The haemolysin-secreting ShlB protein of the outer membrane of Serratia marcescens: Determination of surface-exposed residues and formation of ion-permeable pores by ShlB mutants in artificial lipid bilayer membranes

Molecular Microbiology

Volumn 32, Issue 6, 1999, Pages 1212-1225

  Könninger, Ulrich W ^a   Hobbie, Silke ^a   Benz, Roland ^b   Braun, Volkmar ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOLYSIN; MONOCLONAL ANTIBODY; OUTER MEMBRANE PROTEIN; SIGNAL PEPTIDE;

ANTIGEN BINDING; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL MUTANT; CHANNEL GATING; CONTROLLED STUDY; DELETION MUTANT; GENE INSERTION; GENE MUTATION; ION TRANSPORT; LIPID BILAYER; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN SECRETION; SERRATIA MARCESCENS;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; EPITOPES, B-LYMPHOCYTE; GENETIC ENGINEERING; HEMOLYSIN PROTEINS; IONS; LIPID BILAYERS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PROTEIN STRUCTURE, SECONDARY; SERRATIA MARCESCENS;

EID: 0032991297     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01433.x     Document Type: Article

References (48)

1. Agterberg, M., and Tommassen, J. (1991) Outer membrane protein PhoE as a carrier for the exposure of foreign antigenic determinants at the bacterial cell surface. Antonie Van Leeuwenhoek 59: 249-262.
2. Armstrong, S.K., and McIntosh, M.A. (1995) Epitope insertions define functional and topological features of the Escherichia coli ferric enterobactin receptor. J Biol Chem 270: 2483-2488.
3. Barany, F. (1988) Procedure for linker insertion mutagenesis and use of new kanamycin resistance cassettes. DNA Protein Eng Tech 1: 29-44.
4. Benz, R., Janko, K., Boos, W., and Läuger, P. (1978) Formation of large, ion-permeable membrane channels by the matrix protein (porin) of Escherichia coli. Biochim Biophys Acta 511: 305-319.
5. Benz, R., Schmid, A., and Hancock, R.E.W. (1985) Ion selectivity of Gram-negative bacterial porins. J Bacteriol 162: 722-727.
6. Benz, R., Schmid, A., Maier, C., and Bremer, E. (1988) Characterization of the nucleoside-binding site inside the Tsx-channel of Escherichia coli outer membrane. Eur J Biochem 176: 699-705.
7. Blight, M.A., and Holland, I.B. (1994) Heterologous protein secretion and the versatile Escherichia coli haemolysin translocator. Trends Biotechnol 12: 450-455.
8. Braun, V., Günther, H., Neuss, B., and Tautz, C. (1985) Haemolytic activity of Serratia marcescens. Arch Microbiol 141: 371-376.
9. Braun, V., Neuss, B., Ruan, Y., Schiebel, E., Schöffler, H., and Jander, G. (1987) Identification of the Serratia marcescens haemolysin determinant by cloning into Escherichia coli. J Bacteriol 169: 2113-2120.
10. Carmel, G., and Coulton, J.W. (1991) Internal deletions in the FhuA receptor of Escherichia coli K-12 define domains of ligand interaction. J Bacteriol 173: 4394-4403.
11. Cowan, S.W., Schirmer, T., Rummel, G., Steiert, M., Ghosh, R., Paupitt, R.A., et al. (1992) Crystal structures explain functional properties of two E. coli porins. Nature 358: 727-733.
12. Ferguson, A.D., Hofmann, E., Coulton, J.W., Diederichs, K., and Welte, W. (1998) Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282: 2215-2220.
13. Gromhia, M.M., and Ponnuswamy, P.K. (1993) Prediction of transmembrane β-strands from hydrophobic characteristics of proteins. Int J Peptide Protein Res 42: 420-431.
14. Gromiha, M.M., Majumdar, R., and Ponnuswamy, P.K. (1997) Identification of membrane spanning β strands in bacterial porins. Protein Eng 10: 487-500.
15. Hantke, K. (1981). Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet 182: 288-292.
16. Hertle, R., Brutsche, S., Groeger, W., Hobbie, S., Koch, W., Könninger, U.W., and Braun, V. (1997) Specific phosphatidylethanolamine dependence of Serratia marcescens cytotoxin activity. Mol Microbiol 26: 853-865.
17. Hirono, I., Tange, N., and Aocki, T. (1997) Iron-regulated haemolysin gene from Edwardsiella tarda. Mol Microbiol 24: 851-856.
18. Hueck, C.J. (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379-433.
19. Hughes, C., Stanley, P., and Koronakis, V. (1992) E. coli haemolysin interactions with prokaryotic and eukaryotic cell membranes. Bioessays 14: 519-525.
20. Killmann, H., Benz, R., and Braun, V. (1993) Conversion of the FhuA transport protein into a diffusion channel through the outer membrane of Escherichia coli. EMBO J 12: 3007-3016.
21. Killmann, H., Benz, R., and Braun, V. (1996) Properties of the FhuA channel in the outer membrane after deletion of FhuA portions within and outside the predicted gating loop. J Bacteriol 178: 6913-6920.
