The cytolytic activity of vaginolysin strictly depends on cholesterol and is potentiated by human CD59

Toxins

Volumn 7, Issue 1, 2015, Pages 110-128

  Zilnyte, Milda ^a   Venclovas, Česlovas ^a   Zvirbliene, Aurelija ^a   Pleckaityte, Milda ^a  

^a VILNIUS UNIVERSITY   (Lithuania)

Author keywords

Cholesterol; Cytolysin; HCD59; Liposomes; Pore; Vaginolysin

Indexed keywords

BACTERIAL TOXIN; CD59 ANTIGEN; CHOLESTEROL; CYTOLYSIN; LIPOSOME; MONOCLONAL ANTIBODY; PNEUMOLYSIN; UNCLASSIFIED DRUG; VAGINOLYSIN; BACTERIAL PROTEIN; BACTERIOCIN; CD59 PROTEIN, HUMAN; CYTOTOXIN; INTERMEDILYSIN PROTEIN, STREPTOCOCCUS INTERMEDIUS; PLY PROTEIN, STREPTOCOCCUS PNEUMONIAE; STREPTOLYSIN; VAGINOLYSIN, GARDNERELLA VAGINALIS;

AGAR GEL ELECTROPHORESIS; ARTICLE; CELL CULTURE; CELL FUNCTION; CONTROLLED STUDY; CYTOLYSIS; DOT HYBRIDIZATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTE FUNCTION AND CHARACTERISTICS; FLOW CYTOMETRY; GARDNERELLA VAGINALIS; HEMOLYSIS; NONHUMAN; OLIGOMERIZATION; PATHOGENESIS; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; ADULT; ANIMAL; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; ERYTHROCYTE; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; MOUSE;

BACTERIA (MICROORGANISMS); GARDNERELLA VAGINALIS; STREPTOCOCCUS INTERMEDIUS;

ADULT; ANIMALS; ANTIGENS, CD59; BACTERIAL PROTEINS; BACTERIAL TOXINS; BACTERIOCINS; CELLS, CULTURED; CHO CELLS; CHOLESTEROL; CRICETULUS; CYTOTOXINS; ERYTHROCYTES; HELA CELLS; HUMANS; MICE; STREPTOLYSINS;

EID: 84921773035     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins7010110     Document Type: Article

References (42)

