Role of Overexpressed CFA/I Fimbriae in Bacterial Swimming

Overview

Journal Phys Biol

Specialty Biochemistry

Date 2012 May 8

PMID 22562964

Citations 5

Authors

Ling Cao

Zhiyong Suo

Timothy Lim

SangMu Jun

Muhammedin Deliorman

Carol Riccardi

Laura Kellerman

Recep Avci

Xinghong Yang

Affiliations

Soon will be listed here.

Abstract

Enterotoxigenic Escherichia coli CFA/I is a protective antigen and has been overexpressed in bacterial vectors, such as Salmonella Typhimurium H683, to generate vaccines. Effects that overexpressed CFA/I may engender on the bacterial host remain largely unexplored. To investigate, we constructed a high CFA/I expression strain, H683-pC2, and compared it to a low CFA/I expression strain, H683-pC, and to a non-CFA/I expression strain, H683-pY. The results showed that H683-pC2 was less able to migrate into semisolid agar (0.35%) than either H683-pC or H683-pY. Bacteria that migrated showed motility halo sizes of H683-pC2 < H683-pC < H683-pY. In the liquid culture media, H683-pC2 cells precipitated to the bottom of the tube, while those of H683-pY did not. In situ imaging revealed that H683-pC2 bacilli tended to auto-agglutinate within the semisolid agar, while H683-pY bacilli did not. When the cfaBE fimbrial fiber encoding genes were deleted from pC2, the new plasmid, pC2(-), significantly recovered bacterial swimming capability. Our study highlights the negative impact of overexpressed CFA/I fimbriae on bacterial swimming motility.

Citing Articles

Endospore pili: Flexible, stiff, and sticky nanofibers.

Jonsmoen U, Malyshev D, Oberg R, Dahlberg T, Aspholm M, Andersson M Biophys J. 2023; 122(13):2696-2706.

PMID: 37218131 PMC: 10397575. DOI: 10.1016/j.bpj.2023.05.024.

Bioactive Immune Components of Anti-Diarrheagenic Enterotoxigenic Escherichia coli Hyperimmune Bovine Colostrum Products.

Sears K, Tennant S, Reymann M, Simon R, Konstantopoulos N, Blackwelder W Clin Vaccine Immunol. 2017; 24(8).

PMID: 28637804 PMC: 5583472. DOI: 10.1128/CVI.00186-16.

Regulatory T-cell vaccination independent of auto-antigen.

Pascual D, Yang X, Holderness K, Jun S, Maddaloni M, Kochetkova I Exp Mol Med. 2014; 46:e82.

PMID: 24626168 PMC: 3972794. DOI: 10.1038/emm.2014.4.

Attenuating gene expression (AGE) for vaccine development.

Pascual D, Suo Z, Cao L, Avci R, Yang X Virulence. 2013; 4(5):384-90.

PMID: 23652809 PMC: 3714130. DOI: 10.4161/viru.24886.

Flagella overexpression attenuates Salmonella pathogenesis.

Yang X, Thornburg T, Suo Z, Jun S, Robison A, Li J PLoS One. 2012; 7(10):e46828.

PMID: 23056473 PMC: 3463563. DOI: 10.1371/journal.pone.0046828.

References

TITTSLER R, SANDHOLZER L . The Use of Semi-solid Agar for the Detection of Bacterial Motility. J Bacteriol. 1936; 31(6):575-80. PMC: 543748. DOI: 10.1128/jb.31.6.575-580.1936. View

Evans D, Evans Jr D, Clegg S, Pauley J . Purification and characterization of the CFA/I antigen of enterotoxigenic Escherichia coli. Infect Immun. 1979; 25(2):738-48. PMC: 414505. DOI: 10.1128/iai.25.2.738-748.1979. View

Baker K, Levine M, Morison J, Phillips A, Barry E . CfaE tip mutations in enterotoxigenic Escherichia coli CFA/I fimbriae define critical human intestinal binding sites. Cell Microbiol. 2009; 11(5):742-54. PMC: 2921025. DOI: 10.1111/j.1462-5822.2009.01287.x. View

Galan J, Nakayama K, Curtiss 3rd R . Cloning and characterization of the asd gene of Salmonella typhimurium: use in stable maintenance of recombinant plasmids in Salmonella vaccine strains. Gene. 1990; 94(1):29-35. DOI: 10.1016/0378-1119(90)90464-3. View

Tobias J, Holmgren J, Hellman M, Nygren E, Lebens M, Svennerholm A . Over-expression of major colonization factors of enterotoxigenic Escherichia coli, alone or together, on non-toxigenic E. coli bacteria. Vaccine. 2010; 28(43):6977-84. DOI: 10.1016/j.vaccine.2010.08.047. View

