CompleMent Inhibition by Staphylococcus aureus: Electrostatics of C3d-EfbC and C3d-Ehp association

Cellular and Molecular Bioengineering

Volumn 5, Issue 1, 2012, Pages 32-43

  Gorham Jr , Ronald D ^a   Kieslich, Chris A ^a   Morikis, Dimitrios ^a  

^a University of California Riverside   (United States)

Author keywords

Alanine scan; Bacterial infection; C3; Electrostatic clustering; Electrostatic free energy; Poisson Boltzmann electrostatics

Indexed keywords

ALANINE; COMPLEMENT COMPONENT C3D; EFBC PROTEIN; EHP PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AMINO ACID SUBSTITUTION; ARTICLE; CLUSTER ANALYSIS; COMPLEMENT INHIBITION; COMPLEX FORMATION; CONTROLLED STUDY; IMMUNE EVASION; MATHEMATICAL COMPUTING; NONHUMAN; POISSON BOLTZMANN FREE ENERGY CALCULATION; PREDICTION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; STAPHYLOCOCCUS AUREUS; STATIC ELECTRICITY;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 84857895493     PISSN: 18655025     EISSN: 18655033     Source Type: Journal    
DOI: 10.1007/s12195-011-0195-6     Document Type: Article

References (61)

1. Baker, N. A., D. Sept, S. Joseph, M. J. Holst, and J. A. McCammon. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl Acad. Sci. USA. 98(18):10037-10041, 2001. (Pubitemid 32802969)
2. Berman, H. M., J. Westbrook, Z. Feng, G. Gilliland, T. N. Bhat, H. Weissig, I. N. Shindyalov, and P. E. Bourne. The protein data bank. Nucleic Acids Res. 28(1):235-242, 2000. (Pubitemid 30047768)
3. Chen, H., D. Ricklin, M. Hammel, B. L. Garcia, W. J. McWhorter, G. Sfyroera, Y. Q. Wu, A. Tzekou, S. Li, B. V. Geisbrecht, V. L. Woods, and J. D. Lambris. Allosteric inhibition of complement function by a staphylococcal immune evasion protein. Proc. Natl Acad. Sci. USA. 107(41):17621-17626, 2010.
4. Cheung, A. S., C. A. Kieslich, J. F. Yang, and D. Morikis. Solvation effects in calculated electrostatic association free energies for the C3d-CR2 complex and comparison with experimental data. Biopolymers 93(6):509-519, 2010.
5. DiMaggio, P. A., S. R. McAllister, C. A. Floudas, X. Feng, G. Li, J. D. Rabinowitz, and H. A. Rabitz. Enhancing molecular discovery using descriptor-free rearrangement clustering techniques for sparse datasets. AIChE J. 56(2):405-418, 2010.
6. Dolinsky, T. J., J. E. Nielsen, J. A. McCammon, and N. A. Baker. PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res. 32:W665-W667, 2004. (Pubitemid 38997419)
7. Dong, F., B. Olsen, and N. A. Baker. Computational methods for biomolecular electrostatics. Biophysical tools for biologists: vol 1 in vitro techniques. Methods Cell. Biol. 84:843-870, 2008.
8. Foster, T. J. Immune evasion by Staphylococci. Nat. Rev. Microbiol. 3(12):948-958, 2005. (Pubitemid 43078158)
9. Gabdoulline, R. R., and R. C. Wade. Simulation of the diffusional association of Barnase and Barstar. Biophys. J. 72(5):1917-1929, 1997. (Pubitemid 27184422)
10. Gorham, R. D. Jr., C. A. Kieslich, A. Nichols, N. U. Sausman, M. Foronda, and D. Morikis. An evaluation of Poisson-Boltzmann electrostatic free energy calculations through comparison with experimental mutagenesis data. Biopolymers, in press. doi:10.1002/bip.21644.
11. Gorham, R. D. Jr., C. A. Kieslich, and D. Morikis. Electrostatic clustering and free energy calculations provide a foundation for protein design and optimization. Ann. Biomed. Eng. 39(4):1252-1263, 2011.
12. Gros, P., F. J. Milder, and B. J. C. Janssen. Complement driven by conformational changes. Nat. Rev. Immunol. 8(1):48-58, 2008.
