The outer core lipopolysaccharide of Salmonella enterica serovar Typhi is required for bacterial entry into epithelial cells

Infection and Immunity

Volumn 74, Issue 3, 2006, Pages 1555-1564

  Hoare, Anilei ^a   Bittner, Mauricio ^a   Carter, Javier ^a   Alvarez, Sergio ^a   Zaldívar, Mercedes ^a   Bravo, Denisse ^a   Valvano, Miguel A ^b   Contreras, Inés ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; GLUCOSE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM MUTANT; EPITHELIUM CELL; GENE; GENE DELETION; INTERNALIZATION; MOLECULAR RECOGNITION; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLA ENTERICA SEROVAR TYPHI; SALMONELLA TYPHI; TYPHOID FEVER; WAAB GENE; WAAG GENE; WAAI GENE; WAAJ GENE; WAAK GENE; WBAP GENE; WZY GENE; WZZ GENE;

CELL LINE; EPITHELIAL CELLS; LIPOPOLYSACCHARIDES; SALMONELLA TYPHI;

EID: 33644779645     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.74.3.1555-1564.2006     Document Type: Article

References (63)

1. Alonso, A., and F. García-del Portillo. 2004. Hijacking of eukaryotic functions by intracellular bacterial pathogens. Int. Microbiol. 7:181-191.
2. Bengoechea, J. A., H. Najdenski, and M. Skurnik. 2004. Lipopolysaccharide O antigen status of Yersinia enterocolitica O:8 is essential for virulence and absence of O antigen affects the expression of the other Yersinia virulence factors. Mol. Microbiol. 52:451-469.
3. Bittner, M., S. Saldías, C. Estévez, M. Zaldívar, C. L. Marolda, M. A. Valvano, and I. Contreras. 2002. O-antigen expression in Salmonella enterica serovar Typhi is regulated by nitrogen availability through RpoN-mediated transcriptional control of the rfaH gene. Microbiology 148:3789-3799.
4. Bittner, M., S. Saldías, F. Altamirano, M. A. Valvano, and I. Contreras. 2004. RpoS and RpoN are involved in the growth-dependent regulation of rfaH transcription and O antigen expression in Salmonella enterica serovar Typhi. Microb. Pathog. 36:19-24.
5. R cassettes with the option of Flp-catalized excision of the antibiotic-resistance determinant. Gene 158:9-14.
6. Coyne, M. J., Jr., K. S. Russell, C. L. Coyle, and J. A. Goldberg. 1994. The Pseudomonas aeruginosa algC gene encodes phosphoglucomutase, required for the synthesis of a complete lipopolysaccharide core. J. Bacteriol. 176:3500-3507.
7. Crump, J. A., S. P. Luby, and E. D. Mintz. 2004. The global burden of typhoid fever. Bull. W. H. O. 8:346-353.
8. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
9. Edwards, R. A., G. J. Olsen, and S. R. Maloy. 2002. Comparative genomics of closely related salmonellae. Trends Microbiol. 10:94-99.
10. Farewell, A., R. Brazas, E. Davie, J. Mason, and L. I. Rothfield. 1991. Suppression of the abnormal phenotype of Salmonella typhimurium rfaH mutants by mutations in the genes for transcription termination factor Rho. J. Bacteriol. 173:5188-5193.
11. Finlay, B. B., M. N. Starnbach, C. L. Francis, B. A. D. Stocker, S. Chatfield, G. Dougan, and S. Falkow. 1998. Identification and characterization of TnphoA mutants of Salmonella that are unable to pass through a polarized MDCK epithelial cell monolayer. Mol. Microbiol. 2:757-766.
12. Galán, J. E. 2001. Salmonella interactions with host cells: type III secretion at work. Annu. Rev. Cell Dev. Biol. 17:53-86.
13. Groissman, E, A., and C. Mouslim. 2000. Molecular mechanisms of Salmonella pathogenesis. Curr. Opin. Infect. Dis. 13:519-522.
