Domains in the S-layer protein CbsA of Lactobacillus crispatus involved in adherence to collagens, laminin and lipoteichoic acids and in self-assembly

Molecular Microbiology

Volumn 46, Issue 2, 2002, Pages 381-394

  Antikainen, Jenni ^a   Anton, Lena ^a   Sillanpää, Jouko ^a   Korhonen, Timo K ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; LAMININ; LIPOTEICHOIC ACID; POLYMER; PROTEIN CBSA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL TISSUE; ARTICLE; BACTERIAL CELL WALL; BACTERIUM ADHERENCE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CHEMICAL MODIFICATION; CHICKEN; COLON; CROSS LINKING; ELECTRON MICROSCOPY; ESCHERICHIA COLI; EXTRACTION; GENE DELETION; GENE EXPRESSION; GENETIC CODE; ILEUM; LACTOBACILLUS; LACTOBACILLUS CASEI; LACTOBACILLUS CRISPATUS; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN IMMOBILIZATION; PROTEIN STRUCTURE;

BACTERIAL ADHESION; BACTERIAL PROTEINS; CELL WALL; COLLAGEN; GENE DELETION; LACTOBACILLUS; LACTOBACILLUS CASEI; LAMININ; LIPOPOLYSACCHARIDES; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; TEICHOIC ACIDS;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; GALLUS GALLUS; LACTOBACILLUS; LACTOBACILLUS CASEI; LACTOBACILLUS CRISPATUS; POSIBACTERIA; PROKARYOTA;

EID: 0036430117     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2002.03180.x     Document Type: Article

References (53)

