'Form variation' of the O12 antigen is critical for persistence of Salmonella Typhimurium in the murine intestine

Molecular Microbiology

Volumn 70, Issue 5, 2008, Pages 1105-1119

  Bogomolnaya, Lydia M ^a   Santiviago, Carlos A ^b   Yang, Hee Jeong ^a   Baumler, Andreas J ^c   Andrews Polymenis, Helene L ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CHILE   (Chile)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN O12; GALACTOSE; MEMBRANE PROTEIN; O ANTIGEN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE LOCATION; GENETIC CODE; INTESTINE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM; SEROTYPE; SHIGELLA;

ANIMALS; CACO-2 CELLS; CLONING, MOLECULAR; DNA, BACTERIAL; GENE DELETION; GENES, BACTERIAL; GENOMIC ISLANDS; HUMANS; INTESTINES; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED CBA; MUTATION; O ANTIGENS; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SPECIES SPECIFICITY; VIRULENCE;

AVES; BACTERIA (MICROORGANISMS); MAMMALIA; MURINAE; MUS; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SHIGELLA;

EID: 55349099871     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06461.x     Document Type: Article

References (53)

1. Aldridge, P., Karlinsey, J.E., Becker, E., Chevance, F.F. Hughes, K.T. (2006) Flk prevents premature secretion of the anti-sigma factor FlgM into the periplasm. Mol Microbiol 60 : 630 643.
2. Allison, G.E. Verma, N.K. (2000) Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri. Trends Microbiol 8 : 17 23.
3. Althouse, C., Patterson, S., Fedorka-Cray, P. Isaacson, R.E. (2003) Type 1 fimbriae of Salmonella enterica serovar Typhimurium bind to enterocytes and contribute to colonization of swine in vivo. Infect Immun 71 : 6446 6452.
4. Bajaj, V., Lucas, R.L., Hwang, C. Lee, C.A. (1996) Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental factors is mediated by control of hilA expression. Mol Microbiol 22 : 703 714.
5. Callaway, T.R., Morrow, J.L., Edrington, T.S., Genovese, K.J., Dowd, S., Carroll, J., et al. (2006) Social stress increases fecal shedding of Salmonella typhimurium by early weaned piglets. Curr Issues Intest Microbiol 7 : 65 71.
6. CDC (1999) Salmonella Surveillance: Annual Tabulation Summary, 1998. Atlanta, GA : US Department of Health and Human Services, CDC.
7. Ciucanu, I. Kerek, F. (1984) A simple and rapid method for the permethylation of carbohydrates. Carbohydr Res 131 : 209 217.
8. Datsenko, K.A. Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97 : 6640 6645.
9. DePamphilis, M.L. Adler, J. (1971) Attachment of flagellar basal bodies to the cell envelope: specific attachment to the outer, lipopolysaccharide membrane and the cyoplasmic membrane. J Bacteriol 105 : 396 407.
10. Dorsey, C.W., Laarakker, M.C., Humphries, A.D., Weening, E.H. Baumler, A.J. (2005) Salmonella enterica serotype Typhimurium MisL is an intestinal colonization factor that binds fibronectin. Mol Microbiol 57 : 196 211.
11. Erickson, K.D. Detweiler, C.S. (2006) The Rcs phosphorelay system is specific to enteric pathogens/commensals and activates ydeI, a gene important for persistent Salmonella infection of mice. Mol Microbiol 62 : 883 894.
12. Fields, P.I., Swanson, R.V., Haidaris, C.G. Heffron, F. (1986) Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 83 : 5189 5193.
13. Galán, J.E. Curtiss, R., III (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci USA 86 : 6383 6387.
14. Galan, J.E. Curtiss, R., 3rd (1990) Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect Immun 58 : 1879 1885.
15. Guan, S., Bastin, D.A. Verma, N.K. (1999) Functional analysis of the O antigen glucosylation gene cluster of Shigella flexneri bacteriophage SfX. Microbiology 145 : 1263 1273.