22. Klauser, T., Pohlner, J., and Meyer, T.F. (1993) The secretion pathway of IgA protease-type proteins in Gram-negative bacteria. Bioessays 15: 799-805.
23. Koebnik, R., and Braun, V. (1993) Insertion derivatives containing segments of up to 16 amino acids identify surface and periplasm-exposed regions of the FhuA outer membrane receptor of Escherichia coli. J Bacteriol 175: 825-839.
24. Köster, W., Gudmundsdottir, A., Lundigran, M.D., Seifert, A., and Kadner, R.J. (1991) Deletions or duplications in the BtuB protein affect its level in the outer membrane of Escherichia coli. J Bacteriol 173: 5639-5647.
25. Locher, K.P., Rees, B., Koebnik, R., Mitschler, A., Moulinier, L., Rosenbusch, J.P., and Moras, D. (1998) Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95: 771-778.
26. Merck, K.B., de Cock, H., Verheij, H.M., and Tommassen, J. (1997) Topology of the outer membrane phospholipase A of Salmonella typhimurium. J Bacteriol 179: 3443-3450.
27. Moeck, G.S., Bazzaz, B.S.F., Gras, M.F., Ravi, T.S., Ratcliffe, M.J.H., and Coulton, J.W. (1994) Genetic insertion and exposure of a reporter epitope in the ferrichrome-iron receptor of Escherichia coli K-12. J Bacteriol 176: 4250-4259.
28. Newton, S.M.C., Klebba, P.E., Michel, V., Hofnung, M., and Charbit, A. (1996) Topology of the membrane protein LamB by epitope tagging and a comparison with the X-ray model. J Bacteriol 178: 3447-3456.
29. Ondraczek, R., Hobbie, S., and Braun, V. (1992) In vitro activation of the Serratia marcescens haemolysin through modification and complementation. J Bacteriol 174: 5086-5094.
30. Palmer, K.L., and Munson, Jr, R.S. (1995) Cloning and characterization of the genes encoding the haemolysin of Haemophilus ducreyi. Mol Microbiol 18: 821-830.
31. Poole, K., Schiebel, E., and Braun, V. (1988) Molecular characterization of the haemolysin determinant of Serratia marcescens. J Bacteriol 170: 3177-3188.
32. Pugsley, A.P. (1993) The complete secretory pathway in Gram-negative bacteria. Microbiol Rev 57: 50-108.
33. Ruan, Y., and Braun, V. (1990) Haemolysin as a marker for Serratia. Arch Microbiol 154: 221-225.
34. Schiebel, E., and Braun, V. (1989) Integration of the Serratia marcescens haemolysin into human erythrocyte membranes. Mol Microbiol 3: 445-453.
35. Schiebel, E., Schwarz, H., and Braun, V. (1989) Subcellular location and unique secretion of the haemolysin of Serratia marcescens. J Biol Chem 264: 16311-16320.
36. Schirmer, T., and Cowan, S.W. (1993) Prediction of membrane-spanning β-strands and its application to maltoporin. Protein Sci 2: 1361-1363.
37. Schirmer, T., Keller, T.A., Wang, Y.-F., and Rosenbusch, J.P. (1995) Structural basis for sugar translocation through maltoporin channels at 3.1 Angstrom resolution. Science 267: 512-514.
38. Schlör, S., Schmidt, A., Maier, E., Benz, R., Goebel, W., and Gentschew, I. (1997) In vivo and in vitro studies on interactions between the components of the haemolysin (HlyA) secretion machinery of Escherichia coli. Mol Gen Genet 256: 306-319.
39. Schönherr, R., Tsolis, R., Focareta, T., and Braun, V. (1993) Amino acid replacements in the Serratia marcescens haemolysin ShlA define sites involved in activation and secretion. Mol Microbiol 9: 1229-1237.
40. Schönherr, R., Hilger, M., Broer, S., Benz, R., and Braun, V. (1994) Interaction of Serratia marcescens haemolysin (ShlA) with artificial and erythrocyte membranes: demonstration of the formation of aqueous multistate channels. Eur J Biochem 223: 655-663.
41. Struyvé, M., Visser, J., Adriaanse, H., Benz, R., and Tommassen, J. (1993) Topology of PhoE porin: the 'eyelet' region. Mol Microbiol 7: 131-140.
42. Studier, F.W., and Moffatt, B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189: 113-130.
43. Sukhan, A., and Hancock, R.E.W. (1995) Insertion mutagenesis of the Pseudomonas aeruginosa phosphate-specific porin OprP. J Bacteriol 177: 4917-4920.
44. Tabor, S., and Richardson, C.C. (1985) A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci USA 82: 1074-1078.
45. Totten, P.A., Norn, V.D., and Stam, W.E. (1995) Characterization of the hemolytic activity of Haemophilus ducreyi. Infect Immun 63: 4409-4416.
46. Uphoff, T.S., and Welch, R.A. (1990) Nucleotide sequencing of the Proteus mirabilis calcium-independent haemolysin genes (hpmA and hpmB) reveals sequence similarity with the Serratia marcescens haemolysin genes (shlA and shlB). J Bacteriol 172: 1206-1216.
47. Vogel, H., and Jähnig, F. (1986) Models for the structure of outer membrane proteins in Escherichia coli derived from Raman spectroscopy and prediction methods. J Mol Biol 190: 191-199.
48. Weiss, M.S., and Schulz, G.E. (1992) Structure of porin refined at 1.8 Angstrom resolution. J Mol Biol 227: 493-509.