14. Heinrichs, D. E., M. A. Monteiro, M. B. Perry, and C. Whitfield. 1998. The assembly system for the lipopolysaccharide R2 core-type of Escherichia coli is a hybrid of those found in Escherichia coli K12 and Salmonella enterica. J. Biol. Chem. 273:8849-8859.
15. Hitchcock, P. J., and T. M. Brown. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154:269-277.
16. House, D., A. Bishop, C. Parry, G. Dougan, and J. Wain. 2001. Typhoid fever: pathogenesis and disease. Curr. Opin. Infect. Dis. 14:573-578.
17. Jacques, M. 1996. Role of lipo-oligosaccharides and lipopolysaccharides in bacterial adherence. Trends Microbiol. 4:408-409.
18. Jarrell, K., and A. M. Kropiski. 1977. The chemical composition of the lipopolysaccharide from Pseudomonas aeruginosa strain PAO and a spontaneously derived rough mutant. Microbios 19:103-116.
19. Jones, B. D., and S. Falkow. 1996. Salmonellosis: host immune responses and bacterial virulence determinants. Annu. Rev. Immunol. 14:533-561.
20. Jones, B. D., C. A. Lee, and S. Falkow. 1992. Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect. Immun. 60:2475-2480.
21. Jones, G. H., L. A. Richardson, and D. Uhlman. 1981. The invasion of HeLa cells by Salmonella typhimurium: reversible and irreversible bacterial attachment and the role of bacterial motility. J. Gen. Microbiol. 127:351-360.
22. Khoramina-Falsati, T., S. Harayama, K. Kutsukake, and J. C. Pechere. 1990. Effect of motility and chemotaxis on the invasion of Salmonella typhimurium into HeLa cells. Microb. Pathog. 9:47-53.
23. Kihlstrom, E., and L. Edebo. 1976. Association of viable and inactivated Salmonella typhimurium 395 MS and MR 10 with HeLa cells. Infect. Immun. 14:851-857.
24. Komeda, Y., T. Icho, and T. Iino. 1977. Effects of galU mutation on flagellar formation in Escherichia coli. J. Bacteriol. 129:908-915.
25. Kropiski, A. M., L. C. Chan, and F. H. Milazzo. 1979. The extraction and analysis of lipopolysaccharide from Pseudomonas aeruginosa strain PAO, and three rough mutants. Can. J. Microbiol. 25:390-398.
26. Lee, C. A., B. D. Jones, and S. Falkow. 1992. Identification of a Salmonella typhimurium locus by selection of hyperinvasive mutants. Proc. Natl. Acad. Sci. USA 87:1847-1851.
27. Lesse, A., A. Campagnari, W. E. Bittner, and M. A. Apicella. 1990. Increased resolution of lipopolysaccharides and lipooligosaccharides utilizing tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis. J. Immunol. Methods 126:109-117.
28. Levine, M. M., and B. Sztein. 2000. Shigella, Salmonella typhi, and Escherichia coli, p. 171-194. In M. W. Cunningham and R. S. Fujinami (ed.), Effects of microbes on the immune system. Lippincott, Williams & Wilkins, Philadelphia, Pa.
29. Liu, S.-L., T. Ezaki, H. Miura, K. Matsui, and E. Yabuuchi. 1988. Intact motility as a Salmonella typhi invasion-related factor. Infect. Immun. 56:1967-1973.
30. Lukomski, S., R. A. Hull, and S. I. Hull. 1996. Identification of the O antigen polymerase (rfc) gene in Escherichia coli O4 by insertional mutagenesis using a nonpolar chloramphenicol resistance cassette. J. Bacteriol. 178:240-247.
31. Lyczak, J. B., T. S. Zaidi, M. Grout, M. Bittner, I. Contreras, and G. B. Pier. 2001. Epithelial cell contact-induced alterations in Salmonella enterica serovar Typhi lipopolysaccharide are critical for bacterial internalization. Cell. Microbiol. 3:763-772.