Alves A, Lasaro M, Almeida D, Ferreira L . DNA immunisation against the CFA/I fimbriae of enterotoxigenic Escherichia coli (ETEC). Vaccine. 2000; 19(7-8):788-95. DOI: 10.1016/s0264-410x(00)00244-9. View

Finlay B, Falkow S . Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev. 1997; 61(2):136-69. PMC: 232605. DOI: 10.1128/mmbr.61.2.136-169.1997. View

Saulino E, Bullitt E, Hultgren S . Snapshots of usher-mediated protein secretion and ordered pilus assembly. Proc Natl Acad Sci U S A. 2000; 97(16):9240-5. PMC: 16852. DOI: 10.1073/pnas.160070497. View

Savelkoul P, Willshaw G, McConnell M, Smith H, Hamers A, van der Zeijst B . Expression of CFA/I fimbriae is positively regulated. Microb Pathog. 1990; 8(2):91-9. DOI: 10.1016/0882-4010(90)90073-y. View

10.

Guttenplan S, Blair K, Kearns D . The EpsE flagellar clutch is bifunctional and synergizes with EPS biosynthesis to promote Bacillus subtilis biofilm formation. PLoS Genet. 2010; 6(12):e1001243. PMC: 3000366. DOI: 10.1371/journal.pgen.1001243. View

11.

Amiel E, Lovewell R, OToole G, Hogan D, Berwin B . Pseudomonas aeruginosa evasion of phagocytosis is mediated by loss of swimming motility and is independent of flagellum expression. Infect Immun. 2010; 78(7):2937-45. PMC: 2897393. DOI: 10.1128/IAI.00144-10. View

12.

Ascon M, Hone D, Walters N, Pascual D . Oral immunization with a Salmonella typhimurium vaccine vector expressing recombinant enterotoxigenic Escherichia coli K99 fimbriae elicits elevated antibody titers for protective immunity. Infect Immun. 1998; 66(11):5470-6. PMC: 108685. DOI: 10.1128/IAI.66.11.5470-5476.1998. View

13.

Celli J, Turner B, Afdhal N, Keates S, Ghiran I, Kelly C . Helicobacter pylori moves through mucus by reducing mucin viscoelasticity. Proc Natl Acad Sci U S A. 2009; 106(34):14321-6. PMC: 2732822. DOI: 10.1073/pnas.0903438106. View

14.

Maaloum M, Pernodet N, Tinland B . Agarose gel structure using atomic force microscopy: gel concentration and ionic strength effects. Electrophoresis. 1998; 19(10):1606-10. DOI: 10.1002/elps.1150191015. View

15.

Epstein E, Chapman M . Polymerizing the fibre between bacteria and host cells: the biogenesis of functional amyloid fibres. Cell Microbiol. 2008; 10(7):1413-20. PMC: 2674401. DOI: 10.1111/j.1462-5822.2008.01148.x. View

16.

Wu S, Pascual D, Vancott J, McGhee J, Maneval Jr D, Levine M . Immune responses to novel Escherichia coli and Salmonella typhimurium vectors that express colonization factor antigen I (CFA/I) of enterotoxigenic E. coli in the absence of the CFA/I positive regulator cfaR. Infect Immun. 1995; 63(12):4933-8. PMC: 173709. DOI: 10.1128/iai.63.12.4933-4938.1995. View

17.

Pandey G, Jain R . Bacterial chemotaxis toward environmental pollutants: role in bioremediation. Appl Environ Microbiol. 2002; 68(12):5789-95. PMC: 134409. DOI: 10.1128/AEM.68.12.5789-5795.2002. View

18.

Lindhout T, Lau P, Brewer D, Lam J . Truncation in the core oligosaccharide of lipopolysaccharide affects flagella-mediated motility in Pseudomonas aeruginosa PAO1 via modulation of cell surface attachment. Microbiology (Reading). 2009; 155(Pt 10):3449-3460. DOI: 10.1099/mic.0.030510-0. View

19.

Yang X, Suo Z, Thornburg T, Holderness K, Cao L, Lim T . Expression of Escherichia coli virulence usher protein attenuates wild-type Salmonella. Virulence. 2012; 3(1):29-42. PMC: 3337150. DOI: 10.4161/viru.3.1.18447. View

20.

Magariyama Y, Sugiyama S, Muramoto K, Kawagishi I, Imae Y, Kudo S . Simultaneous measurement of bacterial flagellar rotation rate and swimming speed. Biophys J. 1995; 69(5):2154-62. PMC: 1236449. DOI: 10.1016/S0006-3495(95)80089-5. View