The making of a macromolecular machine: Assembly of the membrane attack complex

Biochemistry

Volumn 53, Issue 12, 2014, Pages 1908-1915

  Bubeck, Doryen ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY;

CELLULAR ASSAYS; CYTOTOXIC; MEMBRANE ATTACK COMPLEXES; MOLECULAR MECHANISM; PORE FORMATION; PROTEIN COMPOSITION; TARGET CELLS;

CHEMISTRY;

COMPLEMENT MEMBRANE ATTACK COMPLEX;

ARTICLE; BINDING SITE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CYTOLYSIS; ENDOTHELIUM CELL; EPITHELIUM CELL; HEMOLYSIS; HOST CELL; HUMAN; LEUKOCYTE; LIPID BILAYER; MUTAGENESIS; NONHUMAN; OLIGOMERIZATION; PRECURSOR; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; TARGET CELL;

ANIMALS; COMPLEMENT MEMBRANE ATTACK COMPLEX; HUMANS; MACROMOLECULAR SUBSTANCES; NEOPLASMS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84898071022     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500157z     Document Type: Article

References (82)

1. Tschopp, J. (1984) Ultrastructure of the membrane attack complex of complement. Heterogeneity of the complex caused by different degree of C9 polymerization J. Biol. Chem. 259, 7857-7863
2. Podack, E. R., Kolb, W. P., and Muller-Eberhard, H. J. (1976) The C5b-9 complex: Subunit composition of the classical and alternative pathway-generated complex J. Immunol. 116, 1431-1434
3. DiScipio, R. G., Smith, C. A., Muller-Eberhard, H. J., and Hugli, T. E. (1983) The activation of human complement component C5 by a fluid phase C5 convertase J. Biol. Chem. 258, 10629-10636
4. Guo, R. F. and Ward, P. A. (2005) Role of C5a in inflammatory responses Annu. Rev. Immunol. 23, 821-852
5. Manthey, H. D., Woodruff, T. M., Taylor, S. M., and Monk, P. N. (2009) Complement component 5a (C5a) Int. J. Biochem. Cell Biol. 41, 2114-2117
6. Fernandez, H. N. and Hugli, T. E. (1978) Primary structural analysis of the polypeptide portion of human C5a anaphylatoxin. Polypeptide sequence determination and assignment of the oligosaccharide attachment site in C5a J. Biol. Chem. 253, 6955-6964
7. Cooper, N. R. and Muller-Eberhard, H. J. (1970) The reaction mechanism of human C5 in immune hemolysis J. Exp. Med. 132, 775-793
8. DiScipio, R. G. (1981) The conversion of human complement component C5 into fragment C5b by the alternative-pathway C5 convertase Biochem. J. 199, 497-504
9. Preissner, K. T., Podack, E. R., and Muller-Eberhard, H. J. (1985) The membrane attack complex of complement: Relation of C7 to the metastable membrane binding site of the intermediate complex C5b-7 J. Immunol. 135, 445-451
10. DiScipio, R. G., Chakravarti, D. N., Muller-Eberhard, H. J., and Fey, G. H. (1988) The structure of human complement component C7 and the C5b-7 complex J. Biol. Chem. 263, 549-560
11. Podack, E. R., Tschoop, J., and Muller-Eberhard, H. J. (1982) Molecular organization of C9 within the membrane attack complex of complement. Induction of circular C9 polymerization by the C5b-8 assembly J. Exp. Med. 156, 268-282
12. Steckel, E. W., Welbaum, B. E., and Sodetz, J. M. (1983) Evidence of direct insertion of terminal complement proteins into cell membrane bilayers during cytolysis. Labeling by a photosensitive membrane probe reveals a major role for the eighth and ninth components J. Biol. Chem. 258, 4318-4324
13. Tschopp, J., Podack, E. R., and Muller-Eberhard, H. J. (1982) Ultrastructure of the membrane attack complex of complement: Detection of the tetramolecular C9-polymerizing complex C5b-8 Proc. Natl. Acad. Sci. U.S.A. 79, 7474-7478
14. Shevach, E. M. (2005) Complement Curr. Protoc. Immunol. 69, 1-4
15. Mollnes, T. E., Lea, T., Harboe, M., and Tschopp, J. (1985) Monoclonal antibodies recognizing a neoantigen of poly(C9) detect the human terminal complement complex in tissue and plasma Scand. J. Immunol. 22, 183-195
