Species specificity of the complement inhibitor compstatin investigated by all-atom molecular dynamics simulations

Proteins: Structure, Function and Bioinformatics

Volumn 78, Issue 12, 2010, Pages 2655-2667

  Tamamis, Phanourios ^a   Morikis, Dimitrios ^b   Floudas, Christodoulos A ^c   Archontis, Georgios ^a  

^a UNIVERSITY OF CYPRUS   (Cyprus)

^b University of California Riverside   (United States)

^c Princeton University   (United States)

Author keywords

C3 inhibitors; Complement system; Compstatin analogs; Innate immune response; Molecular dynamics simulations

Indexed keywords

COMPLEMENT INHIBITOR; COMPSTATIN; UNCLASSIFIED DRUG;

ARTICLE; HUMAN; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; SIMULATION; X RAY DIFFRACTION;

AMINO ACID SEQUENCE; ANIMALS; COMPLEMENT C3; COMPLEMENT INACTIVATOR PROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PEPTIDES, CYCLIC; PROTEIN CONFORMATION; RATS; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; X-RAY DIFFRACTION;

MAMMALIA; PRIMATES; RATTUS;

EID: 77955839358     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22780     Document Type: Article

References (54)

1. Muller-Eberhard HJ. Complement-Chemistry and pathways. In: Gallin JI, Goldstein IM, Synderman R, editors. Inflammation: basic principles and clinical correlates, 2nd ed. New York: Raven Press; 2002. pp 21-54.
2. Sahu A, Lambris JD. Complement inhibitors: a resurgent concept in anti-inflammatory therapeutics. Immunopharmacology 2000;49:133-148.
3. Janssen BJC, Halff EF, Lambris JD, Gros P. Structure of Compstatin in Complex with Complement Component C3c Reveals a New Mechanism of Complement Inhibition. J Biochem 2007;282:29241-29247.
4. Morikis D, Lambris JD. Structure, dynamics, activity and function of compstatin and design of more potent analogs. In: Morikis D, Lambris JD, editors. Structural biology of the complement system, Boca Raton, FL: CRC Press/Taylor & Francis Group; 2005.
5. Soulika AM, Holland MC, Sfyroera G, Sahu A, Lambris JD. Compstatin inhibits complement activation by binding to the β-chain of complement factor 3. Mol Immunol 2006;43:2023-2029.
6. Sahu A, Ray BK, Lambris JD. Inhibition of human complement by a C3-binding peptide isolated from a phage-displayed random peptide library. J Immunol 1996;157:884-891.
7. Morikis D, Assa-Munt N, Sahu A, Lambris JD. Solution structure of compstatin, a potent complement inhibitor. Protein Sci 1998;7:619-627.
8. Klepeis JL, Floudas CA, Morikis D, Lambris JD. Predicting peptide structures using NMR data and deterministic global optimization. J Comput Chem 1999;20:1354-1370.
9. Sahu A, Soulika A, Morikis D, Spruce L, Moore WT, Lambris JD. Binding kinetics, structure-activity relationship, and biotransformation of the complement inhibitor compstatin. J Immunol 2000;165:2491-2499.
10. Morikis D, Roy M, Sahu A, Troganis A, Jennings PA, Tsokos GC, Lambris JD. The structural basis of compstatin activity examined by structure-function- based design of peptide analogs and NMR. J Biol Chem 2002;277:14942-14953.
11. Morikis D, Lambris JD. Structural aspects and design of low-molecular-mass complement inhibitors. Biochem Soc Trans 2002;30:1026-1036.
12. Soulika AM, Morikis D, Sarrias MR, Roy M, Spruce LA, Sahu A, Lambris JD. Studies of structure-activity relations of complement inhibitor compstatin. J Immunol 2003;170:1881-1890.
13. Klepeis J, Floudas CA, Morikis D, Tsokos CG, Argyropoulos E, Spruce L, Lambris JD. Integrated computational and experimental approach for lead optimization and design of compstatin variants with improved activity. J Am Chem Soc 2003;125:8422-8423.
14. Morikis D, Soulika AM, Mallik B, Klepeis JL, Floudas CA, Lambris JD. Improvement of the anti-C3 activity of compstatin using rational and combinatorial approaches. Biochem Soc Trans 2004;32:28-32.
