Forcefield-NCAA: Ab initio charge parameters to aid in the discovery and design of therapeutic proteins and peptides with unnatural amino acids and their application to complement inhibitors of the compstatin family

ACS Synthetic Biology

Volumn 3, Issue 12, 2014, Pages 855-869

  Khoury, George A ^a   Smadbeck, James ^a   Tamamis, Phanourios ^a   Vandris, Andrew C ^a   Kieslich, Chris A ^a   Floudas, Christodoulos A ^a  

^a Princeton University   (United States)

Author keywords

AMBER partial charges; complement; Compstatin; inhibitors; molecular dynamics; noncanonical amino acids; unnatural amino acids

Indexed keywords

AMINO ACID DERIVATIVE; COMPLEMENT INHIBITOR; COMPSTATIN; PEPTIDE DERIVATIVE; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG; AMINO ACID; CYCLOPEPTIDE; PEPTIDE; PROTEIN; PROTEIN BINDING;

AB INITIO CALCULATION; AMINO ACID SUBSTITUTION; ARTICLE; COMPLEMENT ACTIVATION; DRUG DESIGN; DRUG SCREENING; HYDROGEN BOND; IC50; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULAR MODEL; PROTEIN STRUCTURE; STATIC ELECTRICITY; CHEMISTRY; DRUG DEVELOPMENT; INTERNET; METABOLISM; PROCEDURES; RECEIVER OPERATING CHARACTERISTIC; STATISTICAL MODEL; THERMODYNAMICS;

AMINO ACIDS; DRUG DISCOVERY; INTERNET; MODELS, STATISTICAL; MOLECULAR DYNAMICS SIMULATION; PEPTIDES; PEPTIDES, CYCLIC; PROTEIN BINDING; PROTEINS; ROC CURVE; THERMODYNAMICS;

EID: 84914111095     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/sb400168u     Document Type: Article

References (88)