16. Kolb, W. P. and Muller-Eberhard, H. J. (1975) Neoantigens of the membrane attack complex of human complement Proc. Natl. Acad. Sci. U.S.A. 72, 1687-1689
17. Hadders, M. A., Beringer, D. X., and Gros, P. (2007) Structure of C8α-MACPF reveals mechanism of membrane attack in complement immune defense Science 317, 1552-1554
18. Hadders, M. A., Bubeck, D., Roversi, P., Hakobyan, S., Forneris, F., Morgan, B. P., Pangburn, M. K., Llorca, O., Lea, S. M., and Gros, P. (2012) Assembly and regulation of the membrane attack complex based on structures of C5b6 and sC5b9 Cell Rep. 1, 200-207
19. Lovelace, L. L., Cooper, C. L., Sodetz, J. M., and Lebioda, L. (2011) Structure of human C8 protein provides mechanistic insight into membrane pore formation by complement J. Biol. Chem. 286, 17585-17592
20. Aleshin, A. E., Discipio, R. G., Stec, B., and Liddington, R. C. (2012) Crystal structure of c5b-6 suggests structural basis for priming assembly of the membrane attack complex J. Biol. Chem. 287, 19642-19652
21. Aleshin, A. E., Schraufstatter, I. U., Stec, B., Bankston, L. A., Liddington, R. C., and DiScipio, R. G. (2012) Structure of complement C6 suggests a mechanism for initiation and unidirectional, sequential assembly of membrane attack complex (MAC) J. Biol. Chem. 287, 10210-10222
22. Bubeck, D., Roversi, P., Donev, R., Morgan, B. P., Llorca, O., and Lea, S. M. (2011) Structure of human complement C8, a precursor to membrane attack J. Mol. Biol. 405, 325-330
23. Janssen, B. J., Huizinga, E. G., Raaijmakers, H. C., Roos, A., Daha, M. R., Nilsson-Ekdahl, K., Nilsson, B., and Gros, P. (2005) Structures of complement component C3 provide insights into the function and evolution of immunity Nature 437, 505-511
24. Fredslund, F., Laursen, N. S., Roversi, P., Jenner, L., Oliveira, C. L., Pedersen, J. S., Nunn, M. A., Lea, S. M., Discipio, R., Sottrup-Jensen, L., and Andersen, G. R. (2008) Structure of and influence of a tick complement inhibitor on human complement component 5 Nat. Immunol. 9, 753-760
25. Janssen, B. J., Christodoulidou, A., McCarthy, A., Lambris, J. D., and Gros, P. (2006) Structure of C3b reveals conformational changes that underlie complement activity Nature 444, 213-216
26. Stewart, J. L. and Sodetz, J. M. (1985) Analysis of the specific association of the eighth and ninth components of human complement: Identification of a direct role for the alpha subunit of C8 Biochemistry 24, 4598-4602
27. Brannen, C. L. and Sodetz, J. M. (2007) Incorporation of human complement C8 into the membrane attack complex is mediated by a binding site located within the C8β MACPF domain Mol. Immunol. 44, 960-965
28. Slade, D. J., Chiswell, B., and Sodetz, J. M. (2006) Functional studies of the MACPF domain of human complement protein C8α reveal sites for simultaneous binding of C8β, C8γ, and C9 Biochemistry 45, 5290-5296
29. Scibek, J. J., Plumb, M. E., and Sodetz, J. M. (2002) Binding of human complement C8 to C9: Role of the N-terminal modules in the C8α subunit Biochemistry 41, 14546-14551
30. Musingarimi, P., Plumb, M. E., and Sodetz, J. M. (2002) Interaction between the C8α-γ and C8β subunits of human complement C8: Role of the C8β N-terminal thrombospondin type 1 module and membrane attack complex/perforin domain Biochemistry 41, 11255-11260
31. Plumb, M. E. and Sodetz, J. M. (2000) An indel within the C8α subunit of human complement C8 mediates intracellular binding of C8γ and formation of C8α-γ Biochemistry 39, 13078-13083
