Salmonella enterica serotype Typhimurium MisL is an intestinal colonization factor that binds fibronectin

Molecular Microbiology

Volumn 57, Issue 1, 2005, Pages 196-211

  Dorsey, Caleb W ^a   Laarakker, Marijke C ^a   Humphries, Andrea D ^a   Weening, Eric H ^a   Bäumler, Andreas J ^a,b  

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

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL DNA; BINDING PROTEIN; CARBENICILLIN; COLLAGEN TYPE 4; FIBRONECTIN; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; KANAMYCIN; MISL PROTEIN; OUTER MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL OUTER MEMBRANE; BACTERIUM ADHERENCE; BACTERIUM CULTURE; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; GRAM NEGATIVE BACTERIUM; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PURIFICATION; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEROTYPE;

ANIMALS; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BINDING SITES; CELLS, CULTURED; EPITHELIAL CELLS; FEMALE; FIBRONECTINS; GLUTATHIONE TRANSFERASE; HUMANS; INTESTINES; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED BALB C; RECOMBINANT FUSION PROTEINS; SALMONELLA INFECTIONS; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM;

ESCHERICHIA COLI; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

EID: 21244452786     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04666.x     Document Type: Article

References (43)

1. Blanc-Potard, A.B., Solomon, F., Kayser, J., and Groisman, E.A. (1999) The SPI-3 pathogenicity island of Salmonella enterica. J Bacteriol 181: 998-1004.
2. Collinson, S.K., Doig, P.C., Doran, J.L., Clouthier, S., Trust, T.J., and Kay, W.W. (1993) Thin, aggregative fimbriae mediate binding of Salmonella enteritidis to fibronectin. J Bacteriol 175: 12-18.
3. Dahl, J., Wingstrand, A., Nielsen, B., and Baggesen, D.L. (1997)-Elimination of Salmonella typhimurium infection by the strategic movement of pigs. Vet Rec 140: 679-681.
4. Dargatz, D.A., Fedorka-Cray, P.J., Ladely, S.R., and Ferris, K.E. (2000) Survey of Salmonella serotypes shed in feces of beef cows and their antimicrobial susceptibility patterns. J Food Protect 63: 1648-1653.
5. Davies, P.R., Morrow, W.E., Jones, FT., Deen, J., Fedorka-Cray, P.J., and Gray, J.T. (1997) Risk of shedding Salmonella organisms by market-age hogs in a barn with open-flush gutters. J Am Vet Med Assoc 210: 386-389.
6. Dehio, C., and Meyer, M. (1997) Maintenance of broad-host-range incompatibility group P and group Q plasmids and transposition of Tn5 in Bartonella henselae following conjugal plasmid transfer from Escherichia coli. J Bacteriol 179: 538-540.
7. Eriksson, S., Lucchini, S., Thompson, A., Rhen, M., and Hinton, J.C. (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47: 103-118.
8. Fields, P.I., Swanson, R.V., Haidaris, G.G., and Heffron, F. (1986) Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 83: 5189-5193.
9. Ghosh, S., Mittal, A., Vohra, H., and Ganguly, N.K. (1996) Interaction of a rat intestinal brush border membrane glycoprotein with type-1 fimbriae of Salmonella typhimurium. Mol Cell Biochem 158: 125-131.
10. Groisman, E.A., Saier, M.H., and Ochman, H. (1992) Horzontal transfer of a phosphatase gene as evidence for mosaic structure of the Salmonella genome. EMBO J 11: 1309-1316.
11. Gruber, A., and Zingales, B. (1995) Alternative method t3 remove antibacterial antibodies from antisera used for screening of expression libraries. Biotechniques 19: 28-30.
12. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
13. Hantke, K. (1981) Regulation of the ferric iron transport in Escherichia coli K12: Isolation of a constitutive mutant. Mol Gen Genet 182: 288-292.
14. Henderson, I.R., and Nataro, J.P. (2001) Virulence functions of autotransporter proteins. Infect Immun 69: 1231-1243.
15. Henderson, I.R., Navarro-Garcia, F., and Nataro, J.P. (1998) The great escape: structure and function of the autotransporter proteins. Trends Microbiol 6: 370-378.
16. Henderson, I.R., Cappello, R., and Nataro, J.P. (2000) Autotransporter proteins, evolution and redefining protein secretion. Trends Microbiol 8: 529-532.
17. Hoiseth, S.K., and Stocker, B.A.D. (1981) Aromatic-dependent Salmonella typhimurium are non-virulerit and effective as live oral vaccines. Nature 291: 238-239.
18. 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.
19. Kinder, S.A., Badger, J.L., Bryant, G.O., Pepe, U.C., and Miller, V.L. (1993) Cloning of the Yenl restriction endonuclease and methyltransferase from Yersinia enterocolitica serotype O:8 and construction of a transformable R-M+ mutant. Gene 136: 271-275.
20. Kingsley, R.A., van Amsterdam, K., Kramer, N., and Bäumler, 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.