1. Baumeister, W., Wildhaber, I., and Phipps, B.M. (1989) Principles of organization in eubacterial and archaebacterial surface proteins. Can J Microbiol 35: 215-227.
2. Blaser, M.J., Smith, P.F., Hopkins, J.A., Heinzer, I., Bryner, J.H., and Wang, W.-L.L. (1987) Pathogenesis of Campylobacter fetus infection: Serum resistance associated with high-molecular-weight surface proteins. J Infect Dis 155: 696-706.
3. Boot, H.J., Kolen, C.P.A.M., van Noort, J.M., and Pouwels, P.H. (1993) S-layer protein of Lactobacillus acidophilus ATCC 4356: Purification, expression in Escherichia coli, and nucleotide sequence of the corresponding gene. J Bacteriol 175: 6089-6096.
4. Boot, H.J., Kolen, C.P.A.M., and Pouwels, P.H. (1995) Identification, cloning, and nucleotide sequence of a silent S-layer protein gene of Lactobacillus acidophilus ATCC 4356 which has extensive similarity with the S-layer protein gene of this species. J Bacteriol 177: 7222-7230.
5. Boot, H.J., Kolen, C.P.A.M., Pot, B., Kersters, K., and Pouwels, P.H. (1996) The presence of two S-layer protein encoding genes is conserved among species related to Lactobacillus acidophilus. Microbiology 142: 2375-2384.
6. Brechtel, E., and Bahl, H. (1999) In Thermoanaerobacterium thermosulfurigenes EM1 S-layer homology domains do not attach to peptidoglycan. J Bacteriol 181: 5017-5023.
7. Callegari, M.L., Riboli, B., Sanders, J.W., Cocconcelli, P.S., Kok, J., Venama, G., and Morelli, L. (1998) The S-layer gene of Lactobacillus helveticus CNRZ 892: Cloning, sequence and heterologous expression. Microbiology 144: 719-726.
8. Coligan, J.E., Kruisbeck, A.M., Margulies, D.H., Shevach, E.M., and Strober, W. (1994) Current Protocols in Immunology. New York: John Wiley & Sons.
9. Dworkin, J., Tummuru, M.K.R., and Blaser, M.J. (1995) A lipopolysaccharide-binding domain of the Campylobacter fetus S-layer protein resides within the conserved N terminus of a family of silent and divergent homologs. J Bacteriol 177: 1734-1741.
10. Egelseer, E., Schocher, I., Sára, M., and Sleytr, U.B. (1995) The S-layer from Bacillus stearothermophilus DSM 2358 functions as an adhesion site for a high-molecular weight amylase. J Bacteriol 177: 1444-1451.
11. Engelhardt, H., and Peters, J. (1998) Structural research on surface layers: A focus on stability, surface layer homology domains, and surface layer-cell wall interactions. J Struct Biol 124: 276-302.
12. Fujisawa, T., Benno, Y., Yaeshima, T., Mitsuoka, T. (1992) Taxonomic study of the Lactobacillus acidophilus group, with recognition of Lactobacillus gallinarum sp. nov. and synonymy of Lactobacillus acidophilus group A3 (Johnson et al., 1980) with the type strains of Lactobacillus amylovorus (Nakamura 1981). Int J Syst Bacteriol 42: 487-491.
13. Gilbert, C., Atlan, D., Blanc, B., Portalier, R., Germond, J.E., Lapierre, L., and Mollet, B. (1996) A new cell surface proteinase: Sequencing and analysis of the prtB gene from Lactobacillus delbrueckii subsp. bulgaricus. J Bacteriol 178: 3059-3065.
14. Hancock, I., and Poxton, I. (1988) Bacterial Surface Techniques. Chichester: John Wiley & Sons.
15. Helin, J., Caldentey, J., Kalkkinen, N., and Bamford, D.H. (1999) Analysis of the multimeric state of proteins by matrix assisted laser desorption/ionization mass spectrometry after cross-linking with glutaraldehyde. Rapid Commun Mass Spectrom 13: 185-190.
16. Higuchi, R., Krummel, B., and Saiki, R.K. (1988) A general method of in vitro preparation and specific mutagenesis of DNA fragments: Study of protein and DNA interactions. Nucleic Acids Res 16: 7351-7367.
17. Hoiczyk, E., Roggenkamp, A., Reichenbecher, M., Lupas, A., and Heesemann, J. (2000) Structure and sequence analysis of Yersinia YadA and Moraxella UpsAs reveal a novel class of adhesins. EMBO J 19: 5989-5999.
18. Howarka, S., Sára, M., Wang, Y., Kuen, B., Sleytr, U.B., Lubitz, W., and Bayley, H. (2000) Surface-accessible residues in the monomeric and assembled forms of a bacterial surface layer protein. J Biol Chem 275: 37876-37886.
19. Hynönen, U., Westerlund-Wikström, B., Palva, A., and Korhonen, T.K. (2002) Identification by flagellum display of an epithelial cell- and fibronectin-binding function in the SlpA surface protein of Lactobacillus brevis. J Bacteriol 184: 3360-3367.
20. Jonquières, R., Bierne, H., Fiedler, F., Gounon, P., and Cossart, P. (1999) Interaction between the protein InIB of Listeria monocytogenes and lipoteichoic acid: A novel mechanism of protein association at the surface of Gram-positive bacteria. Mol Microbiol 34: 902-914.
21. Korhonen, T.K., Parkkinen, J., Hacker, J., Finne, J., Pere, A., and Holthöfer, H. (1984) Binding of Escherichia coli S fimbria to human kidney epithelium. Infect Immun 54: 322-327.
22. Kotiranta, A., Haapasalo, M., Kari, K., Kerosuo, E., Olsen, I., Sorsa, T., et al. (1998) Surface structure, hydrophobicity, phagocytosis, and adherence to matrix proteins of Bacillus cereus cells with and without the crystalline surface protein layer. Infect Immun 66: 4895-4902.
23. Kukkonen, M., Raunio, T., Virkola, R., Lähteenmäki, K., Mäkelä, 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.
24. Lerche, M., and Reuter, G. (1962) Das vorkommen aerobewachsender grampositiver stäbchendes genus Lactobacillus beijerinck im darminhalt erwaschsener menschen. Zentralbl Bacteriol Abt Orig 185: 446-481.
25. Lortal, S., van Heijenoort, J., Gruber, K., and Sleytr, U.B. (1992) S-layer of Lactobacillus helveticus ATCC 12046: Isolation, chemical characterization and re-forming after extraction with lithium chloride. J Gen Microbiol 138: 611-618.