1. Tweten, R.K. Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect. Immun. 2005, 73, 6199-6209.
2. Los, F.C.O.; Randis, T.M.; Aroian, R.V.; Ratner, A.J. Role of pore-forming toxins in bacterial infectious diseases. Microbiol. Mol. Biol. Rev. 2013, 44, 173-207.
3. Ramachandran, R.; Tweten, R.K.; Johnson, A.E. Membrane-dependent conformational changes initiate cholesterol-dependent cytolysin oligomerization and intersubunit β-strand alignment. Nat. Struct. Mol. Biol. 2004, 11, 697-705.
4. Paul, K.; Chattopadhyay, K. Single point mutation in Vibrio cholera cytolysin compromises the membrane pore-formation mechanism of the toxin. FEBS J. 2012, 279, 4039-4051.
5. Palmer, M.; Harris, R.; Freytag, C.; Kehoe, M.; Tranum-Jensen, J.; Bhakdi, S. Assembly mechanism of the oligomeric streptolysin O pore: The early membrane lesion is lined by a free edge of the lipid membrane and is extended gradually during oligomerization. EMBO J. 1998, 17, 1598-1605.
6. Sonnen, A.F.; Plitzko, J.M.; Gilbert, R.J. Incomplete pneumolysin oligomers form membrane pores. Open Biol. 2014, 4, 140044.
7. Bavdek, A.; Kostanjšek, R.; Antonini, V.; Lakey, J.H.; Dalla Serra, M.; Gilbert, R.J.; Anderluh, G. pH dependence of listeriolysin O aggregation and pore-forming ability. FEBS J. 2012, 279, 126-141.
8. Flanagan, J.J.; Tweten, R.K.; Johnson, A.E.; Heuck, A.P. Cholesterol exposure at the membrane surface is necessary and sufficient to trigger perfringolysin O binding. Biochemistry 2009, 48, 3977-3987.
9. Farrand, A.J.; LaChapelle, S.; Hotze, E.M.; Johnson, A.E.; Tweten, R.K. Only two amino acids are essential for cytolytic toxin recognition of cholesterol at the membrane surface. Proc. Natl. Acad. Sci. USA 2010, 107, 4341-4346.
10. Heuck, A.P.; Hotze, E.M.; Tweten, R.K.; Johnson, A.E. Mechanism of membrane insertion of a multimeric beta-barrel protein: Perfringolysin O creates a pore using ordered and coupled conformational changes. Mol. Cell 2000, 6, 1233-1242.
11. Hotze, E.M.; Wilson-Kubalek, E.; Farrand, A.J.; Bentsen, L.; Parker, M.W.; Johnson, A.E.; Tweten, R.K. Monomer-monomer interactions propagate structural transitions necessary for pore formation by the cholesterol-dependent cytolysins. J. Biol. Chem. 2012, 287, 24534-24543.
12. Giddings, K.S.; Zhao, J.; Sims, P.J.; Tweten, R.K. Human CD59 is a receptor for the cholesterol-dependent cytolysin intermedilysin. Nat. Struct. Mol. Biol. 2004, 11, 1173-1178.
13. Soltani, C.E.; Hotze, E.M.; Johnson, A.E.; Tweten, R.K. Specific protein-membrane contacts are required for prepore and pore assembly by a cholesterol-dependent cytolysin. J. Biol. Chem. 2007, 282, 15709-15716.
14. Rollins, S.A.; Sims, P.J. The complement-inhibitory activity of CD59 resides in its capacity to block incorporation of C9 into membrane C5b-9. J. Immunol 1990, 144, 3478−3483.
15. Kim, D.D.; Song, W.C. Membrane complement regulatory proteins. Clin. Immunol. 2006, 118, 127-136.
16. LaChapelle, S.; Tweten, R.K.; Hotze, E.M. Intermedilysin-receptor interactions during assembly of the pore complex. J. Biol. Chem. 2009, 284, 12719-12726.
17. Nagamune, H.; Ohnishi, C.; Katsuura, A.; Fushitani, K.; Whiley, R.A.; Tsuji, A.; Matsuda, Y. Intermedilysin, a novel cytotoxin specific for human cells secreted by Streptococcus intermedius UNS46 isolated from a human liver abscess. Infect. Immun. 1996, 64, 3093-3100.
18. Gelber, S.E.; Aguilar, J.L.; Lewis, K.L.; Ratner, A.J. Functional and phylogenetic characterization of vaginolysin, the human-specific cytolysin from Gardnerella vaginalis. J. Bacteriol. 2008, 190, 3896-3903.
19. Wickham, S.E.; Hotze, E.M.; Farrand, A.J.; Polekhina, G.; Nero, T.L.; Tomlinson, S.; Parker, M.W.; Tweten, R.K. Mapping the intermedilysin-human CD59 receptor interface reveals a deep correspondence with the binding site on CD59 for complement binding proteins C8α and C9. J. Biol. Chem. 2011, 286, 20952-20962.
20. Menard, J.P.; Fenollar, F.; Henry, M.; Bretelle, F.; Raoult, D. Molecular quantification of Gardnerella vaginalis and Atopobium vaginae loads to predict bacterial vaginosis. Clin. Infect. Dis. 2008, 47, 33-43.
21. Zvirbliene, A.; Pleckaityte, M.; Lasickiene, R.; Kucinskaite-Kodze, I.; Zvirblis, G. Production and characterization of monoclonal antibodies against vaginolysin: Mapping of a region critical for its cytolytic activity. Toxicon 2010, 56, 19-28.