21. Kingsley, R.A., Santos, R.L., Keestra, A.M., Adams, L.G., and Bäumler, A.J. (2002) Salmonella enterica serotype Typhimurium ShdA is an outer membrane fibronectin-binding protein that is expressed in the intestine. Mol Microbiol 43: 895-905.
22. 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.
23. Kingsley, R.A., Keestra, A.M., de Zoete, M.R., and Bäumler, A.J. (2004a) The ShdA adhesin binds to the cationic cradle of the fibronectin 13FnIII repeat module: evidence for molecular mimicry of heparin binding. Mol Microbiol 52: 345-355.
24. Kingsley, R.A., Abi Ghanem, D., Puebla-Osorio, N., Keestra, A.M., Berghman, L., and Bäumler, A.J. (2004b) Fibronectin binding to the Salmonella enterica serotype Typhimurium ShdA autotransporter protein is inhibited by a monoclonal antibody recognizing the A3 repeat. J Bacteriol 186: 4931-4939.
25. Kukkonen, M., Raunio, T., Virkola, R., Lahteenmaki, K., Makela, P.H., Klemm, P., et al. (1993) Basement membrane carbohydrate as a target for bacterial adhesion: binding of type I fimbriae of Salmonella enterica and Escherichia coli to laminin. Mol Microbiol 7: 229-237.
26. Lammers, A., Nuijten, P.J., and Smith, H.E. (1999) The fibronectin binding proteins of Staphylococcus aureus are required for adhesion to and invasion of bovine mammary gland cells. FEMS Microbiol Lett 180: 103-109.
27. Lilleengen, K. (1948) Typing of Salmonella typhimurium by means of bacteriophage. Acta Pathol Microbiol Scand Suppl 77: 2-125.
28. McLaren, I.M., and Wray, C. (1991) Epidemiology of Salmonella typhimurium infection in calves: persistence of salmonellae on calf units. Vet Rec 129: 461-462.
29. Miller, J.H. (1972) Experiments in Molecular Genetics. New York: Cold Spring Harbor Laboratory Press.
30. Monack, D.M., Bouley, D.M., and Falkow, S. (2004) Salmonella typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp1+/ + mice and can be reactivated by IFNgamma neutralization. J Exp Med 199: 231-241.
31. Monteville, M.R., and Konkel, M.E. (2002) Fibronectin-facilitated invasion of T84 eukaryotic cells by Campylobacter jejuni occurs preferentially at the basolateral cell surface. Infect Immun 70: 6665-6671.
32. Morgan, E., Campbell, J., Rowe, S., Bispham, J., Stevens, M., Bowen, A., et al. (2004) Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol Microbiol 54: 994-1010.
33. Naughton, P.J., Grant, G., Bardocz, S., Allen-Vercoe, E., Woodward, M. J., and Pusztai, A. (2001) Expression of type 1 fimbriae (SEF 21) of Salmonella enterica serotype Enteritidis in the early colonisation of the rat intestine. J Med Microbiol 50: 191-197.
34. Oomen, C.J., Van Ulsen, P., Van Gelder, P., Feijen, M., Tommassen, J., and Gros, P. (2004) Structure of the translocator domain of a bacterial autotransporter. EMBO J 23: 1257-1266.
35. Raffatellu, M., Wilson, R.P., Chessa, D., Andrews-Polymenis, H., Tran, Q.T., Lawhon, S., et al. (2005) SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype Typhimurium invasion of epithelial cells. Infect Immun 73: 146-154.
36. Schneider, H.A., and Zinder, N.D. (1956) Nutrition of the host and natural resistance to infection. V. An improved assay employing genetic markers in the double strain inoculation test. J Exp Med 103: 207-223.
37. Schorey, U.S., Li, Q., McCourt, D.W., Bong-Mastek, M., Clark-Curtiss, U.E., Ratliff, T.L., and Brown, E.J. (1995) A Mycobacterium leprae gene encoding a fibronectin binding protein is used for efficient invasion of epithelial cells and Schwann cells. Infect Immun 63: 2652-2657.
38. Secott, T.E., Lin, T.L., and Wu, C.C. (2002) Fibronectin attachment protein is necessary for efficient attachment and invasion of epithelial cells by Mycobacterium avium subsp. paratuberculosis. Infect Immun 70: 2670-2675.
39. Sukupolvi, S., Lorenz, R.G., Gordon, J.I., Bian, Z., Pfeifer, J.D., Normark, S.J., and Rhen, M. (1997) Expression of thin aggregative fimbriae promotes interaction of Salmonella typhimurium SR-11 with mouse small intestinal epithelial cells. Infect Immun 65: 5320-5325.
40. Walia, B., Castaneda, F.E., Wang, L., Kolachala, V.L., Bajaj, R., Roman, J., et al. (2004) Polarized fibronectin secretion induced by adenosine regulates bacterial-epithelial interaction in human intestinal epithelial cells. Biochem J 382: 589-596.
41. Wells, S.J., Fedorka-Cray, P.J., Dargatz, D.A., Ferris, K., and Green, A. (2001) Fecal shedding of Salmonella spp. by dairy cows on farm and at cull cow markets. J Food Protect 64: 3-11.
42. Wray, C., Todd, J.N., and Hinton, M. (1987) Epidemiology of Salmonella typhimurium infection in calves: excretion of S typhimurium in the faeces of calves in different management systems. Vet Rec 121: 293-296.
43. Wray, C., Todd, N., McLaren, I.M., and Beedell, Y.E. (1991) The epidemiology of Salmonella in calves: the role of markets and vehicles. Epidemiol Infect 107: 521-525.