13. Hammel, M., G. Sfyroera, S. Pyrpassopoulos, D. Ricklin, K. X. Ramyar, M. Pop, Z. Jin, J. D. Lambris, and B. V. Geisbrecht. Characterization of Ehp, a secreted complement inhibitory protein from Staphylococcus aureus. J. Biol. Chem. 282(41):30051-30061, 2007. (Pubitemid 350035255)
14. Hammel, M., G. Sfyroera, D. Ricklin, P. Magotti, J. D. Lambris, and B. V. Geisbrecht. A structural basis for complement inhibition by Staphylococcus aureus. Nat. Immunol. 8(4):430-437, 2007. (Pubitemid 46745418)
15. Haspel, N., B. V. Geisbrecht, and L. Kavraki. Multi-scale characterization of the energy landscape of proteins with application to the C3d/Efb-C complex. Proteins 78(4):1004-1014, 2010.
16. Haspel, N., D. Ricklin, B. V. Geisbrecht, L. E. Kavraki, and J. D. Lambris. Electrostatic contributions drive the interaction between Staphylococcus aureus protein Efb-C and its complement target C3d. Protein Sci. 17(11):1894-1906, 2008.
17. Humphrey, W., A. Dalke, and K. Schulten. VMD: visual molecular dynamics. J. Mol. Graphics 14(1):33-38, 1996. (Pubitemid 26152973)
18. Isenman, D. E., and N. R. Cooper. The structure and function of the third component of human complement. I. The nature and extent of conformational changes accompanying C3 activation. Mol. Immunol. 18(4):331-339, 1981. (Pubitemid 11102689)
19. Isenman, D. E., E. Leung, J. D. Mackay, S. Bagby, and J. M. H. van den Elsen. Mutational analyses reveal that the Staphylococcal immune evasion molecule Sbi and complement receptor 2 (CR2) share overlapping contact residues on C3d: implications for the controversy regarding the CR2/C3d cocrystal structure. J. Immunol. 184(4):1946-1955, 2010.
20. Jain, A., M. Mutty, and P. Flyn. Data clustering: a review. ACM Comput. Surv. 31:264-323, 1999.
21. Jongerius, I., B. L. Garcia, B. V. Geisbrecht, J. A. G. van Strijp, and S. H. M. Rooijakkers. Convertase inhibitory properties of Staphylococcal extracellular complement-binding protein. J. Biol. Chem. 285(20):14973-14979, 2010.
22. Jongerius, I., J. Kohl, M. K. Pandey, M. Ruyken, K. P. M. van Kessel, J. A. G. van Strijp, and S. H. M. Rooijakkers. Staphylococcal complement evasion by various convertase-blocking molecules. J. Exp. Med. 204(10):2461-2471, 2007. (Pubitemid 47529330)
23. Kieslich, C. A., R. D. Gorham, Jr, and D. Morikis. Is the rigid-body assumption reasonable? Insights into the effects of dynamics on the electrostatic analysis of barnase-barstar. J. Non-Cryst. Solids 357(2):707-716, 2011.
24. Kieslich, C. A., J. Yang, D. Gunopulos, and D. Morikis. Automated computational framework for the analysis of electrostatic similarities of proteins. Biotechnol. Prog. 27(2):316-325, 2011.
25. Kobayashi, S. D., and F. R. DeLeo. An update on community-associated MRSA virulence. Curr. Opin. Pharmacol. 9(5):545-551, 2009.
26. Laarman, A., F. Milder, J. van Strijp, and S. Rooijakkers. Complement inhibition by gram-positive pathogens: molecular mechanisms and therapeutic applications. J. Mol. Med. 88(2):115-120, 2010.
27. Lee, L. Y. L., M. Hook, D. Haviland, R. A. Wetsel, E. O. Yonter, P. Syribeys, J. Vernachio, and E. L. Brown. Inhibition of complement activation by a secreted Staphylococcus aureus protein. J. Infect. Dis. 190(3):571-579, 2004. (Pubitemid 38982098)
28. Lee, L. Y. L., X. W. Liang, M. Hook, and E. L. Brown. Identification and characterization of the C3 binding domain of the Staphylococcus aureus extracellular fibrinogen-binding protein (Efb). J. Biol. Chem. 279(49):50710-50716, 2004. (Pubitemid 40017808)