22. Pleckaityte, M.; Janulaitiene, M.; Lasickiene, R.; Zvirbliene, A. Genetic and biochemical diversity of Gardnerella vaginalis strains isolated from women with bacterial vaginosis. FEMS Immunol. Med. Microbiol. 2012, 65, 69-77.
23. Tabata, A.; Ohkura, K.; Ohkubo, Y.; Tomoyasu, T.; Ohkuni, H.; Whiley, R.A.; Nagamune, H. The diversity of receptor recognition in cholesterol dependent cytolysins. Microbiol. Immunol. 2014, 58, 155-171.
24. Budvytyte, R.; Pleckaityte, M.; Zvirbliene, A.; Vanderah, D.J.; Valincius, G. Reconstitution of cholesterol-dependent vaginolysin into tethered phospholipid bilayers: Implications for bioanalysis. PLoS One 2013, 8, e82536.
25. Gilbert, N.M.; Lewis, W.G.; Lewis, A.L. Clinical features of bacterial vaginosis in a murine model of vaginal infection with Gardnerella vaginalis. PLoS One 2013, 8, e59539.
26. Dowd, K.J.; Tweten, R.K. The cholesterol-dependent cytolysin signature motif: A critical element in the allosteric pathway that couples membrane binding to pore assembly. PLoS Pathog. 2012, 8, e1002787.
27. Shepard, L.A.; Shatursky, O.; Johnson, A.E.; Tweten, R.K. The mechanism of pore assembly for a cholesterol-dependent cytolysin: Formation of a large prepore complex precedes the insertion of the transmembrane beta-hairpins. Biochemistry 2000, 39, 10284-10293.
28. Hotze, E.M.; Tweten, R.K. Membrane assembly of the cholesterol-dependent cytolysin pore complex. Biochim. Biophys. Acta 2012, 1818, 1028-1038.
29. Polekhina, G.; Giddings, K.S.; Tweten, R.K.; Parker, M.W. Insights into the action of the superfamily of cholesterol-dependent cytolysins from studies of intermedilysin. Proc. Natl. Acad. Sci. USA 2005, 102, 600-605.
30. Farrand, S.; Hotze, E.; Friese, P.; Hollingshead, S.K.; Smith, D.F.; Cummings, R.D.; Dale, G.L.; Tweten, R.K. Characterization of a streptococcal cholesterol-dependent cytolysin with a Lewis y and b specific lectin domain. Biochemistry 2008, 47, 7097-7107.
31. Waheed, A.A.; Shimada, Y.; Heijnen, H.F.; Nakamura, M.; Inomata, M.; Hayashi, M.; Iwashita, S.; Slot, J.W.; Ohno-Iwashita, Y. Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts). Proc. Natl. Acad. Sci. USA 2001, 98, 4926-4931.
32. Gekara, N.O.; Jacobs, T.; Chakraborty, T.; Weiss, S. The cholesterol-dependent cytolysin listeriolysin O aggregates rafts via oligomerization. Cell Microbiol. 2005, 7, 1345-1356.
33. Taylor, S.D.; Sanders, M.E.; Tullos, N.A.; Stray, S.J.; Norcross, E.W.; McDaniel, L.S.; Marquart, M.E. The cholesterol-dependent cytolysin pneumolysin from Streptococcus pneumoniae binds to lipid raft microdomains in human corneal epithelial cells. PLoS One 2013, 8, e61300.
34. Nelson, L.D.; Chiantia, S.; London, E. Perfringolysin O association with ordered lipid domains: Implications for transmembrane protein raft affinity. Biophys. J. 2010, 99, 3255-3263.
35. Johnson, B.B.; Moe, P.C.; Wang, D.; Rossi, K.; Trigatti, B.L.; Heuck, A.P. Modifications in perfringolysin O domain 4 alter the cholesterol concentration threshold required for binding. Biochemistry 2012, 51, 3373-3382.
36. Kimberley, F.C.; Sivasankar, B.; Morgan, P.B. Alternative roles for CD59. Mol. Immunol. 2007, 44, 73-81.
37. LaRocca, T.J.; Stivison, E.A.; Hod, E.A.; Spitalnik, S.L.; Cowan, P.J.; Randis, T.M.; Ratner, A.J. Human-specific bacterial pore-forming toxins induce programmed necrosis in erythrocytes. MBio 2014, 5, e01251-14.
38. Yu, J.; Abagyan, R.; Dong, S.; Gilbert, A.; Nussenzweig, V.; Tomlinson, S. Mapping of the active site of CD59. J. Exp. Med. 1997, 185, 745-753.
39. Cizas, P.; Budvytyte, R.; Morkuniene, R.; Moldovan, R.; Broccio, M.; Lösche, M.; Niaura, G.; Valincius, G.; Borutaite, V. Size-dependent neurotoxicity of beta-amyloid oligomers. Arch. Biochem. Biophys. 2010, 496, 84-92.
40. Söding, J.; Biegert, A.; Lupas, A.N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acid Res. 2005, 33, W244-W248.
41. Rossjohn, J.; Feil, S.C.; McKinstry, W.J.; Tweten, R.K.; Parker, M.W. Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form. Cell 1997, 89, 685-692.
42. Sippl, M.J. Recognition of errors in three-dimensional structures of proteins. Proteins 1993, 17, 355-362.