Characterization of the interaction of single tryptophan containing mutants of IpaC from Shigella flexneri with phospholipid membranes

Biochemistry

Volumn 45, Issue 2, 2006, Pages 626-636

  Harrington, Amanda ^a   Darboe, Numukunda ^a   Kenjale, Roma ^a   Picking, Wendy L ^a   Middaugh, C Russell ^a   Birket, Susan ^a   Picking, William D ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOLOGICAL MEMBRANES; CELLS; FLUORESCENCE; PATHOLOGY; PHOSPHOLIPIDS; SPECTROSCOPIC ANALYSIS;

LIPOSOME VESICLES; PHOSPHOLIPID MEMBRANES; SHIGELLA FLEXNERI; SINGLE TRYPTOPHAN;

NUCLEIC ACID SEQUENCES;

BACTERIAL ANTIGEN; INVASION PLASMID ANTIGEN C; PHOSPHOLIPID; TRYPTOPHAN; UNCLASSIFIED DRUG;

ABSORPTION SPECTROSCOPY; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIUM MUTANT; CELL INVASION; CIRCULAR DICHROISM; CYTOPLASM; DYSENTERY; EFFECTOR CELL; EPITHELIUM CELL; IN VIVO STUDY; INTESTINE CELL; MEMBRANE STRUCTURE; MEMBRANE VESICLE; NONHUMAN; PHOSPHOLIPID VESICLE; PHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN STRUCTURE; SHIGELLA FLEXNERI;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIGENS, BACTERIAL; CELL LINE; CHOLESTEROL; CIRCULAR DICHROISM; HEAT; HUMANS; LIPOSOMES; PHOSPHOLIPIDS; SHEEP; SHIGELLA FLEXNERI; SPECTROMETRY, FLUORESCENCE; TRYPTOPHAN;

BACTERIA (MICROORGANISMS); SHIGELLA; SHIGELLA FLEXNERI;

EID: 30744451417     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0512593     Document Type: Article

References (44)

