The extended multidomain solution structures of the complement protein Crry and its chimeric conjugate Crry-Ig by scattering, analytical ultracentrifugation and constrained modelling: Implications for function and therapy

Journal of Molecular Biology

Volumn 329, Issue 3, 2003, Pages 525-550

  Aslam, Mohammed ^a   Guthridge, Joel M ^b   Hack, Bradley K ^c   Quigg, Richard J ^c   Holers, V Michael ^b   Perkins, Stephen J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

Analytical ultracentrifugation; Constrained modelling; Neutron scattering; Short consensus complement repeat; X ray scattering

Indexed keywords

COMPLEMENT; COMPLEMENT COMPONENT C3B RECEPTOR; COMPLEMENT RECEPTOR RELATED PROTEIN Y; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G1; PEPTIDE; PROTEIN; PROTEIN CRRY IG; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANALYTIC METHOD; ANALYTICAL PARAMETERS; ANTENNA; ARTICLE; CALCULATION; CONJUGATION; COVALENT BOND; CRYSTAL STRUCTURE; MOLECULAR MODEL; MOLECULAR WEIGHT; NEUTRON; NEUTRON SCATTERING; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN STRUCTURE; RADIATION SCATTERING; SEDIMENTATION; STRUCTURE ANALYSIS; ULTRACENTRIFUGATION;

EID: 0037954130     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00492-3     Document Type: Article

References (59)