1. Wang, J. and Hou, T. (2011) Recent advances on aqueous solubility prediction Comb. Chem. High Throughput Screening 14, 328-338
2. Andrade, C. H., Pasqualoto, K. F. M., Ferreira, E. I., and Hopfinger, A. J. (2009) Rational design and 3D-pharmacophore mapping of 5-thiourea-substituted α-thymidine analogues as mycobacterial TMPK inhibitors J. Chem. Inf. Model. 49, 1070-1078
3. Vlieghe, P., Lisowski, V., Martinez, J., and Khrestchatisky, M. (2010) Synthetic therapeutic peptides: Science and market Drug Discovery Today 15, 40-56
4. Craik, D. J., Fairlie, D. P., Liras, S., and Price, D. (2013) The future of peptide-based drugs Chem. Biol. Drug Des. 81, 136-147
5. Adessi, C. and Soto, C. (2002) Converting a peptide into a drug: Strategies to improve stability and bioavailability Curr. Med. Chem. 9, 963-978
6. Miller, S. M., Simon, R. J., Ng, S., Zuckermann, R. N., Kerr, J. M., and Moos, W. H. (1995) Comparison of the proteolytic susceptibilities of homologous l -amino acid, d -amino acid, and N-substituted glycine peptide and peptoid oligomers Drug Dev. Res. 35, 20-32
7. Khoury, G. A., Baliban, R. C., and Floudas, C. A. (2011) Proteome-wide post-translational modification statistics: Frequency analysis and curation of the SWISS-PROT database Sci. Rep. 1, 1-5
8. Bairoch, A. and Apweiler, R. (2000) The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000 Nucleic Acids Res. 28, 45-48
9. Khoury, G. A., Smadbeck, J., Kieslich, C. A., and Floudas, C. A. (2013) Protein folding and de novo protein design for biotechnological applications Trends Biotechnol. 10.1016/j.tibtech.2013.10.008
10. Walsh, C. T. (2006) Posttranslational Modification of Proteins: Expanding Natures Inventory; Roberts and Co. Publishers, Englewood, CO, pp xxi, 490.
11. Merrifield, R. B. (1963) Solid phase peptide synthesis. I. The synthesis of a tetrapeptide J. Am. Chem. Soc. 85, 2149-2154
12. Chalker, J. M. and Davis, B. G. (2010) Chemical mutagenesis: selective post-expression interconversion of protein amino acid residues Curr. Opin. Chem. Biol. 14, 781-789
13. Chalker, J. M., Bernardes, G. J. L., and Davis, B. G. (2011) A tag-and-modify approach to site-selective protein modification Acc. Chem. Res. 44, 730-741
14. Johnson, J. A., Lu, Y. Y., Van Deventer, J. A., and Tirrell, D. A. (2010) Residue-specific incorporation of non-canonical amino acids into proteins: Recent developments and applications Curr. Opin. Chem. Biol. 14, 774-780
15. Neumann, H., Wang, K., Davis, L., Garcia-Alai, M., and Chin, J. W. (2010) Encoding multiple unnatural amino acids via evolution of a quadruplet-decoding ribosome Nature 464, 441-444
16. Wang, L., Xie, J., and Schultz, P. G. (2006) Expanding the genetic code Annu. Rev. Biophys. Biomol. Struct. 35, 225-249
17. Watanabe, T., Muranaka, N., and Hohsaka, T. (2008) Four-base codon-mediated saturation mutagenesis in a cell-free translation system J. Biosci. Bioeng. 105, 211-215
18. Mapelli, C. 2009, Eleven amino acid glucagon-like peptide-1 receptor agonists with antidiabetic activity J. Med. Chem. 52, 7788-7799
19. Sievers, S. A., Karanicolas, J., Chang, H. W., Zhao, A., Jiang, L., Zirafi, O., Stevens, J. T., Munch, J., Baker, D., and Eisenberg, D. (2011) Structure-based design of non-natural amino-acid inhibitors of amyloid fibril formation Nature 475, 96-100
20. Bakos, K., Havass, J., Fülöp, F., Gera, L., Stewart, J. M., Falkay, G., and Tóth, G. K. (2001) Synthesis and receptor binding of oxytocin analogs containing conformationally restricted amino acids Lett. Pept. Sci. 8, 35-40
21. Tamamura, H., Hiramatsu, K., Kusano, a. S., Terakubo, S., Yamamoto, N., Trent, J. O., Wang, Z., Peiper, S. C., Nakashima, H., Otaka, A., and Fujii, N. (2003) Synthesis of potent CXCR4 inhibitors possessing low cytotoxicity and improved biostability based on T140 derivatives Org. Biomol. Chem. 1, 3656-3662
22. Kokubu, T., Hiwada, K., Murakami, E., Imamura, Y., Matsueda, R., Yabe, Y., Koike, H., and Iijima, Y. (1985) Highly potent and specific inhibitors of human renin Hypertension 7, I8-11
23. Mallik, B., Katragadda, M., Spruce, L. A., Carafides, C., Tsokos, C. G., Morikis, D., and Lambris, J. D. (2005) Design and NMR characterization of active analogues of compstatin containing non-natural amino acids J. Med. Chem. 48, 274-286
24. Qu, H., Magotti, P., Ricklin, D., Wu, E. L., Kourtzelis, I., Wu, Y.-Q., Kaznessis, Y. N., and Lambris, J. D. (2011) Novel analogues of the therapeutic complement inhibitor compstatin with significantly improved affinity and potency Mol. Immunol. 48, 481-489
25. Leaver-Fay, A. 2011, Rosetta3 an object-oriented software suite for the simulation and design of macromolecules Methods Enzymol. 487, 545-574
26. Correia, B. E. 2010, Computational design of epitope-scaffolds allows induction of antibodies specific for a poorly immunogenic HIV vaccine epitope Structure 18, 1116-1126
27. Fleishman, S. J., Whitehead, T. A., Ekiert, D. C., Dreyfus, C., Corn, J. E., Strauch, E.-M., Wilson, I. A., and Baker, D. (2011) Computational design of proteins targeting the conserved stem region of influenza hemagglutinin Science 332, 816-821
28. Whitehead, T. A., Chevalier, A., Song, Y., Dreyfus, C., Fleishman, S. J., De Mattos, C., Myers, C. A., Kamisetty, H., Blair, P., Wilson, I. A., and Baker, D. (2012) Optimization of affinity, specificity, and function of designed influenza inhibitors using deep sequencing Nat. Biotechnol. 30, 543-548
