The ShdA adhesin binds to the cationic cradle of the fibronectin 13FnIII repeat module: Evidence for molecular mimicry of heparin binding

Molecular Microbiology

Volumn 52, Issue 2, 2004, Pages 345-355

  Kingsley, Robert A ^a   Keestra, A Marijke ^a   De Zoete, Marcel R ^a   Bäumier, Andreas J ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; BUFFER; COLLAGEN TYPE 1; FIBRONECTIN; HEPARIN; SCLEROPROTEIN; SHDA PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; CATTLE; CONTROLLED STUDY; FROG; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; SALMONELLA ENTERICA;

ANIMALS; ANTITHROMBIN III; BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; CATIONS; COLLAGEN; FIBRONECTINS; HEPARIN; HUMANS; MODELS, MOLECULAR; MOLECULAR MIMICRY; MUTAGENESIS, SITE-DIRECTED; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SALMONELLA TYPHIMURIUM; STRUCTURE-ACTIVITY RELATIONSHIP;

ANURA; BACTERIA (MICROORGANISMS); BOS TAURUS; NEGIBACTERIA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

EID: 1942501147     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.03995.x     Document Type: Article

References (46)

1. Borsi, L., Castellani, P., Balza, E., Siri, A., Pellecchia, C., De Scalzi, F., and Zardi, L. (1986) Large-scale procedure for the purification of fibronectin domains. Anal Biochem 155: 335-345.
2. Busby, T.F., Argraves, W.S., Brew, S.A., Pechik, I., Gilliland, G.L., and Ingham, K.C. (1995) Heparin binding by fibronectin module III-13 involves six discontinuous basic residues brought together to form a cationic cradle. J Biol Chem 270: 18558-18562.
3. Christopher, A.J. (1998) spock. The Structural Properties Observation and Calculation Kit Program Manual. College Station, TX: The center for macromolecular design, Texas A & M University.
4. Conrad, H.E. (1998) Heparin-Binding Proteins. London: Academic Press.
5. 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.
6. 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 Prot 63: 1648-1653.
7. Davies, P.R., Morrow, W.E., Jones, F.T., 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.
8. DeSimone, D.W., Spiegel, E., and Spiegel, M. (1985) The biochemical identification of fibronectin in the sea urchin embryo. Biochem Biophys Res Commun 133: 183-188.
9. Hamburger, Z.A., Brown, M.S., Isberg, R.R., and Bjorkman, P.J. (1999) Crystal structure of invasin: a bacterial integrin-binding protein. Science 286: 291-295.
10. Henderson, I.R., and Nataro, J.P. (2001) Virulence functions of autotransporter proteins. Infect Immun 69: 1231-1243.
11. 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.
12. Hook, M., Bjork, I., Hopwood, J., and Lindahl, U. (1976) Anticoagulant activity of heparin: separation of high-activity and low-activity heparin species by affinity chromatography on immobilized antithrombin. FEBS Lett 66: 90-93.
13. Hynes, R.O., Schwarzbauer, J.E., and Tamkun, J.W. (1984) Fibronectin: a versatile gene for a versatile protein. Ciba Found Symp 108: 75-92.
14. Jonsson, K., Signas, C., Muller, H.P., and Lindberg, M. (1991) Two different genes encode fibronectin binding proteins in Staphylococcus aureus. The complete nucleotide sequence and characterization of the second gene. Eur J Biochem 202: 1041-1048.
15. Kapila, Y.L., Niu, J., and Johnson, P.W. (1997) The high affinity heparin-binding domain and the V region of fibronectin mediate invasion of human oral squamous cell carcinoma cells in vitro. J Biol Chem 272: 18932-18938.
16. Kapila, Y., Doan, D., Tafolla, E., and Fletterick, R. (2001) Three-dimensional structural analysis of fibronectin heparin-binding domain mutations. J Cell Biochem 81: 156-161.
17. Kingsley, R.A., van Amsterdam, K., Kramer, N., and 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.
18. Kingsley, R.A., Santos, R.L., Keestra, A.M., Adams, L.G., and Baumler, 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.
19. Kingsley, R.A., Humphries, A.D., Weening, E., de Zoete, M., Winter, S., Papaconstantinopoulou, A., Dougan, G., and Bäumler, A.J. (2003) Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype Typhimurium. Infect Immun 71: 629-640.
20. Lindgren, P.E., McGavin, M.J., Signas, C., Guss, B., Gurusiddappa, S., Hook, M., and Lindberg, M. (1993) Two different genes coding for fibronectin-binding proteins from Streptococcus dysgalactiae. The complete nucleotide sequences and characterization of the binding domains. Eur J Biochem 214: 819-827.
21. McDonagh, R.P., McDonagh, J., Petersen, T.E., Thogersen, H.C., Skorstengaard, K., Sottrup-Jensen, L., et al. (1981) Amino acid sequence of the factor XIIIa acceptor site in bovine plasma fibronectin. FEBS Lett 127: 174-178.
