Topology of the membrane-bound form of complement protein C9 probed by glycosylation mapping, anti-peptide antibody binding, and disulfide modification

Molecular Immunology

Volumn 47, Issue 7-8, 2010, Pages 1553-1560

  Rossi, Véronique ^a,b   Wang, Yunxia ^a,c   Esser, Alfred F ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^c PEL FREEZ Clinical Systems LLC   (United States)

Author keywords

(Poly)C9; Complement; Complement 9; MACPF; Membrane protein anchoring; Monotopic membrane protein

Indexed keywords

COMPLEMENT COMPONENT C8A; COMPLEMENT COMPONENT C9; CYSTEINE; METAL ION; PEPTIDE ANTIBODY;

ANTIGEN BINDING; ARTICLE; BACTERICIDAL ACTIVITY; BINDING AFFINITY; CONTROLLED STUDY; DISULFIDE BOND; EPITOPE MAPPING; FLOW CYTOMETRY; HEMOLYSIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COMPLEMENT C9; DISULFIDES; GLYCOSYLATION; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDE MAPPING; PEPTIDES; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT; SPODOPTERA;

EID: 77950626562     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2010.01.013     Document Type: Article

References (42)

1. Amiguet P., Brunner J., Tschopp J. The membrane attack complex of complement: lipid insertion of tubular and nontubular polymerized C9. Biochemistry 1985, 24:7328-7334.
2. Chang C.P., Husler T., Zhao J., Wiedmer T., Sims P.J. Identity of a peptide domain of human C9 that is bound by the cell-surface complement inhibitor CD59. J. Biol. Chem. 1994, 269:26424-26430.
3. Chen Q., Lord S.T., Lentz B.R. Construction, properties and specific fluorescent labeling of a bovine prothrombin mutant engineered with a free C-terminal cysteine. Protein Eng. 1996, 9:545-553.
4. Dankert J.R., Esser A.F. Proteolytic modification of human complement protein C9: loss of of poly(C9) and circular letion formation without impairment of function. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:2128-2132.
5. Dankert J.R., Esser A.F. Bacterial killing by complement C9-mediated killing in the absence of C5b-8. Biochem. J. 1987, 244:393-399.
6. DiScipio R.G., Gehring M.R., Podack E.R., Kan C.C., Hugli T.E., Fey G.H. Nucleotide sequence of cDNA and derived amino acid sequence of human complement component C9. Proc. Natl. Acad. Sci. U.S.A. 1984, 81:7298-7302.
7. Dupuis M., Peitsch M.C., Hamann U., Stanley K.K., Tschopp J. Mutations in the putative lipid-interaction domain of complement C9 result in defective secretion of the functional protein. Mol. Immunol. 1993, 30:95-100.
8. Esser A.F., Sodetz J.M. Membrane attack complex proteins C5b-6, C7, C8, and C9 of human complement. Methods Enzymol. 1988, 162:551-578.
9. Esser A.F. The membrane attack complex of complement, assembly, structure and cytotoxic activity. Toxicology 1994, 87:229-247.
10. Esser A.F., Tarnuzzer R.W., Tomlinson S., Tatar L.D., Stanley K.K. Horse complement protein C9: primary structure and cytotoxic activity. Mol. Immunol. 1996, 33:725-733.
11. 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.
12. Hatanaka M., Seya T., Inai S., Shimizu A. The functions of the ninth component of human complement are sustained by disulfide bonds with different susceptibilities to reduction. Biochim. Biophys. Acta 1994, 1209:117-122.
13. Heuck A.P., Tweten R.K., Johnson A.E. Beta-barrel pore-forming toxins: intriguing dimorphic proteins. Biochemistry 2001, 40:9065-9073.
14. Ishida B., Wisnieski B.J., Lavine C.H., Esser A.F. Photolabeling of a hydrophobic domain of the ninth component of human complement. J. Biol. Chem. 1982, 257:10551-10553.
15. Kontermann R., Rauterberg E.W. N-deglycosylation of human complement component C9 reduces its hemolytic activity. Mol. Immunol. 1989, 26:1125-1132.
16. Laine R.O., Esser A.F. Detection of refolding conformers of complement protein C9 during insertion into membranes. Nature 1989, 341:63-65.
17. Laine R.O., Esser A.F. Identification of the discontinuous epitope in human complement protein C9 recognized by anti-melittin antibodies. J. Immunol. 1989, 143:553-557.
18. Laine R.O., Morgan B.P., Esser A.F. Comparison between complement and melittin hemolysis: anti-melittin antibodies inhibit complement lysis. Biochemistry 1988, 27:5308-5314.
19. Luckow V.A., Lee S.C., Barry G.F., Olins P.O. Efficient generation of infectious recombinant baculoviruses by site-specific transposon-mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli. J. Virol. 1993, 67:4566-4579.