15. Klepeis JL, Floudas CA, Morikis D, Tsokos CG, Lambris JD. Design of peptide analogs with improved activity using a de novo protein design approach. Ind Eng Chem Res 2004;43:3817-3826.
16. Mallik B, Katragadda M, Spruce LA, Carafides C, Tsokos CG, Morikis D, Lambris JD. Design and NMR characterization of active analogues of compstatin containing non-natural amino acids. J Med Chem 2005;48:274-286.
17. Morikis D, Mallik B, Zhang L. Biophysical and bioengineering methods for the study of the complement system at atomic resolution. WSEAS Trans Biol Biomed 2006;6:408-413.
18. Tamamis P, Skourtis S, Morikis D, Lambris JD, Archontis G. Conformational analysis of compstatin analogues with molecular dynamics simulations in explicit water. J Mol Graph Model 2007;26:571-580.
19. Mallik B, Lambris JD, Morikis D. Conformational interconversion in compstatin probed with molecular dynamics simulations. Proteins: 2003;52:130-141.
20. Magotti P, Ricklin D, Qu H, Wu Y-Q, Kaznessis YN, Lambris JD. Structure-kinetic relationship analysis of the therapeutic complement inhibitor compstatin. J Mol Recognit 2009;22:495-505.
21. Holland MC, Morikis D, Lambris JD. Synthetic small molecule complement inhibitors. Curr Opin Investig Drugs 2004;5:1164-1173.
22. Morikis D, Floudas CA, Lambris JD. Structure-based integrative computational and experimental approach for the optimization of drug design. In: Sunderam VS, van Albada GD, Sloot PMA, Dongarra JJ, editors. ICCS 2005, lecture notes in computer science: computational science. Berlin: Springer-Verlag; 2005. pp 680-688.
23. Bellows ML, Fung HK, Taylor MS, Floudas CA, López De Victoria A, Morikis D. New compstatin variants through two de novo protein design frameworks. Biophys J 2010;98:2337-2346.
24. Mallik B, Morikis D. Development of a quasi-dynamic pharmacophore model for anti-complement peptide analogues. J Am Chem Soc 2005;127:10967-10976.
25. Chiu TL, Mulakala C, Lambris JD, Kaznessis YN. Development of a new pharmacophore model that discriminates active compstatin analogs. Chem Biol Drug Des 2008;72:249-256.
26. Sahu A, Morikis D, Lambris JD. Compstatin, a peptide inhibitor of complement, exhibits species-specific binding to complement component C3. Mol Immunol 2003;39:557-566.
27. Polydoridis S, Oikonomakos NG, Leonidas DD, Archontis G. Recognition of ribonuclease A by 3'-5'-pyrophosphate-linked dinucleotide inhibitors: a molecular dynamics/continuum electrostatics analysis. Biophys J 2007;92:1659-1672.
28. Archontis G, Watson KA, Xie Q, Andreou G, Chrysina ED, Zographos SE, Oikonomakos NG, Karplus M. Glycogen phosphorylase inhibitors: a free energy perturbation analysis of glucopyranose spirohydantoin analogues. Proteins 2005;61:984-998.
29. Brooks BR, Brooks CL, III, Mackerell AD, Jr, Nilsson L, Petrella RJ, Roux B, Won Y, Archontis G, Bartels C, Boresch S, Caflisch A, Caves L, Cui Q, Dinner AR, Feig M, Fischer S, Gao J, Hodoscek M, Im W, Kuczera K, Lazaridis T, Ma J, Ovchinnikov V, Paci E, Pastor RW, Post CB, Pu JZ, Schaefer M, Tidor B, Venable RM, Woodcock HL, Wu X, Yang W, York DM, Karplus M. CHARMM: the biomolecular simulation program. J Comput Chem 2009;30:1545-1614.
30. Davis ME, Madura JD, Luty BA, McCammon JA. Electrostatics and diffusion of molecules in solution: simulations with the University of Houston Brownian Dynamics Program. Comput Phys Commun 1991;62:187-197.
31. Thompson D, Lazennec C, Plateau P, Simonson T. Probing electrostatic interactions and ligand binding in aspartyl-tRNA synthetase through site-directed mutagenesis and computer simulations. Proteins 2008;71:1450-1460.
