Structural Basis for Recognition of the Pore-Forming Toxin Intermedilysin by Human Complement Receptor CD59

Cell Reports

Volumn 3, Issue 5, 2013, Pages 1369-1377

  Johnson, Steven ^a   Brooks, Nicholas J ^b   Smith, Richard A G ^c   Lea, Susan M ^a   Bubeck, Doryen ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c GUY S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD59 ANTIGEN; CYTOLYSIN; INTERMEDILYSIN; UNCLASSIFIED DRUG; BACTERIOCIN; CHOLESTEROL; INTERMEDILYSIN PROTEIN, STREPTOCOCCUS INTERMEDIUS; LIPID BILAYER; PROTEIN BINDING;

ARTICLE; BINDING SITE; COMPLEMENT ACTIVATION; COMPLEMENT INHIBITION; COMPLEX FORMATION; CRYSTAL STRUCTURE; LIPID BILAYER; MEMBRANE FORMATION; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN FUNCTION; STRUCTURE ANALYSIS; CHEMISTRY; HUMAN; METABOLISM; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS);

ANTIGENS, CD59; BACTERIOCINS; BINDING SITES; CHOLESTEROL; CRYSTALLOGRAPHY, X-RAY; HUMANS; LIPID BILAYERS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84878591801     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.04.029     Document Type: Article

References (48)