32. Marolda, C. L., and M. A. Valvano. 1998. Promoter region of the Escherichia coli O:7-specific lipopolysaccharide gene cluster: structural and functional characterization of an upstream untranslated mRNA sequence. J. Bacteriol. 180:3070-3079.
33. McClelland, M., K. E. Sanderson, J. Spieth, S. W. Clifton, P. Latreille, L. Courtney, S. Porwollik, J. Ali, M. Dante, F. Du, S. Hou, D. Layman, S. Leonard, C. Nguyen, K. Scott, A. Holmes, N. Grewal, E. Mulvaney, E. Ryan, H. Sun, L. Florea, W. Miller, T. Stoneking, M. Nhan, R. Waterston, and R. K. Wilson. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852-856.
34. Miller, I., D. Maskell, C. Hormaeche, K. Johnson, D. Pickard, and G. Dougan. 1989. Isolation of orally attenuated Salmonella typhimurium following TnphoA mutagenesis. Infect. Immun. 57:2758-2763.
35. Mills, S. D., and B. B. Finlay. 1994. Comparison of Salmonella typhi and Salmonella typhimurium: invasion, intracellular growth and localization in cultured human epithelial cells. Microb. Pathog. 17:409-423.
36. Morris, C., C. M. C. Yip, I. S. M. Tsui, D. K-H. Wong, and J. Hackett. 2003. The shufflon of Salmonella enterica serovar Typhi regulates type IVB pilus-mediated bacterial self-association. Infect. Immun. 71:1141-1146.
37. Mrocienski-Wildey, M. J., J. L. Di Fabio, and F. C. Cabello. 1989. Invasion and lysis of HeLa cell monolayers by Salmonella typhi: the role of lipopolysaccharide. Microb. Pathog. 6:143-152.
38. Murray, G. L., S. R. Attridge, and R. Morona. 2003. Regulation of Salmonella typhimurium lipopolysaccharide O antigen chain length is required for virulence: identification of FepE as a second Wzz. Mol. Microbiol. 47:1395-1406.
39. fepE- regulated very long O antigen chains. Microbes Infect. 7:1296-1304.
40. Nevola, J., B. A. D. Stocker, D. Laux, and P. Cohen. 1985. Colonization of a mouse intestine by a virulent Salmonella typhimurium strain and its lipopolysaccharide-defective mutants. Infect. Immun. 50:152-159.
41. Parker, C. T., A. W. Kloser, C. A. Schnaitman, M. A. Stein, S. Gottesman, and B. W. Gibson. 1992. Role of the rfaG and rfaP genes in determining the lipopolysaccharide core structure and cell surface properties of Escherichia coli. J. Bacteriol. 174:2525-2538.
42. Parkhill, J., G. Dougan, K. D. James, N. R. Thomson, D. Pickard, J. Wain, C. Churcher, K. Mungall, S. D. Bentley, M. T. G. Holden, M. Sebaihia, S. Baker, D. Basham, K. Brooks, T. Chillingworth, P. Connerton, A. Cronin, P. Davis, R. M. Davies, L. Dowd, N. White, J. Farrar, T. Feltwell, N. Hamlin, A. Haque, T. T. Hien, S. Holroyd, K. Jagels, A. Krogh, T. S. Larsen, S. Leather, S. Moule, P. O'Gaora, C. Parry, M. Quail, K. Rutherford, M. Simmonds, J. Skelton, K. Stevens, S. Whitehead, and B. G. Barrell. 2001. The complete genome sequence of a multidrug resistant Salmonella enterica serovar Typhi CT18. Nature 413:848-852.
43. Patel, J. C., and J. E. Galán. 2005. Manipulation of the host actin cytoskeleton by Salmonella-all in the name of entry. Curr. Opin. Microbiol. 8:10-15.
44. Pier, G., M. Grout, T. Zaidi, G. Meluleni, S. S. Mueschenborn, G. Banting, R. Ratcliff, M. J. Evans, and W. H. Colledge. 1998. Salmonella typhi uses CFTR to enter intestinal epithelial cells. Nature 393:79-82.
45. Pradel, E., and C. A. Schnaitman. 1991. Effect of rfaH (sfrB) and temperature on expression of rfa genes of Escherichia coli K-12. J. Bacteriol. 173:6428-6431.
46. Raetz, C. R., and C. Whitfield. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700.