22. 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.
23. Mosher, D.F. (1989) Fibronectin. New York: Academic Press.
24. Nolan, L.K., Giddings, C.W., Boland, E.W., Steffen, D.J., Brown, J., and Misek, A. (1995) Detection and characterization of Salmonella typhimurium from a dairy herd in North Dakota. Vet Res Commun 19: 3-8.
25. Nordenman, B., Danielsson, A., and Bjork, I. (1978) The binding of low-affinity and high-affinity heparin to antithrombin. Fluorescence studies. Eur J Biochem 90: 1-6.
26. Pande, H., Calaycay, J., Lee, T.D., Legesse, K., Shively, J.E., Siri, A., et al. (1987) Demonstration of structural differences between the two subunits of human-plasma fibronectin in the carboxy-terminal heparin-binding domain. Eur J Biochem 162: 403-411.
27. Petersen, T.E., Thogersen, H.C., Skorstengaard, K., Vibe-Pedersen, K., Sahl, P., Sottrup-Jensen, L., and Magnusson, S. (1983) Partial primary structure of bovine plasma fibronectin: three types of internal homology. Proc Natl Acad Sci USA 80: 137-141.
28. Rabenstein, D.L. (2002) Heparin and heparan sulfate: structure and function. Nat Prod Rep 19: 312-331.
29. San Antonio, J.D., Lander, A.D., Karnovsky, M.J., and Slayter, H.S. (1994) Mapping the heparin-binding sites on type I collagen monomers and fibrils. J Cell Biol 125: 1179-1188.
30. Schwarz-Linek, U., Werner, J.M., Pickford, A.R., Gurusiddappa, S., Kim, J.H., Pilka, E.S., et al. (2003) Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423: 177-181.
31. Sekiguchi, K., and Hakomori, S. (1983) Domain structure of human plasma fibronectin. Differences and similarities between human and hamster fibronectins. J Biol Chem 258: 3967-3973.
32. Sekiguchi, K., Siri, A., Zardi, L., and Hakomori, S. (1983) Differences in domain structure between pericellular matrix and plasma fibronectins as revealed by domain-specific antibodies combined with limited proteolysis and S-cyanylation: a preliminary note. Biochem Biophys Res Commun 116: 534-540.
33. Sharma, A., Askari, J.A., Humphries, M.J., Jones, E.Y., and Stuart, D.I. (1999) Crystal structure of a heparin-and integrin-binding segment of human fibronectin. Embo J 18: 1468-1479.
34. Signas, C., Raucci, G., Jonsson, K., Lindgren, P.E., Anantharamaiah, G.M., Hook, M., and Lindberg, M. (1989) Nucleotide sequence of the gene for a fibronectin-binding protein from Staphylococcus aureus: use of this peptide sequence in the synthesis of biologically active peptides. Proc Natl Acad Sci USA 86: 699-703.
35. Skorstengaard, K., Thogersen, H.C., Vibe-Pedersen, K., Petersen, T.E., and Magnusson, S. (1982) Purification of twelve cyanogen bromide fragments from bovine plasma fibronectin and the amino acid sequence of eight of them. Overlap evidence aligning two plasmic fragments, internal homology in gelatin-binding region and phosphorylation site near C terminus. Eur J Biochem 128: 605-623.
36. Skorstengaard, K., Thogersen, H.C., and Petersen, T.E. (1984) Complete primary structure of the collagen-binding domain of bovine fibronectin. Eur J Biochem 140: 235-243.
37. Skorstengaard, K., Jensen, M.S., Petersen, T.E., and Magnusson, S. (1986a) Purification and complete primary structures of the heparin-, cell-, and DNA-binding domains of bovine plasma fibronectin. Eur J Biochem 154: 15-29.
38. Skorstengaard, K., Jensen, M.S., Sahl, P., Petersen, T.E., and Magnusson, S. (1986b) Complete primary structure of bovine plasma fibronectin. Eur J Biochem 161: 441-453.
39. Stebbins, C.E., and Galan, J.E. (2001) Structural mimicry in bacterial virulence. Nature 412: 701-705.
40. Talay, S.R., Valentin-Weigand, P., Timmis, K.N., and Chhatwal, G.S. (1994) Domain structure and conserved epitopes of Sfb protein, the fibronectin-binding adhesin of Streptococcus pyogenes. Mol Microbiol 13: 531-539.
41. Vibe-Pedersen, K., Sahl, P., Skorstengaard, K., and Petersen, T.E. (1982) Amino acid sequence of a peptide from bovine plasma fibronectin containing a free sulfhydryl group (cysteine). FEBS Lett 142: 27-30.
42. 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 Prot 64: 3-11.
43. 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.
44. 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.
45. Yamada, K.M., Kennedy, D.W., Kimata, K., and Pratt, R.M. (1980) Characterization of fibronectin interactions with glycosaminoglycans and identification of active proteolytic fragments. J Biol Chem 255: 6055-6063.
46. Zardi, L., Carnemolla, B., Balza, E., Borsi, L., Castellani, P., Rocco, M., and Siri, A. (1985) Elution of fibronectin proteolytic fragments from a hydroxyapatite chromatography column. A simple procedure for the purification of fibronectin domains. Eur J Biochem 146: 571-579.