32. Thompson D, Plateau P, Simonson T. Free-energy simulations and experiments reveal long-range electrostatic interactions and substrate-assisted specificity in an aminoacyl-tRNA synthetase. Chembiochem 2006;7:337-344.
33. Eswar N, Marti-Renom MA, Webb B, Madhusudhan MS, Eramian D, Shen M, Pieper U, Sali A. Comparative protein structure modeling with MODELLER. Current protocols in bioinformatics, New York: John Wiley; 2006. Suppl. 15, 5.6. 1-5. 6.30.
34. Krivov GG, Shapovalov MV, Dunbrack RL, Jr. Improved prediction of protein side-chain conformations with SCWRL4. Proteins 2009;77:778-795.
35. Janssen BJC, Huizinga EG, Raaijmakers HC, Roos A, Daha MR, Nilsson-Ekdahl K, Nilsson B, Gros P. Structures of complement component C3 provide insights into the function and evolution of immunity. Nature 2005;437:505-511.
36. Mackerell AD, Jr, Bashford D, Bellott M, Dunbrack RL, Jr, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FKT, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE, III, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiorkewicz-Kuczera J, Yin D, Karplus M. An all-atom empirical potential for molecular modelling and dynamics study of proteins. J Phys Chem B 1998;102:3586-3616.
37. Mackerell AD, Jr, Feig M, Brooks CL, III. Extending the treatment of backbone energetics in protein force fields: limitations of gasphase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 2004;25:1400-1415.
38. Macias AT, Mackerell AD, Jr. CH/pi interactions involving aromatic amino acids: refinement of the CHARMM tryptophan force field. J Comput Chem 2005;26:1452-1463.
39. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983;79:926-935.
40. Neria E, Fischer S, Karplus M. Simulation of activation free energies in molecular systems. J Chem Phys 1996;105:1902-1921.
41. Darden T, York D, Pedersen L. Particle Mesh Ewald: an N log (N) method for Ewald sums in large systems. J Chem Phys 1993;98:10089-10092.
42. Nose S. A unified formulation of the constant temperature molecular dynamics method. J Chem Phys 1984;81:511-519.
43. Hoover W. Canonical dynamics: equilibrium phase-space distributions. Phys Rev A 1985;31:1695-1697.
44. Feller S, Zhang Y, Pastor RW, Brooks B. Constant-pressure molecular-dynamics simulation: the Langevin piston method. J Chem Phys 1995;103:4613-4621.
45. Ryckaert JP, Ciccotti G, Berendsen HJC. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 1977;23:327-341.
46. Seeber M, Cecchini M, Rao F, Settanni G, Caflisch A. Wordom: a program for efficient analysis of molecular dynamics simulations. Bioinformatics 2007;23:2625-2627.
47. Massova I, Kollman PA. Combined molecular mechanical and continuum solvent approach (MM-PBSA/GBSA) to predict ligand binding. Perspect Drug Discov Des 2000;18:113-135.
48. Im W, Lee MS, Brooks CL, III. Generalized Born model with a simple smoothing function. J Comput Chem 2003;24:1691-1702.
49. Chen J, Im W, Brooks, CL, III. Balancing solvation and intramolecular interactions: toward a consistent generalized Born force field. J Am Chem Soc 2006;128:3728-3736.
50. Singh N, Warshel A. Absolute binding free energy calculations: on the accuracy of computational scoring of protein-ligand interactions. Proteins 2010;78:1705-1723.
51. Gilson MK, Zhou HX. Calculation of protein-ligand binding affinities. Annu Rev Biophys Biomol Struct 2007;36:21-42.
52. Swanson JMJ, Henchmann R, McCammon JA. Revisiting free energy calculations: a theoretical connection to MM/PBSA and direct calculation of the association free energy. Biophys J 2004;86:67-74.
53. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and Clustal X version 2.0. Bioinformatics 2007;23:2947-2948.
54. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamic. J Mol Graph 1996;14:33-38.