Use of time-resolved FRET to validate crystal structure of complement regulatory complex between C3b and factor H (N terminus)

Protein Science

Volumn 20, Issue 12, 2011, Pages 2102-2112

  Pechtl, Isabell C ^a   Neely, Robert K ^a   Dryden, David T F ^a   Jones, Anita C ^a   Barlow, Paul N ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

C3b; Complement system; Factor H; Fluorescent protein labeling; Resonance energy transfer; Time resolved fluorescence

Indexed keywords

COMPLEMENT COMPONENT C3B; COMPLEMENT FACTOR H; CYSTEINE; THIOESTER;

AMINO TERMINAL SEQUENCE; ARTICLE; CONJUGATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; FLUORESCENCE RESONANCE ENERGY TRANSFER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; VALIDATION PROCESS;

COMPLEMENT C3B; COMPLEMENT FACTOR H; CRYSTALLOGRAPHY, X-RAY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY;

EID: 81755172091     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.738     Document Type: Article

References (43)

1. Walport MJ (2001) Complement. First of two parts. N Engl J Med 344: 1058-1066.
2. Walport MJ (2001) Complement. Second of two parts. N Engl J Med 344: 1140-1144.
3. Ricklin D, Hajishengallis G, Yang K, Lambris JD (2010) Complement: a key system for immune surveillance and homeostasis. Nat Immunol 11: 785-797.
4. Law SK, Dodds AW (1997) The internal thioester and the covalent binding properties of the complement proteins C3 and C4. Protein Sci 6: 263-274. (Pubitemid 27079917)
5. Lachmann PJ (2009) The amplification loop of the complement pathways. Adv Immunol 104: 115-149.
6. Fishelson Z, Pangburn MK, Muller-Eberhard HJ (1984) Characterization of the initial C3 convertase of the alternative pathway of human complement. J Immunol 132: 1430-1434. (Pubitemid 14154572)
7. Kirkitadze MD, Barlow PN (2001) Structure and flexibility of the multiple domain proteins that regulate complement activation. Immunol Rev 180: 146-161. (Pubitemid 32472859)
8. Lachmann PJ, Hughes-Jones NC (1984) Initiation of complement activation. Springer Semin Immunopathol 7: 143-162. (Pubitemid 14010634)
9. Sim RB, DiScipio RG (1982) Purification and structural studies on the complement-system control protein beta1H (Factor H). Biochem J 205: 285-293. (Pubitemid 13226501)
10. Hageman GS, Anderson DH, Johnson LV, Hancox LS, Taiber AJ, Hardisty LI, Hageman JL, Stockman HA, Borchardt JD, Gehrs KM, Smith RJ, Silvestri G, Russell SR, Klaver CC, Barbazetto I, Chang S, Yannuzzi LA, Barile GR, Merriam JC, Smith RT, Olsh AK, Bergeron J, Zernant J, Merriam JE, Gold B, Dean M, Allikmets R (2005) A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc Natl Acad Sci U S A 102: 7227-7232. (Pubitemid 40696361)
11. Kavanagh D, Goodship T (2010) Genetics and complement in atypical HUS. Pediatr Nephrol 25: 2431-2442.
12. Meri S, Pangburn MK (1990) Discrimination between activators and nonactivators of the alternative pathway of complement: regulation via a sialic acid/polyanion binding site on factor H. Proc Natl Acad Sci U S A 87:3982-3986.
13. Sharma AK, Pangburn MK (1996) Identification of three physically and functionally distinct binding sites for C3b in human complement factor H by deletion mutagenesis. Proc Natl Acad Sci U S A 93: 10996-11001. (Pubitemid 26333106)
14. Pangburn MK (2000) Host recognition and target differentiation by factor H, a regulator of the alternative pathway of complement. Immunopharmacology 49:149-157.
15. Kristensen T, Tack BF (1986) Murine protein H is comprised of 20 repeating units, 61 amino acids in length. Proc Natl Acad Sci U S A 83: 3963-3967. (Pubitemid 16062402)
16. Norman DG, Barlow PN, Baron M, Day AJ, Sim RB, Campbell ID (1991) Three-dimensional structure of a complement control protein module in solution. J Mol Biol 219: 717-725. (Pubitemid 121003544)
17. Barlow PN, Steinkasserer A, Norman DG, Kieffer B, Wiles AP, Sim RB, Campbell ID (1993) Solution structure of a pair of complement modules by nuclear magnetic resonance. J Mol Biol 232: 268-284. (Pubitemid 23245413)
18. Perkins SJ, Haris PI, Sim RB, Chapman D (1988) A study of the structure of human complement component factor H by Fourier transform infrared spectroscopy and secondary structure averaging methods. Biochemistry 27: 4004-4012.
19. Kirkitadze MD, Krych M, Uhrin D, Dryden DT, Smith BO, Cooper A, Wang X, Hauhart R, Atkinson JP, Barlow PN (1999) Independently melting modules and highly structured intermodular junctions within complement receptor type 1. Biochemistry 38: 7019-7031.
20. Gigli I, Fujita T, Nussenzweig V (1979) Modulation of the classical pathway C3 convertase by plasma proteins C4 binding protein and C3b inactivator. Proc Natl Acad Sci U S A 76: 6596-6600. (Pubitemid 10163445)