16. Hansen-Wester, I. Hensel, M. (2002) Genome-based identification of chromosomal regions specific for Salmonella spp. Infect Immun 70 : 2351 2360.
17. Helander, I.M., Moran, A.P. Makela, P.H. (1992) Separation of two lipopolysaccharide populations with different contents of O-antigen factor 122 in Salmonella enterica serovar typhimurium. Mol Microbiol 6 : 2857 2862.
18. Hensel, M., Shea, J.E., Gleeson, C., Jones, M.D., Dalton, E. Holden, D.W. (1995) Simultaneous identification of bacterial virulence genes by negative selection. Science 269 : 400 403.
19. Huan, P.T., Bastin, D.A., Whittle, B.L., Lindberg, A.A. Verma, N.K. (1997a) Molecular characterization of the genes involved in O-antigen modification, attachment, integration and excision in Shigella flexneri bacteriophage SfV. Gene 195 : 217 227.
20. Huan, P.T., Whittle, B.L., Bastin, D.A., Lindberg, A.A. Verma, N.K. (1997b) Shigella flexneri type-specific antigen V: cloning, sequencing and characterization of the glucosyl transferase gene of temperate bacteriophage SfV. Gene 195 : 207 216.
21. Humphries, A.D., Raffatellu, M., Winter, S., Weening, E.H., Kingsley, R.A., Droleskey, R., et al. (2003) The use of flow cytometry to detect expression of subunits encoded by 11 Salmonella enterica serotype Typhimurium fimbrial operons. Mol Microbiol 48 : 1357 1376.
22. Hurd, H.S., McKean, J.D., Griffith, R.W., Wesley, I.V. Rostagno, M.H. (2002) Salmonella enterica infections in market swine with and without transport and holding. Appl Environ Microbiol 68 : 2376 2381.
23. Iseki, S. Kashiwagi, K. (1955) Induction of somatic antigen 1 by bacteriophage in Salmonella B group. Proc Jpn Acad 31 : 558 563.
24. Iseki, S. Kashiwagi, K. (1959) Conversion of type antigen IV in Shigella flexneri by bacteriophage. Proc Jpn Acad 35 : 407 412.
25. Kauffmann, F.A. (1941) A typhoid variant and a new serological variation in the Salmonella group. J Bacteriol 41 : 127 140.
26. Kelterborn, E. (1967) Salmonella-species. First Isolations, Names and Occurrence. Karl-Marx-Stadt : S. Hirzel Verlag Leipzig.
27. Kinder, S.A, Badger, J.L., Bryant, G.O., Pepe, J.C. Miller, V.L. (1993) Cloning of the YenI restriction endonulease and methyltransferase from Yersinia enterocolitica serothype 0:8 and construction of a transformable R-M+ mutant. Gene 136 : 271 275.
28. Kingsley, R.A., van Amsterdam, K., Kramer, N. Baumler, A.J. (2000) The shdA gene is restricted to serotypes of Salmonella enterica subspecies I and contributes to efficient and prolonged fecal shedding. Infect Immun 68 : 2720 2727.
29. Kingsley, R.A., Humphries, A.D., Weening, E.H., De Zoete, M.R., Winter, S., Papaconstantinopoulou, A., et al. (2003) Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype typhimurium: identification of intestinal colonization and persistence determinants. Infect Immun 71 : 629 640.
30. Lawley, T.D., Chan, K., Thompson, L.J., Kim, C.C., Govoni, G.R. Monack, D.M. (2006) Genome-wide screen for salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2 : e11.
31. McClelland, M., Sanderson, K.E., Spieth, J., Clifton, S.W., Latreille, P., Courtney, L., et al. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413 : 852 856.
32. Makela, P.H. (1973) Glucosylation of lipopolysaccharide in Salmonella: mutants negative for O antigen factor 1221. J Bacteriol 116 : 847 856.
33. Makela, P.H. Makela, O. (1966) Salmonella antigen 12-2: genetics of form variation. Ann Med Exp Biol Fenn 44 : 310 317.
34. Makela, P.H., Hovi, M., Saxen, H., Valtonen, M.V. Valtonen, V.V. (1988) Salmonella, complement, and mouse macrophages. Immunol Lett 19 : 217 222.
35. Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., et al. (1999) Food-related illness and death in the United States. Emerg Infect Dis 5 : 607 625.
36. Morgan, E., Campbell, J.D., Rowe, S.C., Bispham, J., Stevens, M.P., Bowen, A.J., et al. (2004) Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol Microbiol 53 : 994 1010.
37. Nikaido, K. Nikaido, H. (1971) Glucosylation of lipopolysaccharide in Salmonella: biosynthesis of O antigen factor 12-2 (II. Structure of the lipid intermediate). J Biol Chem 246 : 3912 3919.
38. Nikaido, H., Nikaido, K., Nakae, T. Makela, P.H. (1971) Glucosylation of lipopolysaccharide in Salmonella: biosynthesis of O antigen factor 12 2. I. Over-all reaction. J Biol Chem 246 : 3902 3911.
39. Porwollik, S., Wong, R.M. McClelland, M. (2002) Evolutionary genomics of Salmonella: gene acquisitions revealed by microarray analysis. Proc Natl Acad Sci USA 99 : 8956 8961.
40. Prasadarao, N.V., Srivastava, P.K., Rudrabhatla, R.S., Kim, K.S., Huang, S.H. Sukumaran, S.K. (2003) Cloning and expression of the Escherichia coli K1 outer membrane protein A receptor, a gp96 homologue. Infect Immun 71 : 1680 1688.
41. Reuhs, B.L., Geller, D.P., Kim, J.S., Fox, J.E., Kolli, V.S. Pueppke, S.G. (1998) Sinorhizobium fredii and Sinorhizobium meliloti produce structurally conserved lipopolysaccharides and strain-specific K antigens. Appl Environ Microbiol 64 : 4930 4938.
42. Rundell, K. Shuster, C.W. (1975) Membrane-associated nucleotide sugar reactions: influence of mutations affecting lipopolysaccharide on the first enzyme of O-antigen synthesis. J Bacteriol 123 : 928 936.
43. Russel, M. Kazmierczak, B. (1993) Analysis of the structure and subcellular location of filamentous phage pIV. J Bacteriol 175 : 3998 4007.
44. Sambrook, J. Russell, D. (2001) Molecular Cloning: A Laboratory Manual. Woodbury, NY : Cold Spring Harbor Laboratory Press.
45. Tinelli, R. Staub, A.M. (1960) [Immunochemical study of Salmonella. 7. Study of the products formed by the controlled acid hydrolysis of the polysaccharide extracted from S. typhi. Part 1. Analysis of antigen 0 12 in the Kauffmann-White scheme]. Bull Soc Chim Biol 42 : 583 599.
46. Uzzau, S., Figueroa-Bossi, N., Rubino, S. Bossi, L. (2001) Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci USA 98 : 15264 15269.
47. Valtonen, V.V. Makela, P.H. (1971) The effect of lipopolysaccharide modification - antigenic factors 1,5,12 2 and 27 - on the virulence of salmonella strains for mice. J Gen Microbiol 69 : 107 115.
48. Vernikos, G.S. Parkhill, J. (2006) Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 22 : 2196 2203.
49. Weening, E.H., Barker, J.D., Laarakker, M.C., Humphries, A.D., Tsolis, R.M. Baumler, A.J. (2005) The Salmonella enterica serotype Typhimurium lpf, bcf, stb, stc, std, and sth fimbrial operons are required for intestinal persistence in mice. Infect Immun 73 : 3358 3366.
50. West, N.P., Sansonetti, P., Mounier, J., Exley, R.M., Parsot, C., Guadagnini, S., et al. (2005) Optimization of virulence functions through glucosylation of Shigella LPS [see comment]. Science 307 : 1313 1317.
51. Westphal, O. Jann, K. (1965) Bacterial lipopolysaccharides. Extraction with phenol-water and further applications of the procedure. In Methods in Carbohydrate Chemistry, Vol. 5. Whistler, R.C. (ed.). New York : Academic Press, p. 83.
52. Xu, M., Struck, D.K., Deaton, J., Wang, I.N. Young, R. (2004) A signal-arrest-release sequence mediates export and control of the phage P1 endolysin. Proc Natl Acad Sci USA 101 : 6415 6420.
53. York, W.S., Darvill, M., McNeil, T., Stevenson, T. Albersheim, P. (1985) Isolation and characterization of plant cell walls and cell wall components. Methods Enzymol 118 : 3 40.