20. McCloskey M.A., Dankert J.R., Esser A.F. Assembly of complement components C5b-8 and C5b-9 on lipid bilayer membranes: visualization by freeze-etch electron microscopy. Biochemistry 1989, 28:534-540.
21. Müller-Eberhard H.J. The membrane attack complex of complement. Annu. Rev. Immunol. 1986, 4:503-528.
22. Peitsch M.C., Amiguet P., Guy R., Brunner J., Maizel J.V., Tschopp J. Localization and molecular modelling of the membrane-inserted domain of the ninth component of human complement and perforin. Mol. Immunol. 1990, 27:589-602.
23. Picot D., Garavito R.M. Prostaglandin H synthase: implications for membrane structure. FEBS Lett. 1994, 346:21-25.
24. Plumb M.E., Sodetz J.M. Proteins of the membrane attack complex. The Human Complement System in Health and Disease 1998, 119-148. Marcel Dekker, New York, NY. J.E. Volanakis, M.M. Frank (Eds.).
25. Podack E.R. Molecular composition of the tubular structure of the membrane attack complex of complement. J. Biol. Chem. 1984, 259:8641-8647.
26. Podack E.R., Tschopp J. Polymerization of the ninth component of complement (C9): formation of poly(C9) with a tubular ultrastructure resembling the membrane attack complex of complement. Proc. Natl. Acad. Sci. U.S.A. 1982, 79:574-578.
27. Rosado C.J., Kondos S., Bull T.E., Kuiper M.J., Law R.H., Buckle A.M., Voskoboinik I., Bird P.I., Trapani J.A., Whisstock J.C., Dunstone M.A. The MACPF/CDC family of pore-forming toxins. Cell Microbiol. 2008, 10:1765-1774.
28. Rossi V., Bally I., Thielens N.M., Esser A.F., Arlaud G.J. Baculovirus-mediated expression of truncated modular fragments from the catalytic region of human complement serine protease C1s. Evidence for the involvement of both complement control protein modules in the recognition of the C4 protein substrate. J. Biol. Chem. 1998, 273:1232-1239.
29. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual 1989, Cold Spring HarborLaboratory, Cold Spring Harbor, NY.
30. Scibek J.J., Plumb M.E., Sodetz J.M. Binding of human complement C8 to C9: role of the N-terminal modules in the C8 alpha subunit. Biochemistry 2002, 41:14546-14551.
31. Slade D.J., Chiswell B., Sodetz J.M. Functional studies of the MACPF domain of human complement protein C8alpha reveal sites for simultaneous binding of C8beta, C8gamma, and C9. Biochemistry 2006, 45:5290-5296.
32. Slade D.J., Lovelace L.L., Chruszcz M., Minor W., Lebioda L., Sodetz J.M. Crystal structure of the MACPF domain of human complement protein C8 alpha in complex with the C8 gamma subunit. J. Mol. Biol. 2008, 379:331-342.
33. Stanley K.K., Page M., Campbell A.K., Luzio J.P. A mechanism for the insertion of complement component C9 into target membranes. Mol. Immunol. 1986, 23:451-458.
34. Taylor K.M., Morgan B.P., Campbell A.K. Altered glycosylation and selected mutation in recombinant human complement component C9: effects on haemolytic activity. Immunology 1994, 83:501-506.
35. Taylor P.W. Complement-mediated killing of susceptible gram-negative bacteria: an elusive mechanism. Exp. Clin. Immunogenet. 1992, 9:48-56.
36. Tomlinson S., Ueda E., Maruniak J.E., Garcia-Canedo A., Bjes E.S., Esser A.F. The expression of hemolytically active human complement protein C9 in mammalian, insect, and yeast cells. Protein Exp. Purif. 1993, 4:141-148.
37. Tomlinson S., Wang Y., Ueda E., Esser A.F. Chimeric horse/human recombinant C9 proteins identify the amino acid sequence in horse C9 responsible for restriction of hemolysis. J. Immunol. 1995, 155:436-444.
38. Tschopp J., Podack E.R., Müller-Eberhard H.J. Ultrastructure of the membrane attack complex of complement: detection of the tetramolecular C9-polymerizing complex C5b-8. Proc. Natl. Acad. Sci. U.S.A. 1982, 79:7474-7478.
39. Tschopp J., Podack E.R., Müller-Eberhard H.J. The membrane attack complex of complement: C5b-8 complex as accelerator of C9 polymerization. J. Immunol. 1985, 134:495-499.
40. Wang Y., Bjes E.S., Esser A.F. Molecular aspects of complement-mediated bacterial killing. Periplasmic conversion of C9 from a protoxin to a toxin. J. Biol. Chem. 2000, 275:4687-4692.
41. Ware C.F., Kolb W.P. Assembly of the functional membrane attack complex of human complement: formation of disulfide-linked C9 dimers. Proc. Natl. Acad. Sci. U.S.A. 1981, 78:6426-6430.
42. Yamamoto K., Migita S. Mechanisms for the spontaneous formation of covalently linked polymers of the terminal membranolytic complement protein (C9). J. Biol. Chem. 1983, 258:7887-7889.