 10.1016/s0092-8674(00)80437-7. View

Garmendia J, Frankel G, Crepin V . Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun. 2005; 73(5):2573-85. PMC: 1087358. DOI: 10.1128/IAI.73.5.2573-2585.2005. View

Tobe T, Beatson S, Taniguchi H, Abe H, Bailey C, Fivian A . An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc Natl Acad Sci U S A. 2006; 103(40):14941-6. PMC: 1595455. DOI: 10.1073/pnas.0604891103. View

10.

McDaniel T, Kaper J . A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol Microbiol. 1997; 23(2):399-407. DOI: 10.1046/j.1365-2958.1997.2311591.x. View

11.

Webster R . The tol gene products and the import of macromolecules into Escherichia coli. Mol Microbiol. 1991; 5(5):1005-11. DOI: 10.1111/j.1365-2958.1991.tb01873.x. View

12.

Lazzaroni J, Germon P, Ray M, Vianney A . The Tol proteins of Escherichia coli and their involvement in the uptake of biomolecules and outer membrane stability. FEMS Microbiol Lett. 1999; 177(2):191-7. DOI: 10.1111/j.1574-6968.1999.tb13731.x. View

13.

Walburger A, Lazdunski C, Corda Y . The Tol/Pal system function requires an interaction between the C-terminal domain of TolA and the N-terminal domain of TolB. Mol Microbiol. 2002; 44(3):695-708. DOI: 10.1046/j.1365-2958.2002.02895.x. View

14.

Dubuisson J, Vianney A, Hugouvieux-Cotte-Pattat N, Lazzaroni J . Tol-Pal proteins are critical cell envelope components of Erwinia chrysanthemi affecting cell morphology and virulence. Microbiology (Reading). 2005; 151(Pt 10):3337-3347. DOI: 10.1099/mic.0.28237-0. View

15.

Heilpern A, Waldor M . CTXphi infection of Vibrio cholerae requires the tolQRA gene products. J Bacteriol. 2000; 182(6):1739-47. PMC: 94473. DOI: 10.1128/JB.182.6.1739-1747.2000. View

16.

Bowe F, Lipps C, Tsolis R, Groisman E, Heffron F, Kusters J . At least four percent of the Salmonella typhimurium genome is required for fatal infection of mice. Infect Immun. 1998; 66(7):3372-7. PMC: 108354. DOI: 10.1128/IAI.66.7.3372-3377.1998. View

17.

Fortney K, Young R, Bauer M, Katz B, Hood A, Munson Jr R . Expression of peptidoglycan-associated lipoprotein is required for virulence in the human model of Haemophilus ducreyi infection. Infect Immun. 2000; 68(11):6441-8. PMC: 97731. DOI: 10.1128/IAI.68.11.6441-6448.2000. View

18.

Hellman J, Roberts Jr J, Tehan M, Allaire J, Warren H . Bacterial peptidoglycan-associated lipoprotein is released into the bloodstream in gram-negative sepsis and causes inflammation and death in mice. J Biol Chem. 2002; 277(16):14274-80. DOI: 10.1074/jbc.M109696200. View

19.

Masilamani R, Cian M, Dalebroux Z . Salmonella Tol-Pal Reduces Outer Membrane Glycerophospholipid Levels for Envelope Homeostasis and Survival during Bacteremia. Infect Immun. 2018; 86(7). PMC: 6013679. DOI: 10.1128/IAI.00173-18. View

20.

Hirakawa H, Suzue K, Kurabayashi K, Tomita H . The Tol-Pal System of Uropathogenic Is Responsible for Optimal Internalization Into and Aggregation Within Bladder Epithelial Cells, Colonization of the Urinary Tract of Mice, and Bacterial Motility. Front Microbiol. 2019; 10:1827. PMC: 6698795. DOI: 10.3389/fmicb.2019.01827. View