1. Hale, T. L. (1991) Genetic basis of virulence in Shigella species, Microbiol. Rev. 55, 206-224.
2. Centers for Disease Control and Prevention (2005) Shigellosis, http://www.cdc.gov/ncidod/dbmd/diseaseinfo/shigellosis_g.htm.
3. Behrana, V., Harty, J. T., and Jones, B. D. (1998) Interactions of the invasive pathogens Salmonella typhimurium, Listeria monocytogenes, and Shigella flexneri with M cells and murine Peyer's patches, Infect. Immun. 66, 3758-3766.
4. Clerc, P., and Sansonetti, P. J. (1987) Entry of Shigella flexneri into HeLa cells: evidence for directed phagocytosis involving actin polymerization and myosin accumulation, Infect. Immun. 55, 2681-2688.
5. Niebuhr, K., and Sansonetti, P. J. (2000) Invasion of epithelial cells by bacterial pathogens the paradigm of Shigella, Subcell. Biochem. 33, 251-287.
6. Tran Van Nhieu, G., Bourdet-sicard, R., Dumenil, G., Blocker, A., and Sansonetti, P. J. (2000) Bacterial signals and cell responses during Shigella entry into epithelial cells, Cell. Microbiol. 2, 187-193.
7. Tran Van Nhieu, G., Caron, E., Hall, A., and Sansonetti, P. J. (1999) IpaC induces actin polymerization and filopodia formation during Shigella entry into epithelial cells, EMBO J. 18, 3249-3262.
8. Sansonetti, P. J., Ryter, A., Clerc, Pl., Maurelli, A. T., and Mounier, J. (1986) Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic acuole and plasmid-mediated contact hemolysis, Infect. Immun. 51, 461-469.
9. Menard, R., Sansonetti, P. J., and Parsot, C. (1993) Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells, J. Bacteriol. 175, 5899-5906.
10. Menard, R., Prevost, M. C., Gounon, P., Sansonetti, P., and Dehio, C. (1996) The secreted Ipa complex of Shigella flexneri promotes entry into mammalian cells, Proc. Natl. Acad. Sci. U.S.A. 93, 1254-1258.
11. Watarai, M., Funato, S., and Sasakawa, C. (1996) Interaction of Ipa proteins of Shigella flexneri with alpha5beta1 integrin promotes entry of the bacteria into mammalian cells, J. Exp. Med. 183, 991-999.
12. Marquart, M. E., Picking, W. L., and Picking, W. D. (1996) Soluble invasion plasmid antigen C (IpaC) from Shigella flexneri elicits epithelial cell responses related to pathogen invasion, Infect. Immun. 64, 4182-4187.
13. Kueltzo, L. A., Osiecki, J., Barker, J., Picking, W. L., Wessel, A., Picking, W. D., and Middaugh, C. R. (2003) Structure-function analysis of invasion plasmid antigen C (IpaC) from Shigella flexneri, J. Biol. Chem. 278, 2792-2798.
14. Osiecki, J., Barker, J., Picking, W. L., Barnoski-Serifs, A., Berring, E., Shah, S., Harrington, A., and Picking, W. D. (2001) IpaC from Shigella and SipC from Salmonella possess similar biochemical properties but are functionally distinct, Mol. Microbiol. 42, 469-481.
15. Tran, N., Serfis, A. B., Davis, R., Osiecki, J. C., Coye, L., Picking, W. L., and Picking, W. D. (2000) Interaction of Shigella flexneri IpaC with model membranes correlates with effects on cultured cells, Infect. Immun. 68, 3710-3715.
16. Kuwae, A., Yoshida, S., Tamano, K., Mimuro, H., Suzuki, T., and Sasakawa, C. (2001) Shigella invasion of macrophage requires the insertion of IpaC into the host plasma membrane. Functional analysis of IpaC, J. Biol. Chem. 276, 32230-32239.
17. Terajima, J., Moriishi, E., Kurata, T., and Watanabe, H. (1999) Preincubation of recombinant Ipa proteins of Shigella sonnei promotes entry of non-invasive Escherichia coli into HeLa cells, Microb. Pathog. 26, 223-230.
18. De Geyter, C., Vogt, B., Benjelloun-Touimi, Z., Sansonetti, P. J., Ruysschaert, J.-M., Parsot, C., and Cabiaux, V. (1997) Purification of IpaC, a protein involved in entry of Shigella flexneri into epithelial cells and characterization of its interaction with lipid membranes, FEBS Lett. 400, 149-154.
19. Picking, W. L., Coye, L., Osiecki, J. C., Serfis, A., and Picking, W. D. (2001) Identification of functional regions within invasion plasmid antigen C (IpaC) of Shigella flexneri, Mol. Microbiol. 39, 100-111.
20. Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Glasgow, B. J. (2001) Site-directed tryptophan fluorescence reveals the solution structure of tear lipocalin: evidence for features that confer promiscuity in ligand binding, Biochemistry 40, 14754-14762.
21. Harrington, A. T., Hearn, P. D., Picking, W. L., Barker, J. R., Wessel, A., and Picking, W. D. (2003) Structural characterization of the N terminus of IpaC from Shigella flexneri, Infect. Immun. 71, 1255-1264.