32. Lovelace, L. L., Chiswell, B., Slade, D. J., Sodetz, J. M., and Lebioda, L. (2008) Crystal structure of complement protein C8γ in complex with a peptide containing the C8γ binding site on C8α: Implications for C8γ ligand binding Mol. Immunol. 45, 750-756
33. Parker, C. L. and Sodetz, J. M. (2002) Role of the human C8 subunits in complement-mediated bacterial killing: Evidence that C8γ is not essential Mol. Immunol. 39, 453-458
34. Slade, D. J., Lovelace, L. L., Chruszcz, M., Minor, W., Lebioda, L., and Sodetz, J. M. (2008) Crystal structure of the MACPF domain of human complement protein C8α in complex with the C8γ subunit J. Mol. Biol. 379, 331-342
35. Phelan, M. M., Thai, C. T., Soares, D. C., Ogata, R. T., Barlow, P. N., and Bramham, J. (2009) Solution structure of factor I-like modules from complement C7 reveals a pair of follistatin domains in compact pseudosymmetric arrangement J. Biol. Chem. 284, 19637-19649
36. 15N resonance assignments of the complement control protein modules of the complement component C7 Biomol. NMR Assignments 7, 285-288
37. Feil, S. C., Ascher, D. B., Kuiper, M. J., Tweten, R. K., and Parker, M. W. (2014) Structural Studies of Streptococcus pyogenes Streptolysin O Provide Insights into the Early Steps of Membrane Penetration J. Mol. Biol. 426, 785-792
38. Polekhina, G., Giddings, K. S., Tweten, R. K., and Parker, M. W. (2005) Insights into the action of the superfamily of cholesterol-dependent cytolysins from studies of intermedilysin Proc. Natl. Acad. Sci. U.S.A. 102, 600-605
39. Rossjohn, J., Feil, S. C., McKinstry, W. J., Tweten, R. K., and Parker, M. W. (1997) Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form Cell 89, 685-692
40. Rossjohn, J., Polekhina, G., Feil, S. C., Morton, C. J., Tweten, R. K., and Parker, M. W. (2007) Structures of perfringolysin O suggest a pathway for activation of cholesterol-dependent cytolysins J. Mol. Biol. 367, 1227-1236
41. Shatursky, O., Heuck, A. P., Shepard, L. A., Rossjohn, J., Parker, M. W., Johnson, A. E., and Tweten, R. K. (1999) The mechanism of membrane insertion for a cholesterol-dependent cytolysin: A novel paradigm for pore-forming toxins Cell 99, 293-299
42. Heuck, A. P., Hotze, E. M., Tweten, R. K., and Johnson, A. E. (2000) Mechanism of membrane insertion of a multimeric β-barrel protein: Perfringolysin O creates a pore using ordered and coupled conformational changes Mol. Cell 6, 1233-1242
43. Shepard, L. A., Heuck, A. P., Hamman, B. D., Rossjohn, J., Parker, M. W., Ryan, K. R., Johnson, A. E., and Tweten, R. K. (1998) Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens perfringolysin O: An α-helical to β-sheet transition identified by fluorescence spectroscopy Biochemistry 37, 14563-14574
44. Weiland, M. H., Qian, Y., and Sodetz, J. M. (2014) Membrane pore formation by human complement: Functional importance of the transmembrane β-hairpin (TMH) segments of C8α and C9 Mol. Immunol. 57, 310-316
45. Tilley, S. J., Orlova, E. V., Gilbert, R. J., Andrew, P. W., and Saibil, H. R. (2005) Structural basis of pore formation by the bacterial toxin pneumolysin Cell 121, 247-256
46. Hotze, E. M., Wilson-Kubalek, E., Farrand, A. J., Bentsen, L., Parker, M. W., Johnson, A. E., and Tweten, R. K. (2012) Monomer-monomer interactions propagate structural transitions necessary for pore formation by the cholesterol-dependent cytolysins J. Biol. Chem. 287, 24534-24543
47. Dowd, K. J. and Tweten, R. K. (2012) The cholesterol-dependent cytolysin signature motif: A critical element in the allosteric pathway that couples membrane binding to pore assembly PLoS Pathog. 8, e1002787
48. Giddings, K. S., Zhao, J., Sims, P. J., and Tweten, R. K. (2004) Human CD59 is a receptor for the cholesterol-dependent cytolysin intermedilysin Nat. Struct. Mol. Biol. 11, 1173-1178