47. Rojas, G., S. Saldías, M. Bittner, M. Zaldívar, and I. Contreras. 2001. The rfaH gene, which affects lipopolysaccharide synthesis in Salmonella enterica Serovar Typhi, is differentially expressed during the bacterial growth phase. FEMS Microbiol. Lett. 204:123-128.
48. Rowe, P. S. N., and P. M. Meadow. 1983. Structure of the core oligosaccharide from the lipopolysaccharide of Pseudomonas aeruginosa and its defective mutants. Eur. J. Biochem. 132:329-337.
49. Saldías, M. S. 2004. Functional analysis of WbaP, essential enzyme in the biosynthesis of O-antigen in Salmonella enterica. Ph.D. thesis. Universidad de Chile, Santiago, Chile.
50. St. Geme, J. W., III. 2002. Molecular and cellular determinants of non-typeable Haemophilus influenzas adherence and invasion. Cell. Microbiol. 4:191-200.
51. Stone, B. J., C. M. García, J. L. Badger, T. Hassett, R. I. Smith, and V. L. Miller. 1992. Identification of novel loci affecting entry of Salmonella enteritidis into eukaryotic cells. J. Bacteriol. 174:3945-3952.
52. Townsend, S. M., N. Kramer, R. Edwards, S. Baker, N. Hamlin, M. Simmonds, K. Stevens, S. Maloy, J. Parkhill, G. Dougan, and J. Bäumler. 2001. Salmonella enterica serovar Typhi possesses a unique repertoire of fimbrial gene sequences. Infect. Immun. 69:2894-2901.
53. Tsai, C. M., and C. E. Frasch. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119:115-119.
54. Tsui, I. S. M., C. M. C. Yip, J. Hackett, and C. Morris. 2003. The type IVB pili of Salmonella enterica serovar Typhi bind to the cystic fibrosis transmembrane conductance regulator. Infect. Immun. 71:6049-6050.
55. Wain, J., D. House, D. Pickard, G. Dougan, and G. Frankel. 2001. Acquisition of virulence-associated factors by the enteric pathogens Escherichia coli and Salmonella enterica. Philos. Trans. R. Soc. London B 356:1-8.
56. Wain, J., D. House, J. Parkhill, C. Parry, and G. Dougan. 2002. Unlocking the genome of the human typhoid bacillus. Lancet Infect. Dis. 2:163-170.
57. Wang, L., and P. R Reeves. 1994. Involvement of the galactosyl-1- phosphate transferase encoded by the Salmonella enterica rfbP gene in O-antigen subunit processing. J. Bacteriol. 176:4348-4356.
58. Wang, L., S. Jensen, R. Hallman, and P. R. Reeves. 1998. Expression of the O antigen gene cluster is regulated by RfaH through the JUMPstart sequence. FEMS Microbiol. Lett. 165:201-206.
59. West, N. P., P. Sansonetti, J. Mounier, R M. Exley, C. Parsot, S. Guadagnini, M.-C. Prévost, A. Prochnicka-Chalufour, M. Delepierre, M. Tanguy, and C. M. Tang. 2005. Optimization of virulence functions through glucosylation of Shigella LPS. Science 307:1313-1317.
60. Wollin, R., S. Greeger, L. I. Rothfield, B. A. D. Stocker, and A. A. Lindberg. 1983. Salmonella typhimurium mutants defective in UDP D-galactose: lipopolysaccharide α-1,6-D-galactosyl-transferase. J. Biol. Chem. 258:3769-3774.
61. Young, D., T. Hussell, and G. Dougan. 2002. Chronic bacterial infections: living with unwanted guests. Nat. Immunol. 3:1026-1032.
62. Zaidi, T. S., S. M. J. Fleiszig, M. J. Preston, J. B. Goldberg, and G. Pier. 1996. Lipopolysaccharide outer core is a ligand for corneal cell binding and ingestion of Pseudomonas aeruginosa. Investig. Ophthmal. Vis. Sci. 37:976-986.
63. Zhang, X.-L., I. S. M. Tsiu, C. M. C. Yip, A. W. Y. Fung, D. K.-H. Wong, X. Dai, Y. Yang, J. Hackett, and C. Morris. 2000. Salmonella enterica serovar Typhi uses type IVB pili to enter human intestinal epithelial cells. Infect. Immun. 68:3067-3073.