26. Lupas, A., Engelhardt, H., Peters, J., Santarius, U., Volker, S., and Baumeister, W. (1994) Domain structure of the Acetogenium kivui surface layer revealed by electron crystallography and sequence analysis. J Bacteriol 176: 1224-1233.
27. McCracken, V.J., and Lorenz, R.G. (2001) The gastrointestinal ecosystem: A precarious alliance among epithelium, immunity and microbiota. Cell Microbiol 3: 1-11.
28. T. J Bacteriol 182: 6857-6861.
29. Mercenier, A., Müller-Alouf, H., and Grangette, C. (2000) Lactic acid bacteria as live vaccines. Curr Issues Mol Biol 2: 17-25.
30. Mesnage, S., Tosi-Couture, E., and Fouet, A. (1999) Production and cell surface anchoring of functional fusions between the SLH motifs of the Bacillus anthracis S-layer proteins and the Bacillus subtilis levansucrase. Mol Microbiol 31: 927-936.
31. Mitsuoka, T. (1969) Vergleichende untersuchengenu über die laktobazillen aus den faeces von menschen, sweinen und hühnern. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg 210: 32-51.
32. Neuhaus, F.C. (1985) Inter-chain transacylation of D-alanine ester residues of lipoteichoic acid: A unique mechanism of membrane communication. Biochem Soc Trans 13: 987-990.
33. Noonan, B., and Trust, T.J. (1997) The synthesis, secretion and role in virulence of the paracrystalline surface protein layers of Aeromonas salmonicida and A. hydrophila. FEMS Microbiol Lett 154: 1-7.
34. Pouttu, R., Westerlund-Wikström, B., Lång, H., Alsti, K., Virkola, R., Saarela, U., et al. (2001) matB, a common fimbrillin gene of Escherichia coli, expressed in a genetically conserved, virulent clonal group. J Bacteriol 183: 4727-4736.
35. Pouwels, P.H., Vriesema, A., Martinez, B., Tielen, F.J., Seegers, J.F.M., Leer, R.J., et al. (2001) Lactobacilli as vehicles for targeting antigens to mucosal tissues by surface exposition of foreign peptides. Methods Enzymol 336: 369-389.
36. Pum, D., and Sleytr, U.B. (1999) The application of bacterial S-layers in molecular nanotechnology. Trends Biotechnol 17: 8-12.
37. Pum, D., Messner, P., and Sleytr, U.B. (1991) Role of the S layer in morphogenesis and cell division of the archaebacterium Methanocorpusculum sinense. J Bacteriol 173: 6865-6873.
38. Rich, R.L., Kreikemeyer, B., Owens, R.T., LaBrenz, S., Narayana, S.V., Weinstock, G.M., et al. (1999) Ace is a collagen-binding MSCRAMM from Enterococcus faecalis. J Biol Chem 274: 26939-26945.
39. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989)Molecular Cloning: A Laboratory Manual, 2nd Edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
40. Sára, M., and Sleytr, U.B. (2000) S-layer proteins. J Bacteriol 182: 859-868.
41. Sára, M., Egelseer, E.M., Dekitsch, C., and Sleytr, U.B. (1998) Identification of two binding domains, one for peptidoglycan and another for a secondary cell wall polymer, on the N-terminal part of the S-layer protein SbsB from Bacillus stearothermophilus PV72/p2. J Bacteriol 180: 6780-6783.
42. Scott, M.G., Gold, M.R., and Hancock, R.E.W. (1999) Interaction of cationic peptides with lipoteichoic acid and Gram-positive bacteria. Infect Immun 67: 6445-6453.
43. Sillanpää, J., Martínez, B., Antikainen, J., Toba, T., Kalkkinen, N., Tankka, S., et al. (2000) Characterization of the collagen-binding S-layer protein CbsA of Lactobacillus crispatus. J Bacteriol 182: 6440-6450.
44. Sleytr, U.B., and Beveridge, T.J. (1999) Bacterial S-layers. Trends Microbiol 7: 253-260.
45. Smit, E., Oling, F., Demel, R., Martinez, B., and Pouwels, P.H. (2001) The S-layer protein of Lactobacillus acidophilus ATCC 4356: Identification and characterisation of domains responsible for S-protein assembly and cell wall binding. J Mol Biol 305: 245-257.
46. Steidler, L., Hans, W., Schotte, L., Neirynck, S., Obermeier, F., Falk, W., et al. (2000) Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289: 1352-1355.
47. Stinson, M.W., McLaughlin, R., Choi, S.H., Juarez, Z.E., and Barnard, J. (1998) Streptococcal histone-like protein: Primary structure of hlpA and protein binding to lipoteichoic acid and epithelial cells. Infect Immun 66: 259-265.
48. Symersky, J., Patti, J.M., Carson, M., House-Pompeo, K., Teale, M., Moore, D., et al. (1997) Structure of the collagen-binding domain from a Staphylococcus aureus adhesin. Nature Struct Biol 4: 833-838.
49. Tamm, A., Tarkkanen, A.-M., Korhonen, T.K., Kuusela, P., Toivanen, P., and Skurnik, M. (1993) Hydrophobic domains affect the collagen-binding specificity and surface polymerization as well as virulence potential of the YadA protein of Yersinia enterocolitica. Mol Microbiol 10: 995-1011.
50. Toba, T., Virkola, R., Westerlund, B., Björkman, Y., Sillanpää, J., Vartio, T., et al. (1995) A collagen-binding S-layer protein in Lactobacillus crispatus. Appl Environ Microbiol 61: 2467-2471.
51. Vidgrén, G., Palva, I., Pakkanen, R., Lounatmaa, K., and Palva, A. (1992) S-layer protein gene of Lactobacillus brevis: Cloning by polymerase chain reaction and determination of the nucleotide sequence. J Bacteriol 174: 7419-7427.
52. Westerlund-Wikström, B., Tanskanen, J., Virkola, R., Hacker, J., Lindberg, M., Skurnik, M., and Korhonen, T.K. (1997) Functional expression of adhesive peptides as fusions to Escherichia coli flagellin. Protein Eng 10: 1319-1326.
53. Yother, J., and White, J.M. (1994) Novel surface attachment mechanism of the Streptococcus pneumoniae protein PspA. J Bacteriol 176: 2976-2985.