49. Soltani, C. E., Hotze, E. M., Johnson, A. E., and Tweten, R. K. (2007) Specific protein-membrane contacts are required for prepore and pore assembly by a cholesterol-dependent cytolysin J. Biol. Chem. 282, 15709-15716
50. LaChapelle, S., Tweten, R. K., and Hotze, E. M. (2009) Intermedilysin-receptor interactions during assembly of the pore complex: Assembly intermediates increase host cell susceptibility to complement-mediated lysis J. Biol. Chem. 284, 12719-12726
51. Johnson, S., Brooks, N. J., Smith, R. A., Lea, S. M., and Bubeck, D. (2013) Structural basis for recognition of the pore-forming toxin intermedilysin by human complement receptor CD59 Cell Rep. 3, 1369-1377
52. Wickham, S. E., Hotze, E. M., Farrand, A. J., Polekhina, G., Nero, T. L., Tomlinson, S., Parker, M. W., and Tweten, R. K. (2011) 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. 286, 20952-20962
53. Law, R. H., Lukoyanova, N., Voskoboinik, I., Caradoc-Davies, T. T., Baran, K., Dunstone, M. A., DAngelo, M. E., Orlova, E. V., Coulibaly, F., Verschoor, S., Browne, K. A., Ciccone, A., Kuiper, M. J., Bird, P. I., Trapani, J. A., Saibil, H. R., and Whisstock, J. C. (2010) The structural basis for membrane binding and pore formation by lymphocyte perforin Nature 468, 447-451
54. Kolb, W. P., Haxby, J. A., Arroyave, C. M., and Muller-Eberhard, H. J. (1973) The membrane attack mechanism of complement. Reversible interactions among the five native components in free solution J. Exp. Med. 138, 428-437
55. DiScipio, R. G. (1992) Formation and structure of the C5b-7 complex of the lytic pathway of complement J. Biol. Chem. 267, 17087-17094
56. Schonermark, S., Rauterberg, E. W., Shin, M. L., Loke, S., Roelcke, D., and Hansch, G. M. (1986) Homologous species restriction in lysis of human erythrocytes: A membrane-derived protein with C8-binding capacity functions as an inhibitor J. Immunol. 136, 1772-1776
57. Nemerow, G. R., Yamamoto, K. I., and Lint, T. F. (1979) Restriction of complement-mediated membrane damage by the eighth component of complement: A dual role for C8 in the complement attack sequence J. Immunol. 123, 1245-1252
58. Podack, E. R., Kolb, W. P., and Muller-Eberhard, H. J. (1977) The SC5b-7 complex: Formation, isolation, properties, and subunit composition J. Immunol. 119, 2024-2029
59. Bhakdi, S. and Roth, M. (1981) Fluid-phase SC5b-8 complex of human complement: Generation and isolation from serum J. Immunol. 127, 576-580
60. Preissner, K. P., Podack, E. R., and Muller-Eberhard, H. J. (1989) SC5b-7, SC5b-8 and SC5b-9 complexes of complement: Ultrastructure and localization of the S-protein (vitronectin) within the macromolecules Eur. J. Immunol. 19, 69-75
61. Bhakdi, S. and Tranum-Jensen, J. (1982) Hydrophilic-amphiphilic transition of the terminal SC5b-8 complement complex through tryptic modification: Biochemical and ultrastructural studies Mol. Immunol. 19, 1167-1177
62. Meri, S., Morgan, B. P., Davies, A., Daniels, R. H., Olavesen, M. G., Waldmann, H., and Lachmann, P. J. (1990) Human protectin (CD59), an 18,000-20,000 MW complement lysis restricting factor, inhibits C5b-8 catalysed insertion of C9 into lipid bilayers Immunology 71, 1-9
63. Farkas, I., Baranyi, L., Ishikawa, Y., Okada, N., Bohata, C., Budai, D., Fukuda, A., Imai, M., and Okada, H. (2002) 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. 539, 537-545
64. Ninomiya, H. and Sims, P. J. (1992) The human complement regulatory protein CD59 binds to the α-chain of C8 and to the "b" domain of C9 J. Biol. Chem. 267, 13675-13680
65. Meri, S., Waldmann, H., and Lachmann, P. J. (1991) Distribution of protectin (CD59), a complement membrane attack inhibitor, in normal human tissues Lab. Invest. 65, 532-537