22. Provencher, S., and Glockner, J. (1981) Estimation of globular protein secondary structure from circular dichroism, Biochemistry 20, 33-37.
23. Sreerama, N., and Woody, R. W. (1993) A self-consistent method for the analysis of protein secondary structure from circular dichroism, Anal. Biochem. 209, 32-44.
24. Manavalan, P., and Johnson, W. C., Jr. (1987) Variable selection method improves the prediction of protein secondary structure from circular dichroism spectra, Anal. Biochem. 167, 76-85.
25. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves, Methods Enzymol. 131, 266-280.
26. Raja, S. M., Rawat, S. S., Chattopadhyay, A., and Lala, A. K. (1999) Localization and environment of tryptophans in soluble and membrane-bound states of a pore-forming toxin from Staphylococcus aureus, Biophys. J. 76, 1469-1479.
27. Rausell, C., Munoz-Garay, C., Miranda-CassoLuengo, R., Gomez, I., Rudino-Pinera, E., Soberon, M., and Bravo, A. (2004) Tryptophan spectroscopy studies and black lipid bilayer analysis indicate that the oligomeric structure of Cry 1 Ab toxin from Bacillus thuringiensis is the membrane-inserted intermediate, Biochemistry 43, 166-174.
28. Stern, O., and Volmer, M. (1919) On the quenching time of fluorescence, Z. Phys. 20, 183-188.
29. Kueltzo, L. A., Ersoy, B., Ralston, J. P., and Middaugh, C. R. (2003) Derivative absorbance spectroscopy and protein phase diagrams as tools for comprehensive protein characterization: a bGCSF case study, J. Pharm. Sci. 92, 1805-1820.
30. Mach, H., and Middaugh, C. R. (1993) Measuring protein spectra in the presence of light scattering, BioTechniques 15, 240-242.
31. Richmond, J. Y., and McKinney, R. W., Eds. (1999) Biosafety in Microbiological and Biomedical Laboratories, 4th ed., U.S. Government Printing Office, Washington, DC.
32. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, 2nd ed., Plenum Press, New York.
33. Pallen, M. J., Dougan, G., and Frankel, G. (1997) Coiled-coil domains in proteins secreted by type III secretion systems, Mol. Microbiol. 25, 423-425.
34. Eftink, M. R., Ionescu, R., Ramsay, G. D., Wong, C. Y., Wu, J. Q., and Maki, A. H. (1996) Thermodynamics of the unfolding and spectroscopic properties of the V66W mutant of Staphylococcal nuclease and its 1-136 fragment, Biochemistry 35, 8084-8094.
35. van der Goot, F. G., Tran Van Nhieu, G., Allaoui, A., Sansonetti, P., and Lafont, F. (2004) Rafts can trigger contact-mediated secretion of bacterial effectors via a lipid-based mechanism, J. Biol. Chem. 279, 47792-47798.
36. Lafont, F., Tran Van Nhieu, G., Hanada, K., Sansonetti, P., and van der Goot, F. G. (2002) Initial steps of Shigella infection depend on the cholesterol/sphingolipid raft-mediated CD44-IpaB interaction, EMBO J. 21, 4449-4457.
37. Hayward, R. D., Cain, R. J., McGhie, E. J., Phillips, N., Garner, M. J., and Koronakis, V. (2005) Cholesterol binding by the bacterial type III translocon is essential for virulence effector delivery into mammalian cells, Mol. Microbiol. 56, 590-603.
38. Hattendorf, D. A., and Lindquist, S. L. (2002) Analysis of the AAA sensor-2 motif in the C-terminal ATPase domain of Hsp104 with a site-specific fluorescent probe of nucleotide binding, Proc. Natl. Acad. Sci. U.S.A. 99, 2732-2727.
39. Yengo, C. M., Fagnant, P. M., Chrin, L., Rovner, A. S., and Berger, C. L. (1998) Smooth muscle myosin mutants containing a single tryptophan reveal molecular interactions at the actin-binding interface, Proc. Natl. Acad. Sci. U.S.A. 95, 12944-12949.
40. Sackmann, E. (1995) Biological membranes architecture and function, in Structure and Dynamics of Membranes (Lipowsky, R., and Sackmann, E., Eds.) pp 1-64, Elsevier, Amsterdam.
41. Gilbert, R. J. (2002) Pore-forming toxins, Cell. Mol. Life Sci. 59, 832-844.
42. Kusumi, A., Tsuda, M., Akino, T., Ohnishi, S., and Terayama, Y. (1983) Protein-phospholipid-cholesterol interaction in the photolysis of invertebrate rhodopsin, Biochemistry 22, 1165-1170.
43. Subczynski, W. K., Wisniewska, A., Yin, J.-J., Hyde, J. S., and Kusumi, A. (1994) Hydrophobic carriers of lipid bilayer membranes formed by reduction of water penetration by alkyl chain unsaturation and cholesterol, Biochemistry 33, 7670-7681.
44. Bloom, M., and Mouritsen, O. G. (1995) The evolution of membranes, in Structure and Dynamics of Membranes (Lipowsky, R., and Sackmann, E., Eds.) pp 65-95, Elsevier, Amsterdam.