29. Lee, L. P., and B. Tidor. Optimization of binding electrostatics: charge complementarity in the barnase-barstar protein complex. Protein Sci. 10(2):362-377, 2001. (Pubitemid 32225656)
30. MacKerell, A. D., D. Bashford, M. Bellott, R. L. Dunbrack, J. D. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, W. E. Reiher, B. Roux, M. Schlenkrich, J. C. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin, and M. Karplus. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102(18):3586-3616, 1998. (Pubitemid 128576688)
31. Mallik, B., L. Zhang, S. Koide, and D. Morikis. pH dependence of stability of the 10th human fibronectin type III domain: a computational study. Biotechnol. Prog. 24(1):48-55, 2008. (Pubitemid 351231249)
32. Marti-Renom, M. A., A. C. Stuart, A. Fiser, R. Sanchez, F. Melo, and A. Sali. Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. 29:291-325, 2000. (Pubitemid 30599596)
33. McCammon, J. A., S. H. Northrup, and S. A. Allison. Diffusional dynamics of ligand receptor association. J. Phys. Chem. 90(17):3901-3905, 1986.
34. Morikis, D., and J. D. Lambris. Structural Biology of the Complement System. Boca Raton: Taylor & Francis/CRC Press, 2005.
35. Morikis, D., A. K. Rizos, D. Spandidos, and E. Krambovitis. Electrostatic modeling of peptides derived from the V3-loop of HIV-1 gp120: implications in the interaction with chemokine receptor CCR5. Int. J. Mol. Med. 19(3):343-352, 2007.
36. Nizet, V. Understanding how leading bacterial pathogens subvert innate immunity to reveal novel therapeutic targets. J. Allergy Clin. Immunol. 120(1):13-22, 2007. (Pubitemid 46990514)
37. Petke, J. D. Cumulative and discrete similarity analysis of electrostatic potentials and fields. J. Comput. Chem. 14(8):928-933, 1993.
38. Phillips, J. C., R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R. D. Skeel, L. Kale, and K. Schulten. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26(16):1781-1802, 2005. (Pubitemid 43078511)
39. Pyaram, K., C. A. Kieslich, V. N. Yadav, D. Morikis, and A. Sahu. Influence of electrostatics on the complement regulatory functions of Kaposica, the complement inhibitor of Kaposi's Sarcoma-associated herpesvirus. J. Immunol. 184(4):1956-1967, 2010.
40. Qureshi, N. N., D. Morikis, and N. L. Schiller. Contribution of specific amino acid changes in penicillin binding protein 1 to amoxicillin resistance in clinical Helicobacter pylori isolates. Antimicrob. Agents Chemother. 55(1):101-109, 2011.
41. R Development Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria 2008. ISBN 3-900051-07-0. URL http://www.R-project.org.
42. Ricklin, D., S. K. Ricklin-Lichtsteiner, M. M. Markiewski, B. V. Geisbrecht, and J. D. Lambris. Cutting edge: members of the Staphylococcus aureus extracellular fibrinogen-binding protein family inhibit the interaction of C3d with complement receptor 2. J. Immunol. 181(11):7463-7467, 2008.
43. Rooijakkers, S. H. M., J. Wu, M. Ruyken, R. van Domselaar, K. L. Planken, A. Tzekou, D. Ricklin, J. D. Lambris, B. J. C. Janssen, J. A. G. van Strijp, and P. Gros. Structural and functional implications of the alternative complement pathway C3 convertase stabilized by a staphylococcal inhibitor. Nat. Immunol. 10(7):721-727, 2009.
44. Ruíz-Gomez, G., J. Lim, M. A. Halili, G. T. Le, P. K. Madala, G. Abbenante, and D. P. Fairlie. Structure-activity relationships for substrate-based inhibitors of human complement factor B. J. Med. Chem. 52(19):6042-6052, 2009.