21. Alsenz J, Lambris JD, Schulz TF, Dierich MP (1984) Localization of the complement-component-C3b-binding site and the cofactor activity for factor I in the 38 kDa tryptic fragment of factor H. Biochem J 224: 389-398. (Pubitemid 15168431)
22. Schulz TF, Alsenz J, Dierich MP (1985) Localization of functionally important areas of the regulator protein factor H using monoclonal antibodies. Wien Klin Wochenschr 97: 248-252. (Pubitemid 15148284)
23. Schmidt CQ, Herbert AP, Kavanagh D, Gandy C, Fenton CJ, Blaum BS, Lyon M, Uhrin D, Barlow PN (2008) A new map of glycosaminoglycan and C3b binding sites on factor H. J Immunol 181: 2610-2619.
24. Hocking HG, Herbert AP, Kavanagh D, Soares DC, Ferreira VP, Pangburn MK, Uhrin D, Barlow PN (2008) Structure of the N-terminal region of complement factor H and conformational implications of disease-linked sequence variations. J Biol Chem 283:9475-9487.
25. Okemefuna AI, Gilbert HE, Griggs KM, Ormsby RJ, Gordon DL, Perkins SJ (2008) The regulatory SCR-1/5 and cell surface-binding SCR-16/20 fragments of factor H reveal partially folded-back solution structures and different self-associative properties. J Mol Biol 375:80-101. (Pubitemid 350161888)
26. Morgan HP, Schmidt CQ, Guariento M, Blaum BS, Gillespie D, Herbert AP, Kavanagh D, Mertens HD, Svergun DI, Johansson CM, Uhrin D, Barlow PN, Hannan JP (2011) Structural basis for engagement by complement factor H of C3b on a self surface. Nat Struct Mol Biol 18: 463-470.
27. Wu J, Wu YQ, Ricklin D, Janssen BJ, Lambris JD, Gros P (2009) Structure of complement fragment C3b-factor H and implications for host protection by complement regulators. Nat Immunol 10: 728-733.
28. Nishida N, Walz T, Springer TA (2006) Structural transitions of complement component C3 and its activation products. Proc Natl Acad Sci U S A 103: 19737-19742. (Pubitemid 46037500)
29. Szakonyi G, Guthridge JM, Li D, Young K, Holers VM, Chen XS (2001) Structure of complement receptor 2 in complex with its C3d ligand. Science 292: 1725-1728. (Pubitemid 32506247)
30. Gilbert HE, Eaton JT, Hannan JP, Holers VM, Perkins SJ (2005) Solution structure of the complex between CR2 SCR 1-2 and C3d of human complement: an X-ray scattering and sedimentation modelling study. J Mol Biol 346: 859-873. (Pubitemid 40247723)
31. Hannan JP, Young KA, Guthridge JM, Asokan R, Szakonyi G, Chen XS, Holers VM (2005) Mutational analysis of the complement receptor type 2 (CR2/CD21)-C3d interaction reveals a putative charged SCR1 binding site for C3d. J Mol Biol 346: 845-858. (Pubitemid 40247722)
32. Kovacs JM, Hannan JP, Eisenmesser EZ, Holers VM (2009) Mapping of the C3d ligand binding site on complement receptor 2 (CR2/CD21) using nuclear magnetic resonance and chemical shift analysis. J Biol Chem 284: 9513-9520.
33. van den Elsen JM, Isenman DE (2011) A crystal structure of the complex between human complement receptor 2 and its ligand C3d. Science 332: 608-611.
34. Kajander T, Lehtinen MJ, Hyvarinen S, Bhattacharjee A, Leung E, Isenman DE, Meri S, Goldman A, Jokiranta TS (2011) Dual interaction of factor H with C3d and glycosaminoglycans in host-nonhost discrimination by complement. Proc Natl Acad SciUS A 108: 2897-2902.
35. Krissinel E (2010) Crystal contacts as nature's docking solutions. J Comput Chem 31: 133-143.
36. Clegg RM (1995) Fluorescence resonance energy transfer. Curr Opin Biotechnol 6: 103-110.
37. Johnson I, Spence MTZ, editors. Molecular probes handbook, a guide to fluorescenet probes and labeling technologies. Invitrogren.
38. Cheng KH, Wiedmer T, Sims PJ (1985) Fluorescence resonance energy transfer study of the associative state of membrane-bound complexes of complement proteins C5b-8. J Immunol 135: 459-464. (Pubitemid 15011469)
39. Bexborn F, Andersson PO, Chen H, Nilsson B, Ekdahl KN (2008) The tick-over theory revisited: formation and regulation of the soluble alternative complement C3 convertase (C3(H2O)Bb). Mol Immunol 45: 2370-2379.
40. Pechtl IC, Kavanagh D, McIntosh N, Harris CL, Barlow PN (2011) Disease-associated N-terminal complement factor H mutations perturb cofactor and decayaccelerating activities. J Biol Chem 286: 11082-11090.
41. Schmidt CQ, Herbert AP, Mertens HD, Guariento M, Soares DC, Uhrin D, Rowe AJ, Svergun DI, Barlow PN (2010) The central portion of factor H (modules 10-15) is compact and contains a structurally deviant CCP module. J Mol Biol 395: 105-122.
42. Dodds AW (1993) Small-scale preparation of complement components C3 and C4. Methods Enzymol 223:46-61.
43. Usami M, Ohno Y (2005) Preparation of complement fragments C3b and C3a from purified rat complement component C3 by activated cobra venom factor. J Pharmacol Toxicol Methods 52: 260-263. (Pubitemid 41207202)