1. Law S.K.A., Reid K.B.M. Complement. 2nd edit. 1995;IRL Press, Oxford.
2. Quigg R.J., Holers V.M. Characterization of rat complement receptors and regulatory proteins. CR2 and Crry are conserved and the C3b receptor of neutrophils and platelets is distnct from CR1. J. Immunol. 155:1995;1481-1488.
3. Holers V.M. Phenotypes of complement knockouts. Immunopharmacology. 49:2000;125-131.
4. Kim Y.U., Kinoshita T., Molina H., Hourcade D., Seya T., Wagner L.M., Holers V.M. Mouse complement regulatory protein Crry/p65 utilizes the specific mechanisms of both decay-accelerating factor and membrane cofactor protein. J. Exp. Med. 181:1995;151-159.
5. Molina H., Wong W., Kinoshita T., Brenner C., Foley S., Holers V.M. Distinct receptor and regulatory properties of recombinant mouse complement receptor 1 (CR1) and Crry, the two genetic homologs of human CR1. J. Exp. Med. 175:1992;121-129.
6. Xu C., Mao D., Holers V.M., Balanca B., Cheng A.M., Molina H. A critical role for murine complement regulator Crry in fetomaternal tolerance. Science. 287:2000;498-501.
7. Quigg R.J., Kozono Y., Berthiaume D., Lim A., Salant D.J., Weinfeld A., et al. Blockade of antibody-induced glomerulonephritis with Crry-Ig, a soluble murine complement inhibitor. J. Immunol. 160:1998;4553-4560.
8. Schiller B., Cunningham P.N., Alexander J.J., Bao L.H., Holers V.M., Quigg R.J. Expression of a soluble complement inhibitor protects transgenic mice from antibody-induced acute renal failure. J. Am. Soc. Nephrol. 12:2001;71-79.
9. He C., Alexander J.J., Lim A., Quigg R.J. Production of the rat complement regulator Crry as an active soluble protein in Pichia pastoris. Arch. Biochem. Biophys. 341:1997;347-352.
10. Quigg R.J., He C., Lim A., Berthiaume D., Alexander J.J., Kraus D., Holers V.M. Transgenic mice overexpressing the complement inhibitor Crry as a soluble protein are protected from antibody-induced glomerular injury. J. Exp. Med. 188:1998;1321-1331.
11. Alexander J.J., Lim A., He C., MacDonald R.L., Holers V.M., Quigg R.J. Renal, central nervous system and pancreatic overexpression of recombinant soluble Crry in transgenic mice. A novel means of protection from complement-mediated injury. Immunopharmacology. 42:1999;245-254.
12. Rehrig S., Fleming S.D., Anderson J., Guthridge J.M., Rakstang J., McQueen C.E., et al. Complement inhibitor, complement receptor 1-related gene/protein y-Ig attentuates intestinal damage after the onset of mesenteric ischemia/reperfusion injury in mice. J. Immunol. 167:2001;5921-5927.
13. Holers V.M., Girardi G., Mo L., Guthridge J.M., Molina H., Pierangeli S.S., et al. Complement C3 activation is required for anti-phospholipid antibody-induced fetal loss. J. Exp. Med. 195:2002;211-220.
14. Perkins S.J., Gilbert H.E., Aslam M., Hannan J.P., Holers V.M., Goodship T.H.J. Solution structures of complement components by X-ray and neutron scattering and analytical ultracentrifugation. Biochem. Soc. Trans. 30:2002;996-1001.
15. Schwarzenbacher R., Zeth K., Diederichs K., Gries A., Kostner G.M., Laggner P., Prassl R. Crystal structure of human β2-glycoprotein I: implications for phospholipid binding and the antiphospholipid syndrome. EMBO J. 18:1999;6228-6239.
16. Bouma B., de Groot P.G., van den Elsen J.M.H., Ravelli R.B.G., Schouten A., Simmelink M.J.A., et al. Adhesion mechanism of human β2glycoprotein I to phospholipids based on its crystal structure. EMBO J. 18:1999;5166-5174.
17. Murthy K.H.M., Smith S.A., Ganesh V.K., Judge K.W., Mullin N., Barlow P.N., et al. Crystal structure of a complement control protein that regulates both pathways of complement activation and binds heparan sulfate proteoglycans. Cell. 104:2001;301-311.
18. Hammel M., Kriechbaum M., Gries A., Kostner G.M., Laggner P., Prassl R. Solution structure of human and bovine β2-glycoprotein I revealed by small angle X-ray scattering. J. Mol. Biol. 321:2002;85-97.
19. Guthridge J.M., Rakstang J.K., Young K.A., Hinshelwood J., Aslam M., Robertson A., Gipson M.G., Sarrias M.R., et al. Structural studies in solution of the recombinant N-terminal pair of short consensus/complement repeat domains of complement receptor type 2 (CR2/CD21) and its interaction with its ligand C3dg. Biochemistry. 40:2001;5931-5941.
20. Gilbert, H. E., Hannan, J., Holers, V. M., Perkins, S. J. (2002). Ultracentrifugation of the complex formed between CR2 SCR-1/2 and C3d shows that SCR-1 is extended away from SCR-2 in the complex. Biochemical Society Meeting 677, July 2002, Cardiff, UK.
21. Szakonyi G., Guthridge J.M., Li D., Young K., Holers V.M., Chen X.S. Structure of complement receptor 2 in complex with its C3d ligand. Science. 292:2001;1725-1728.
22. Prota A.E., Sage D.R., Stehle T., Fingeroth J.D. The crystal structure of human CD21: implications for Epstein-Barr virus and C3d binding. Proc. Natl Acad. Sci. USA. 99:2002;10641-10646.
23. Aslam M., Perkins S.J. Folded-back solution structure of monomeric Factor H of human complement by synchrotron X-ray and neutron scattering, analytical ultracentrifugation and constrained molecular modelling. J. Mol. Biol. 309:2001;1117-1138.
24. Glatter O., Kratky O. Small-angle X-ray Scattering. 1982;Academic Press, New York.
25. Perkins S.J., Chung L.P., Reid K.B.M. Unusual ultrastructure of complement component C4b-binding protein of human complement by synchrotron X-ray scattering and hydrodynamic analysis. Biochem. J. 223:1986;779-807.
26. Boehm M.K., Woof J.M., Kerr M.A., Perkins S.J. The Fab and Fc fragments of IgA1 exhibit a different arrangement from that in IgG: a study by X-ray and neutron solution scattering and homology modelling. J. Mol. Biol. 286:1999;1421-1447.
27. Perkins S.J. X-ray and neutron scattering analyses of hydration shells: a molecular interpretation based on sequence predictions and modelling fits. Biophys. Chem. 93:2001;129-139.