45. Serruto, D., R. Rappuoli, M. Scarselli, P. Gros, and J. A. G. van Strijp. Molecular mechanisms of complement evasion: learning from staphylococci and meningococci. Nat. Rev. Microbiol. 8(6):393-399, 2010.
46. Sfyroera, G., M. Katragadda, D. Morikis, S. N. Isaacs, and J. D. Lambris. Electrostatic modeling predicts the activities of orthopoxvirus complement control proteins. J. Immunol. 174(4):2143-2151, 2005. (Pubitemid 40223958)
47. Sheinerman, F. B., R. Norel, and B. Honig. Electrostatic aspects of protein-protein interactions. Curr. Opin. Struct. Biol. 10(2):153-159, 2000. (Pubitemid 30198940)
48. Sibbald, M., A. K. Ziebandt, S. Engelmann, M. Hecker, A. de Jong, H. J. A. Harmsen, G. C. Raangs, I. Stokroos, J. P. Arends, J. Y. F. Dubois, and J. A. van Dijl. Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol. Mol. Biol. Rev. 70(3):755-788, 2006. (Pubitemid 44484692)
49. Simonson, T. Electrostatics and dynamics of proteins. Rep. Prog. Phys. 66(5):737-787, 2003. (Pubitemid 36685137)
50. Sitkoff, D., K. A. Sharp, and B. Honig. Accurate calculation of hydration free-energies using macroscopic solvent models. J. Phys. Chem. 98(7):1978-1988, 1994.
51. Torreira, E., A. Tortajada, T. Montes, S. de Rodriguez Córdoba, and O. Llorca. Coexistence of closed and open conformations of complement factor B in the alternative pathway C3bB(Mg2+) proconvertase. J. Immunol. 183(11):7347-7351, 2009.
52. Torreira, E., A. Tortajada, T. Montes, S. de Rodriguez Córdoba, and O. Llorca. 3D structure of the C3bB complex provides insights into the activation and regulation of the complement alternative pathway convertase. Proc. Natl Acad. Sci. USA. 106(3):882-887, 2009.
53. Wade, R. C., R. R. Gabdoulline, and F. Rienzo. Protein interaction property similarity analysis. Int. J. Quantum Chem. 83(3-4):122-127, 2001. (Pubitemid 32517562)
54. Walport, M. J. Advances in immunology: complement (first of two parts). N. Engl. J. Med. 344(14):1058-1066, 2001. (Pubitemid 32267977)
55. Warshel, A., P. K. Sharma, M. Kato, and W. W. Parson. Modeling electrostatic effects in proteins. Biochim. Biophys. Acta 1764(11):1647-1676, 2006. (Pubitemid 46070172)
56. Wu, J., Y. Q. Wu, D. Ricklin, J. D. Lambris, and P. Gros. Structure of complement fragment C3b-factor H and implications for host protection by complement regulators. Nat. Immunol. 10(7):728-734, 2009.
57. Wyatt, M. A., W. Wang, C. M. Roux, F. C. Beasley, D. E. Heinrichs, P. M. Dunman, and N. A. Magarvey. Staphylococcus aureus nonribosomal peptides secondary metabolites regulate virulence. Science 329(5989):294-296, 2010.
58. Xu, Y., S. V. L. Narayana, and J. E. Volanakis. Structural biology of the alternative pathway convertase. Immunol. Rev. 180:123-135, 2001. (Pubitemid 32472857)
59. Zhang, X. Y., C. L. Bajaj, B. Kwon, T. J. Dolinsky, J. E. Nielsen, and N. A. Baker. Application of new multiresolution methods for the comparison of biomolecular electrostatic properties in the absence of global structure similarity. Multiscale Model. Simul. 5(4):1196-1213, 2006. (Pubitemid 350285619)
60. Zhang, L., B. Mallik, and D. Morikis. Immunophysical exploration of C3d-CR2(CCP1-2) interaction using molecular dynamics and electrostatics. J. Mol. Biol. 369(2):567-583, 2007. (Pubitemid 46678038)
61. Zhang, L., and D. Morikis. Immunophysical properties and prediction of activities for vaccinia virus complement control protein and smallpox inhibitor of complement enzymes using molecular dynamics and electrostatics. Biophys. J. 90(9):3106-3119, 2006.