Single point mutation in Vibrio cholerae cytolysin compromises the membrane pore-formation mechanism of the toxin

FEBS Journal

Volumn 279, Issue 21, 2012, Pages 4039-4051

  Paul, Karan ^a   Chattopadhyay, Kausik ^a  

^a INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH MOHALI   (India)

Author keywords

bacterial protein toxin; cholesterol; membrane; pore forming toxin; Vibrio cholerae cytolysin

Indexed keywords

CHOLESTEROL; CYTOLYSIN; LIPOSOME;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTE MEMBRANE; FLOW CYTOMETRY; FLUORESCENCE; HEMOLYSIS; HUMAN; HUMAN CELL; MUTANT; NONHUMAN; OLIGOMERIZATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY; VIBRIO CHOLERAE; WESTERN BLOTTING; WILD TYPE;

BLOTTING, WESTERN; CHOLESTEROL; CYTOTOXINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTE MEMBRANE; FLOW CYTOMETRY; HEMOLYSIS; HUMANS; LIPOSOMES; PERFORIN; PHOSPHATIDYLCHOLINES; POINT MUTATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; VIBRIO CHOLERAE;

BACTERIA (MICROORGANISMS); EUKARYOTA; VIBRIO CHOLERAE;

EID: 84867573809     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08809.x     Document Type: Article

References (43)