28. McRorie D.K., Voelker P.J. Self-associating Systems in the Analytical Ultracentrifuge. 1993;Beckman Instruments, Palo Alto.
29. Wiles A.P., Shaw G., Bright J., Perczel A., Campbell I.D., Barlow P.N. NMR studies of a viral protein that mimics the regulators of complement activation. J. Mol. Biol. 272:1997;253-265.
30. Casasnovas J.M., Larvie M., Stehle T. Crystal structure of two CD46 domains reveals an extended measles virus-binding surface. EMBO J. 18:1999;2911-2922.
31. Smith B.O., Mallin R.L., Krych-Goldberg M., Wang X., Hauhart R.E., Bromek K., et al. Structure of the C3b binding site of CR1 (CD35), the immune adherence receptor. Cell. 108:2002;769-780.
32. Harris L.J., Skaletsky E., McPherson A. Crystallographic structure of an intact IgG1 monoclonal antibody. J. Mol. Biol. 275:1998;861-872.
33. Perkins S.J., Ashton A.W., Boehm M.K., Chamberlain D.C. Molecular structures from low angle X-ray and neutron scattering strudies. Int. J. Biol. Macromol. 22:1998;1-16.
34. Quigg R.J. Use of complement inhibitors in tissue injury. Trends Mol. Med. 8:2002;430-436.
35. Cunningham P.N., Holers V.M., Alexander J.J., Guthridge J.M., Carroll M.C., Quigg R.J. Complement is activated in kidney by endotoxin but does not cause the ensuing acute renal failure. Kidney Int. 58:2000;1580-1587.
36. Davoust N., Nataf S., Reiman R., Holers V.M., Campbell I.L., Barnum S.R. Central nervous system-targeted expression of the complement inhibitors Crry prevents experimental allergic encephalomyelitis. J. Immunol. 163:1999;6551-6556.
37. Perkins S.J., Sim R.B. Molecular modelling of human complement component C3 and its fragments by solution scattering. Eur. J. Biochem. 157:1986;155-168.
38. Perkins S.J., Nealis A.S., Sim R.B. Molecular modelling for human complement component C4 and its fragments by X-ray and neutron solution scattering. Biochemistry. 29:1990;1167-1175.
39. Mayans M.O., Coadwell W.J., Beale D., Symons D.B.A., Perkins S.J. Demonstration by pulsed neutron scattering that the arrangement of the Fab and Fc fragments in the overall structures of bovine IgG1 and IgG2 in solution is similar. Biochem. J. 311:1995;283-291.
40. Towns-Andrews E., Berry A., Bordas J., Mant G.R., Murray P.K., Roberts K., et al. Time-resolved X-ray diffraction station: X-ray optics, detectors and data acquisition. Rev. Sci. Instrum. 60:1989;2346-2349.
41. Worgan J.S., Lewis R., Fore N.S., Sumner I.L., Berry A., Parker B., et al. The application of multiwire X-ray detectors to experiments using synchrotron radiation. Nucl. Instrum. Methods Phys. Res. A291:1990;447-454.
42. Perkins S.J. High-flux X-ray and neutron scattering studies. Chowdhry B., Harding S.E. Protein-Ligand Interactions: A Practical Approach. vol. 1:2000;223-262 Oxford University Press, Oxford.
43. Boulin C., Kempf R., Koch M.H.J., McLaughlin S.M. Data appraisal, evaluation and display for synchrotron radiation experiments: hardware and software. Nucl. Instrum. Methods. A249:1986;399-407.
44. Heenan R.K., King S.M. Proceedings of an International Seminar on Structural Investigations at Pulsed Neutron Sources, Dubna, 1st-4th September 1992. Report E3-93-65. Proceedings of an International Seminar on Structural Investigations at Pulsed Neutron Sources, Dubna, 1st-4th September 1992. Report E3-93-65. 1993;Joint Institute for Nuclear Research, Dubna.
45. Lindner P., May R.P., Timmins P.A. Upgrading of the SANS instrument D11 at the ILL. Physica B. 180:1992;967-972.
46. Kratky O. X-ray small angle scattering with substances of biological interest in diluted solutions. Prog. Biophys. Chem. 13:1963;105-173.
47. Wignall G.D., Bates F.S. Absolute calibration of small angle neutron scattering data. J. Appl. Crystallog. 20:1987;28-40.
48. Hjelm R.P. The small-angle approximation of X-ray and neutron scatter from rigid rods of non-uniform cross section and finite length. J. Appl. Crystallog. 18:1985;452-460.
49. Perkins S.J. Protein volumes and hydration effects: the calculation of partial specific volumes, neutron scattering matchpoints and 280 nm absorption coefficients for proteins and glycoproteins from amino acid sequences. Eur. J. Biochem. 157:1986;169-180.
50. Semenyuk A.V., Svergun D.I. GNOM - a program package for small-angle scattering data-processing. J. Appl. Crystallog. 24:1991;537-540.
51. Svergun D.I. Determination of the regularization parameter in indirect transform methods using perceptual criteria. J. Appl. Crystallog. 25:1992;495-503.
52. Philo J. A method for directly fitting the time derivative of sedimentation velocity data and an alternative algorithm for calculating sedimentation coefficient distribution functions. Anal. Biochem. 279:2000;151-163.
53. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:1983;2577-2637.
54. Lee B., Richards F.M. An interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55:1971;379-400.
55. Šali A., Blundell T.L. The definition of general topological equivalence in protein structures: a procedure involving comparison of properties and relationships through simulated annealing and dynamic programming. J. Mol. Biol. 212:1990;403-428.
56. Ashton A.W., Boehm M.K., Gallimore J.R., Pepys M.B., Perkins S.J. Pentameric and decameric structures in solution of the serum amyloid P component by X-ray and neutron scattering and molecular modelling analyses. J. Mol. Biol. 272:1997;408-422.
57. Perkins S.J., Weiss H. Low resolution structural studies of mitochondrial ubiquinol-cytochrome c reductase in detergent solutions by neutron scattering. J. Mol. Biol. 168:1983;847-866.
58. 1-antitrypsin by neutron and X-ray solution scattering. Biochem. J. 267:1990;203-212.
59. Perkins S.J., Smith K.F., Kilpatrick J.M., Volanakis J.E., Sim R.B. Modelling of the serine protease fold by X-ray and neutron scattering and sedimentation analyses: its occurrence in factor D of the complement system. Biochem. J. 295:1993;87-99.