66. Leath, K. J., Johnson, S., Roversi, P., Hughes, T. R., Smith, R. A., Mackenzie, L., Morgan, B. P., and Lea, S. M. (2007) High-resolution structures of bacterially expressed soluble human CD59 Acta Crystallogr. F63, 648-652
67. Fletcher, C. M., Harrison, R. A., Lachmann, P. J., and Neuhaus, D. (1994) Structure of a soluble, glycosylated form of the human complement regulatory protein CD59 Structure 2, 185-199
68. Huang, Y., Qiao, F., Abagyan, R., Hazard, S., and Tomlinson, S. (2006) Defining the CD59-C9 binding interaction J. Biol. Chem. 281, 27398-27404
69. Huang, Y., Smith, C. A., Song, H., Morgan, B. P., Abagyan, R., and Tomlinson, S. (2005) Insights into the human CD59 complement binding interface toward engineering new therapeutics J. Biol. Chem. 280, 34073-34079
70. Bodian, D. L., Davis, S. J., Morgan, B. P., and Rushmere, N. K. (1997) Mutational analysis of the active site and antibody epitopes of the complement-inhibitory glycoprotein, CD59 J. Exp. Med. 185, 507-516
71. Kuijpers, T. W., Nguyen, M., Hopman, C. T., Nieuwenhuys, E., Dewald, G., Lankester, A. C., Roos, A., van der Ende, A., Fijen, C., and de Boer, M. (2010) Complement factor 7 gene mutations in relation to meningococcal infection and clinical recurrence of meningococcal disease Mol. Immunol. 47, 671-677
72. Zoppi, M., Weiss, M., Nydegger, U. E., Hess, T., and Spath, P. J. (1990) Recurrent meningitis in a patient with congenital deficiency of the C9 component of complement. First case of C9 deficiency in Europe Arch. Intern. Med. 150, 2395-2399
73. Arnold, D. F., Roberts, A. G., Thomas, A., Ferry, B., Morgan, B. P., and Chapel, H. (2009) A novel mutation in a patient with a deficiency of the eighth component of complement associated with recurrent meningococcal meningitis J. Clin. Immunol. 29, 691-695
74. Parker, C. J. (1996) Molecular basis of paroxysmal nocturnal hemoglobinuria Stem Cells 14, 396-411
75. Fishelson, Z., Donin, N., Zell, S., Schultz, S., and Kirschfink, M. (2003) Obstacles to cancer immunotherapy: Expression of membrane complement regulatory proteins (mCRPs) in tumors Mol. Immunol. 40, 109-123
76. Gorter, A. and Meri, S. (1999) Immune evasion of tumor cells using membrane-bound complement regulatory proteins Immunol. Today 20, 576-582
77. Doss, S., Garrett, Z., Sutcliffe, F., and Stevens, A. (2012) NICE guidance on rituximab for first-line treatment of symptomatic stage III-IV follicular lymphoma in previously untreated patients Lancet Oncol. 13, 128-130
78. Glennie, M. J., French, R. R., Cragg, M. S., and Taylor, R. P. (2007) Mechanisms of killing by anti-CD20 monoclonal antibodies Mol. Immunol. 44, 3823-3837
79. DAuria, F., Guariglia, R., Villani, O., Mansueto, G., Grieco, V., Zonno, A., Bianchino, G., Di Giovannantonio, L., Vita, G., and Musto, P. (2010) Modulation of CD20 antigen expression after rituximab treatment: A retrospective study in patients with chronic lymphocytic leukemia Clin. Ther. 32, 1911-1916
80. Ge, X., Wu, L., Hu, W., Fernandes, S., Wang, C., Li, X., Brown, J. R., and Qin, X. (2011) rILYd4, a human CD59 inhibitor, enhances complement-dependent cytotoxicity of ofatumumab against rituximab-resistant B-cell lymphoma cells and chronic lymphocytic leukemia Clin. Cancer Res. 17, 6702-6711
81. Hu, W., Ge, X., You, T., Xu, T., Zhang, J., Wu, G., Peng, Z., Chorev, M., Aktas, B. H., Halperin, J. A., Brown, J. R., and Qin, X. (2011) Human CD59 inhibitor sensitizes rituximab-resistant lymphoma cells to complement-mediated cytolysis Cancer Res. 71, 2298-2307
82. The PyMOL Molecular Graphics System, version 1.3r1 (2010) Schrodinger, LLC, Portland, OR.