1. Alouf JE, &, Popoff MR, (2006) The Comprehensive Sourcebook of Bacterial Protein Toxins, 3rd edn. Academic Press, New York.
2. Iacovache I, Bischofberger M, &, van der Goot FG, (2010) Structure and assembly of pore-forming proteins. Curr Opin Struct Biol 20, 241-246.
3. Iacovache I, van der Goot FG, &, Pernot L, (2008) Pore formation: an ancient yet complex form of attack. Biochim Biophys Acta 1778, 1611-1623.
4. Gonzalez M, Bischofberger M, Pernot L, van der Goot F, &, Frêche B, (2008) Bacterial pore-forming toxins: the (w)hole story? Cell Mol Life Sci 65, 493-507.
5. Tilley SJ, &, Saibil HR, (2006) The mechanism of pore formation by bacterial toxins. Curr Opin Struct Biol 16, 230-236.
6. Heuck AP, Tweten RK, &, Johnson AE, (2001) Beta-barrel pore-forming toxins: intriguing dimorphic proteins. Biochemistry 40, 9065-9073.
7. Walker B, Braha O, Cheley S, &, Bayley H, (1995) An intermediate in the assembly of a pore-forming protein trapped with a genetically engineered switch. Chem Biol 2, 99-105.
8. Walker B, Krishnasastry M, Zorn L, &, Bayley H, (1992) Assembly of the oligomeric membrane pore formed by staphylococcal alpha-hemolysin examined by truncation mutagenesis. J Biol Chem 267, 21782-21786.
9. Valeva A, Palmer M, &, Bhakdi S, (1997) Staphylococcal alpha-toxin: formation of the heptameric pore is partially cooperative and proceeds through multiple intermediate stages. Biochemistry 36, 13298-13304.
10. Bayley H, Jayasinghe L, &, Wallace M, (2005) Prepore for a breakthrough. Nat Struct Mol Biol 12, 385-386.
11. De S, &, Olson R, (2011) Crystal structure of the Vibrio cholerae cytolysin heptamer reveals common features among disparate pore-forming toxins. Proc Natl Acad Sci USA 108, 7385-7390.
12. Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, &, Gouaux JE, (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274, 1859-1866.
13. Olson R, &, Gouaux E, (2005) Crystal structure of the Vibrio cholerae cytolysin (VCC) pro-toxin and its assembly into a heptameric transmembrane pore. J Mol Biol 350, 997-1016.
14. Kaper JB, Morris JG Jr, &, Levine MM, (1995) Cholera. Clin Microbiol Rev 8, 48-86.
15. Honda T, &, Finkelstein RA, (1979) Purification and characterization of a hemolysin produced by Vibrio cholerae biotype El Tor: another toxic substance produced by cholera vibrios. Infect Immun 26, 1020-1027.
16. Goldberg SL, &, Murphy JR, (1984) Molecular cloning of the hemolysin determinant from Vibrio cholerae El Tor. J Bacteriol 160, 239-244.
17. Yamamoto K, Al-Omani M, Honda T, Takeda Y, &, Miwatani T, (1984) Non-O1 Vibrio cholerae hemolysin: purification, partial characterization, and immunological relatedness to El Tor hemolysin. Infect Immun 45, 192-196.
18. Ichinose Y, Yamamoto K, Nakasone N, Tanabe MJ, Takeda T, Miwatani T, &, Iwanaga M, (1987) Enterotoxicity of El Tor-like hemolysin of non-O1 Vibrio cholerae. Infect Immun 55, 1090-1093.
19. Krasilnikov OV, Muratkhodjaev JN, &, Zitzer AO, (1992) The mode of action of Vibrio cholerae cytolysin. The influences on both erythrocytes and planar lipid bilayers. Biochim Biophys Acta 1111, 7-16.
20. Zitzer A, Walev I, Palmer M, &, Bhakdi S, (1995) Characterization of Vibrio cholerae El Tor cytolysin as an oligomerizing pore-forming toxin. Med Microbiol Immunol 184, 37-44.
21. Ikigai H, Akatsuka A, Tsujiyama H, Nakae T, &, Shimamura T, (1996) Mechanism of membrane damage by El Tor hemolysin of Vibrio cholerae O1. Infect Immun 64, 2968-2973.
22. Menzl K, Maier E, Chakraborty T, &, Benz R, (1996) HlyA hemolysin of Vibrio cholerae O1 biotype El Tor. Identification of the hemolytic complex and evidence for the formation of anion-selective ion-permeable channels. FEBS J 240, 646-654.
23. Yuldasheva LN, Merzlyak PG, Zitzer AO, Rodrigues CG, Bhakdi S, &, Krasilnikov OV, (2001) Lumen geometry of ion channels formed by Vibrio cholerae EL Tor cytolysin elucidated by nonelectrolyte exclusion. Biochim Biophys Acta 1512, 53-63.
24. Chattopadhyay K, Bhattacharyya D, &, Banerjee KK, (2002) Vibrio cholerae hemolysin. Implication of amphiphilicity and lipid-induced conformational change for its pore-forming activity. FEBS J 269, 4351-4358.
25. Zitzer A, Westover EJ, Covey DF, &, Palmer M, (2003) Differential interaction of the two cholesterol-dependent, membrane-damaging toxins, streptolysin O and Vibrio cholerae cytolysin, with enantiomeric cholesterol. FEBS Lett 553, 229-231.
26. Zitzer A, Bittman R, Verbicky CA, Erukulla RK, Bhakdi S, Weis S, Valeva A, &, Palmer M, (2001) Coupling of cholesterol and cone-shaped lipids in bilayers augments membrane permeabilization by the cholesterol-specific toxins streptolysin O and Vibrio cholerae cytolysin. J Biol Chem 276, 14628-14633.
27. Zitzer A, Harris JR, Kemminer SE, Zitzer O, Bhakdi S, Muething J, &, Palmer M, (2000) Vibrio cholerae cytolysin: assembly and membrane insertion of the oligomeric pore are tightly linked and are not detectably restricted by membrane fluidity. Biochim Biophys Acta 1509, 264-274.
28. Harris JR, Bhakdi S, Meissner U, Scheffler D, Bittman R, Li G, Zitzer A, &, Palmer M, (2002) Interaction of the Vibrio cholerae cytolysin (VCC) with cholesterol, some cholesterol esters, and cholesterol derivatives: a TEM study. J Struct Biol 139, 122-135.
29. Ikigai H, Otsuru H, Yamamoto K, &, Shimamura T, (2006) Structural requirements of cholesterol for binding to Vibrio cholerae hemolysin. Microbiol Immunol 50, 751-757.
30. Lakowicz JR, (2006) Principles of Fluorescence Spectroscopy, 3rd edn. Springer, New York.
31. Chattopadhyay K, &, Banerjee KK, (2003) Unfolding of Vibrio cholerae hemolysin induces oligomerization of the toxin monomer. J Biol Chem 278, 38470-38475.
32. Harris JR, &, Palmer M, (2010) Cholesterol specificity of some heptameric beta-barrel pore-forming bacterial toxins: structural and functional aspects. Subcell Biochem 51, 579-596.
33. He Y, &, Olson R, (2010) Three-dimensional structure of the detergent-solubilized Vibrio cholerae cytolysin (VCC) heptamer by electron cryomicroscopy. J Struct Biol 169, 6-13.
34. Lohner S, Walev I, Boukhallouk F, Palmer M, Bhakdi S, &, Valeva A, (2009) Pore formation by Vibrio cholerae cytolysin follows the same archetypical mode as β-barrel toxins from Gram-positive organisms. FASEB J 23, 2521-2528.
35. Paul K, &, Chattopadhyay K, (2011) Unfolding distinguishes the Vibrio cholerae cytolysin precursor from the mature form of the toxin. Biochemistry 50, 3936-3945.
36. Saha N, &, Banerjee KK, (1997) Carbohydrate-mediated regulation of interaction of Vibrio cholerae hemolysin with erythrocyte and phospholipid vesicle. J Biol Chem 272, 162-167.
37. Zitzer A, Palmer M, Weller U, Wassenaar T, Biermann C, Tranum-Jensen J, &, Bhakdi S, (1997) Mode of primary binding to target membranes and pore formation induced by Vibrio cholerae cytolysin (hemolysin). FEBS J 247, 209-216.
38. Farrand AJ, LaChapelle S, Hotze EM, Johnson AE, &, Tweten RK, (2010) Only two amino acids are essential for cytolytic toxin recognition of cholesterol at the membrane surface. Proc Natl Acad Sci USA 107, 4341-4346.
39. CCP4 (Collaborative Computational Project N) (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50, 760-763.
40. Arnold K, Bordoli L, Kopp J, &, Schwede T, (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201.
41. Kiefer F, Arnold K, Kunzli M, Bordoli L, &, Schwede T, (2009) The SWISS-MODEL repository and associated resources. Nucleic Acids Res 37, D387-D392.
42. Ramachandran S, Kota P, Ding F, &, Dokholyan NV, (2011) Automated minimization of steric clashes in protein structures. Proteins 79, 261-270.
43. DeLano WL, (2002) The PyMOL Molecular Graphics System. http://www.pymol.org.