1. Adams P.D., Afonine P.V., Bunkóczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:213-221.
2. Aleshin A.E., Schraufstatter I.U., Stec B., Bankston L.A., Liddington R.C., DiScipio R.G. Structure of complement C6 suggests a mechanism for initiation and unidirectional, sequential assembly of membrane attack complex (MAC). J.Biol. Chem. 2012, 287:10210-10222.
3. Anstee D.J. The nature and abundance of human red cell surface glycoproteins. J.Immunogenet. 1990, 17:219-225.
4. Bodian D.L., Davis S.J., Morgan B.P., Rushmere N.K. Mutational analysis of the active site and antibody epitopes of the complement-inhibitory glycoprotein, CD59. J.Exp. Med. 1997, 185:507-516.
5. Bourdeau R.W., Malito E., Chenal A., Bishop B.L., Musch M.W., Villereal M.L., Chang E.B., Mosser E.M., Rest R.F., Tang W.J. Cellular functions and X-ray structure of anthrolysin O, a cholesterol-dependent cytolysin secreted by Bacillus anthracis. J.Biol. Chem. 2009, 284:14645-14656.
6. Czajkowsky D.M., Hotze E.M., Shao Z., Tweten R.K. Vertical collapse of a cytolysin prepore moves its transmembrane beta-hairpins to the membrane. EMBO J. 2004, 23:3206-3215.
7. 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.
8. Emsley P., Lohkamp B., Scott W.G., Cowtan K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:486-501.
9. Farkas I., Baranyi L., Ishikawa Y., Okada N., Bohata C., Budai D., Fukuda A., Imai M., Okada H. CD59 blocks not only the insertion of C9 into MAC but inhibits ion channel formation by homologous C5b-8 as well as C5b-9. J.Physiol. 2002, 539:537-545.
10. Fishelson Z., Donin N., Zell S., Schultz S., Kirschfink M. Obstacles to cancer immunotherapy: expression of membrane complement regulatory proteins (mCRPs) in tumors. Mol. Immunol. 2003, 40:109-123.
11. Fletcher C.M., Harrison R.A., Lachmann P.J., Neuhaus D. Structure of a soluble, glycosylated form of the human complement regulatory protein CD59. Structure 1994, 2:185-199.
12. Fraser D.A., Harris C.L., Williams A.S., Mizuno M., Gallagher S., Smith R.A., Morgan B.P. Generation of a recombinant, membrane-targeted form of the complement regulator CD59: activity invitro and invivo. J.Biol. Chem. 2003, 278:48921-48927.
13. 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.
14. Gorter A., Meri S. Immune evasion of tumor cells using membrane-bound complement regulatory proteins. Immunol. Today 1999, 20:576-582.
15. Hadders M.A., Beringer D.X., Gros P. Structure of C8alpha-MACPF reveals mechanism of membrane attack in complement immune defense. Science 2007, 317:1552-1554.
16. Hadders M.A., Bubeck D., Roversi P., Hakobyan S., Forneris F., Morgan B.P., Pangburn M.K., Llorca O., Lea S.M., Gros P. Assembly and regulation of the membrane attack complex based on structures of C5b6 and sC5b9. Cell Rep 2012, 1:200-207.
17. Hill A., Ridley S.H., Esser D., Oldroyd R.G., Cullen M.J., Kareclas P., Gallagher S., Smith G.P., Richards S.J., White J., et al. Protection of erythrocytes from human complement-mediated lysis by membrane-targeted recombinant soluble CD59: a new approach to PNH therapy. Blood 2006, 107:2131-2137.
18. 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.
19. Huang Y., Smith C.A., Song H., Morgan B.P., Abagyan R., Tomlinson S. Insights into the human CD59 complement binding interface toward engineering new therapeutics. J.Biol. Chem. 2005, 280:34073-34079.
20. Huang Y., Qiao F., Abagyan R., Hazard S., Tomlinson S. Defining the CD59-C9 binding interaction. J.Biol. Chem. 2006, 281:27398-27404.
21. Hughes T.R., Ross K.S., Cowan G.J., Sivasankar B., Harris C.L., Mitchell T.J., Morgan B.P. Identification of the high affinity binding site in the Streptococcus intermedius toxin intermedilysin for its membrane receptor, the human complement regulator CD59. Mol. Immunol. 2009, 46:1561-1567.
22. Kieffer B., Driscoll P.C., Campbell I.D., Willis A.C., van der Merwe P.A., Davis S.J. Three-dimensional solution structure of the extracellular region of the complement regulatory protein CD59, a new cell-surface protein domain related to snake venom neurotoxins. Biochemistry 1994, 33:4471-4482.
23. Koçer A., Walko M., Feringa B.L. Synthesis and utilization of reversible and irreversible light-activated nanovalves derived from the channel protein MscL. Nat. Protoc. 2007, 2:1426-1437.
24. LaChapelle S., Tweten R.K., Hotze E.M. Intermedilysin-receptor interactions during assembly of the pore complex: assembly intermediates increase host cell susceptibility to complement-mediated lysis. J.Biol. Chem. 2009, 284:12719-12726.
25. Law R.H., Lukoyanova N., Voskoboinik I., Caradoc-Davies T.T., Baran K., Dunstone M.A., D'Angelo M.E., Orlova E.V., Coulibaly F., Verschoor S., et al. The structural basis for membrane binding and pore formation by lymphocyte perforin. Nature 2010, 468:447-451.
26. Leath K.J., Johnson S., Roversi P., Hughes T.R., Smith R.A., Mackenzie L., Morgan B.P., Lea S.M. High-resolution structures of bacterially expressed soluble human CD59. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2007, 63:648-652.
27. Lebedev A.A., Vagin A.A., Murshudov G.N. Intensity statistics in twinned crystals with examples from the PDB. Acta Crystallogr. D Biol. Crystallogr. 2006, 62:83-95.
28. Lehto T., Meri S. Interactions of soluble CD59 with the terminal complement complexes. CD59 and C9 compete for a nascent epitope on C8. J.Immunol. 1993, 151:4941-4949.
29. Lehto M.T., Sharom F.J. Proximity of the protein moiety of a GPI-anchored protein to the membrane surface: a FRET study. Biochemistry 2002, 41:8368-8376.
30. Lovelace L.L., Cooper C.L., Sodetz J.M., Lebioda L. Structure of human C8 protein provides mechanistic insight into membrane pore formation by complement. J.Biol. Chem. 2011, 286:17585-17592.
31. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., Read R.J. Phaser crystallographic software. J.Appl. Cryst. 2007, 40:658-674.
32. Meri S., Morgan B.P., Davies A., Daniels R.H., Olavesen M.G., Waldmann H., Lachmann P.J. Human protectin (CD59), an 18,000-20,000 MW complement lysis restricting factor, inhibits C5b-8 catalysed insertion of C9 into lipid bilayers. Immunology 1990, 71:1-9.
33. Meri S., Waldmann H., Lachmann P.J. Distribution of protectin (CD59), a complement membrane attack inhibitor, in normal human tissues. Lab. Invest. 1991, 65:532-537.
34. 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.
35. Nagamune H., Ohkura K., Sukeno A., Cowan G., Mitchell T.J., Ito W., Ohnishi O., Hattori K., Yamato M., Hirota K., et al. The human-specific action of intermedilysin, a homolog of streptolysin O, is dictated by domain 4 of the protein. Microbiol. Immunol. 2004, 48:677-692.
36. Ninomiya H., Sims P.J. The human complement regulatory protein CD59 binds to the alpha-chain of C8 and to the "b"domain of C9. J.Biol. Chem. 1992, 267:13675-13680.
37. 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.
38. 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.
39. 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.
40. Rossjohn J., Polekhina G., Feil S.C., Morton C.J., Tweten R.K., Parker M.W. Structures of perfringolysin O suggest a pathway for activation of cholesterol-dependent cytolysins. J.Mol. Biol. 2007, 367:1227-1236.
41. Rudd P.M., Morgan B.P., Wormald M.R., Harvey D.J., van den Berg C.W., Davis S.J., Ferguson M.A., Dwek R.A. The glycosylation of the complement regulatory protein, human erythrocyte CD59. J.Biol. Chem. 1997, 272:7229-7244.
42. 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.
43. Soltani C.E., Hotze E.M., Johnson A.E., Tweten R.K. Structural elements of the cholesterol-dependent cytolysins that are responsible for their cholesterol-sensitive membrane interactions. Proc. Natl. Acad. Sci. USA 2007, 104:20226-20231.
44. Tilley S.J., Orlova E.V., Gilbert R.J., Andrew P.W., Saibil H.R. Structural basis of pore formation by the bacterial toxin pneumolysin. Cell 2005, 121:247-256.
45. Tweten R.K., Parker M.W., Johnson A.E. The cholesterol-dependent cytolysins. Curr. Top. Microbiol. Immunol. 2001, 257:15-33.
46. 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 C8alpha and C9. J.Biol. Chem. 2011, 286:20952-20962.
47. Winter G. xia2: an expert system for macromolecular crystallography data reduction. J.Appl. Cryst. 2010, 43:186-190.
48. Xu L., Huang B., Du H., Zhang X.C., Xu J., Li X., Rao Z. Crystal structure of cytotoxin protein suilysin from Streptococcus suis. Protein Cell 2010, 1:96-105.