Mutations affecting the extreme C terminus of Escherichia coli haemolysin A reduce haemolytic activity by altering the folding of the toxin

Microbiology

Volumn 156, Issue 8, 2010, Pages 2495-2505

  Jumpertz, Thorsten ^a   Chervaux, Christian ^b   Racher, Kathleen ^c   Zouhair, Maria ^d   Blight, Mark A ^d   Holland, I Barry ^d   Schmitt, Lutz ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b DANONE RESEARCH   (France)

^c Indian and Northern Affairs ^*  (Canada)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE; HEMOLYSIN; HEMOLYSIN A; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; HLYA PROTEIN, E COLI;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; ESCHERICHIA COLI; FLUORESCENCE SPECTROSCOPY; GENE DELETION; GENE MUTATION; HEMOLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN SECRETION; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; SECRETION (PROCESS);

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BETA-LACTAMASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEMOLYSIN PROTEINS; HEMOLYSIS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN FOLDING;

ESCHERICHIA COLI;

EID: 77955355049     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.038562-0     Document Type: Article

References (25)

1. Andersen, C., Koronakis, E., Bokma, E., Eswaran, J., Humphreys, D., Hughes, C. & Koronakis, V. (2002). Transition to the open state of the TolC periplasmic tunnel entrance. Proc Natl Acad Sci U S A 99, 11103-11108.
2. Balakrishnan, L., Hughes, C. & Koronakis, V. (2001). Substrate-triggered recruitment of the TolC channel-tunnel during type I export of hemolysin by Escherichia coli. J Mol Biol 313, 501-510.
3. Balsalobre, C., Silvan, J. M., Berglund, S., Mizunoe, Y., Uhlin, B. E. & Wai, S. N. (2006). Release of the type I secreted alpha-haemolysin via outer membrane vesicles from Escherichia coli. Mol Microbiol 59, 99-112.
4. Bauer, M. E. & Welch, R. A. (1997). Pleiotropic effects of a mutation in rfaC on Escherichia coli hemolysin. Infect Immun 65, 2218-2224.
5. Baumann, U., Wu, S., Flaherty, K. M. & McKay, D. B. (1993). Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two-domain protein with a calcium binding parallel beta roll motif. EMBO J 12, 3357-3364.
6. Benabdelhak, H., Kiontke, S., Horn, C., Ernst, R., Blight, M. A., Holland, I. B. & Schmitt, L. (2003). A specific interaction between the NBD of the ABC-transporter HlyB and a C-terminal fragment of its transport substrate haemolysin A. J Mol Biol 327, 1169-1179.
7. Chenal, A., Guijarro, J. I., Raynal, B., Delepierre, M. & Ladant, D. (2009). RTX calcium binding motifs are intrinsically disordered in the absence of calcium: implication for protein secretion. J Biol Chem 284, 1781-1789.
8. Chervaux, C. & Holland, I. B. (1996). Random and directed mutagenesis to elucidate the functional importance of helix II and F-989 in the C-terminal secretion signal of Escherichia coli hemolysin. J Bacteriol 178, 1232-1236.
9. Chervaux, C., Sauvonnet, N., Le Clainche, A., Kenny, B., Hung, A. L., Broome-Smith, J. K. & Holland, I. B. (1995). Secretion of active beta-lactamase to the medium mediated by the Escherichia coli haemolysin transport pathway. Mol Gen Genet 249, 237-245.
10. Delepelaire, P. (2004). Type I secretion in Gram-negative bacteria. Biochim Biophys Acta 1694, 149-161.
11. Goni, F. M. & Ostolaza, H. (1998). E. coli alpha-hemolysin: a membrane-active protein toxin. Braz J Med Biol Res 31, 1019-1034.
12. Halegoua, S. & Inouye, M. (1979). Translocation and assembly of outer membrance proteins of Escherichia coli. Selective accumulation of precursors and novel assembly intermediates caused by phenethyl alcohol. J Mol Biol 130, 39-61.
13. Herlax, V. & Bakas, L. (2007). Fatty acids covalently bound to alpha-hemolysin of Escherichia coli are involved in the molten globule conformation: implication of disordered regions in binding promiscuity. Biochemistry 46, 5177-5184.
14. Holland, I. B., Benabdelhak, H., Young, J., de Lima Pimenta, A., Schmitt, L. & Blight, M. A. (2003). Bacterial ABC transporters involved in protein translocation. In ABC Proteins: from Bacteria to Man, pp. 209-241. Edited by I. B. Holland, S. P. C. Cole, K. Kuchler & C. F. Higgins. London: Academic Press.
15. Holland, I. B., Schmitt, L. & Young, J. (2005). Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway. Mol Membr Biol 22, 29-39.
16. Hyland, C., Vuillard, L., Hughes, C. & Koronakis, V. (2001). Membrane interaction of Escherichia coli hemolysin: flotation and insertion-dependent labeling by phospholipid vesicles. J Bacteriol 183, 5364-5370.
17. 2+ between the periplasm and the cytosol of Escherichia coli. Cell Calcium 32, 183-192.
18. Kenny, B., Chervaux, C. & Holland, I. B. (1994). Evidence that residues -15 to -46 of the haemolysin secretion signal are involved in early steps in secretion, leading to recognition of the translocator. Mol Microbiol 11, 99-109.
19. Koronakis, V., Koronakis, E. & Hughes, C. (1989). Isolation and analysis of the C-terminal signal directing export of Escherichia coli hemolysin protein across both bacterial membranes. EMBO J 8, 595-605.
20. Koronakis, V., Sharff, A., Koronakis, E., Luisi, B. & Hughes, C. (2000). Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405, 914-919.
21. Pimenta, A. L., Racher, K., Jamieson, L., Blight, M. A. & Holland, I. B. (2005). Mutations in HlyD, part of the type 1 translocator for hemolysin secretion, affect the folding of the secreted toxin. J Bacteriol 187, 7471-7480.
22. Sanchez-Magraner, L., Viguera, A. R., Garcia-Pacios, M., Garcillan, M. P., Arrondo, J. L., de la Cruz, F., Goni, F. M. & Ostolaza, H. (2007). The calcium-binding C-terminal domain of Escherichia coli alpha-hemolysin is a major determinant in the surface-active properties of the protein. J Biol Chem 282, 11827-11835.
23. Sotomayor Perez, A. C., Karst, J. C., Davi, M., Guijarro, J. I., Ladant, D. & Chenal, A. (2010). Characterization of the regions involved in the calcium-induced folding of the intrinsically disordered RTX motifs from the Bordetella pertussis adenylate cyclase toxin. J Mol Biol 397, 534-549.
24. Stanley, P., Packman, L. C., Koronakis, V. & Hughes, C. (1994). Fatty acylation of two internal lysine residues required for the toxic activity of Escherichia coli hemolysin. Science 266, 1992-1996.
25. Vakharia, H., German, G. J. & Misra, R. (2001). Isolation and characterization of Escherichia coli tolC mutants defective in secreting enzymatically active alpha-hemolysin. J Bacteriol 183, 6908-6916.