29. Jiang, L., Althoff, E. A., Clemente, F. R., Doyle, L., Rothlisberger, D., Zanghellini, A., Gallaher, J. L., Betker, J. L., Tanaka, F., Barbas, I., Carlos, F., Hilvert, D., Houk, K. N., Stoddard, B. L., and Baker, D. (2008) De novo computational design of retro-aldol enzymes Science 319, 1387-1391
30. Richter, F. 2012, Computational design of catalytic dyads and oxyanion holes for ester hydrolysis J. Am. Chem. Soc. 134, 16197-16206
31. Althoff, E. A., Wang, L., Jiang, L., Giger, L., Lassila, J. K., Wang, Z., Smith, M., Hari, S., Kast, P., Herschlag, D., Hilvert, D., and Baker, D. (2012) Robust design and optimization of retroaldol enzymes Protein Sci. 21, 717-726
32. Siegel, J. B., Zanghellini, A., Lovick, H. M., Kiss, G., Lambert, A. R., St.Clair, J. L., Gallaher, J. L., Hilvert, D., Gelb, M. H., Stoddard, B. L., Houk, K. N., Michael, F. E., and Baker, D. (2010) Computational design of an enzyme catalyst for a stereoselective bimolecular Diels-Alder reaction Science 329, 309-313
33. Rothlisberger, D., Khersonsky, O., Wollacott, A. M., Jiang, L., DeChancie, J., Betker, J., Gallaher, J. L., Althoff, E. A., Zanghellini, A., Dym, O., Albeck, S., Houk, K. N., Tawfik, D. S., and Baker, D. (2008) Kemp elimination catalysts by computational enzyme design Nature 453, 190-195
34. Eiben, C. B., Siegel, J. B., Bale, J. B., Cooper, S., Khatib, F., Shen, B. W., Players, F., Stoddard, B. L., Popovic, Z., and Baker, D. (2012) Increased Diels-Alderase activity through backbone remodeling guided by Foldit players Nat. Biotechnol. 30, 190-192
35. Saraf, M. C., Moore, G. L., Goodey, N. M., Cao, V. Y., Benkovic, S. J., and Maranas, C. D. (2006) IPRO: an iterative computational protein library redesign and optimization procedure Biophys. J. 90, 4167-4180
36. Khoury, G. A., Fazelinia, H., Chin, J. W., Pantazes, R. J., Cirino, P. C., and Maranas, C. D. (2009) Computational design of Candida boidinii xylose reductase for altered cofactor specificity Protein Sci. 18, 2125-2138
37. Renfrew, P. D., Choi, E. J., Bonneau, R., and Kuhlman, B. (2012) Incorporation of noncanonical amino acids into Rosetta and use in computational protein-peptide interface design PLoS One 7, e32637
38. Petrov, D., Margreitter, C., Grandits, M., Oostenbrink, C., and Zagrovic, B. (2013) A systematic framework for molecular dynamics simulations of protein post-translational modifications PLoS Comput. Biol. 9, e1003154
39. Margreitter, C., Petrov, D., and Zagrovic, B. (2013) Vienna-PTM web server: A toolkit for MD simulations of protein post-translational modifications Nucleic Acids Res. 41, W422-W426
40. Klepeis, J. L., Floudas, C. A., Morikis, D., Tsokos, C. G., Argyropoulos, E., Spruce, L., and Lambris, J. D. (2003) Integrated computational and experimental approach for lead optimization and design of compstatin variants with improved activity J. Am. Chem. Soc. 125, 8422-8423
41. Klepeis, J. L., Floudas, C. A., Morikis, D., Tsokos, C. G., and Lambris, J. D. (2004) Design of peptide analogues with improved activity using a novel de novo protein design approach Ind. Eng. Chem. Res. 43, 3817-3826
42. Bellows, M. L., Taylor, M. S., Cole, P. A., Shen, L., Siliciano, R. F., Fung, H. K., and Floudas, C. A. (2010) Discovery of entry inhibitors for HIV-1 via a new de novo protein design framework Biophys. J. 99, 3445-3453
43. Bellows, M. L., Fung, H. K., Taylor, M. S., Floudas, C. A., Lopez de Victoria, A., and Morikis, D. (2010) New compstatin variants through two de novo protein design frameworks Biophys. J. 98, 2337-2346
44. Fung, H. K., Floudas, C. A., Taylor, M. S., Zhang, L., and Morikis, D. (2008) Toward full-sequence de novo protein design with flexible templates for human β-defensin-2 Biophys. J. 94, 584-599
45. Bellows-Peterson, M. L., Fung, H. K., Floudas, C. A., Kieslich, C. A., Zhang, L., Morikis, D., Wareham, K. J., Monk, P. N., Hawksworth, O. A., and Woodruff, T. M. (2012) De novo peptide design with C3a receptor agonist and antagonist activities: Theoretical predictions and experimental validation J. Med. Chem. 55, 4159-4168
46. Smadbeck, J., Peterson, M. B., Khoury, G. A., Taylor, M. S., and Floudas, C. A. (2013) Protein WISDOM: A workbench for in silico de novo design of biomolecules J. Visualized Exp. e50476
47. Lopez de Victoria, A., Gorham, R. D., Bellows-Peterson, M. L., Ling, J., Lo, D. D., Floudas, C. A., and Morikis, D. (2011) A new generation of potent complement inhibitors of the compstatin family Chem. Biol. Drug Des. 77, 431-440
48. Bellows, M. L. and Floudas, C. A. (2010) Computational methods for de novo protein design and its applications to the human immunodeficiency virus 1, purine nucleoside phosphorylase, ubiquitin specific protease 7, and histone demethylases Curr. Drug Targets 11, 264-278
49. Tamamis, P., López de Victoria, A., Gorham, R. D., Bellows-Peterson, M. L., Pierou, P., Floudas, C. A., Morikis, D., and Archontis, G. (2012) Molecular dynamics in drug design: New generations of compstatin analogs Chem. Biol. Drug Des. 79, 703-718
50. Khoury, G. A., Thompson, J. P., Smadbeck, J., Kieslich, C. A., and Floudas, C. A. (2013) Forcefield-PTM: Ab initio charge and AMBER forcefield parameters for frequently occurring post-translational modifications J. Chem. Theory Comput. 9, 5653-5674
51. Duan, Y., Wu, C., Chowdhury, S., Lee, M. C., Xiong, G., Zhang, W., Yang, R., Cieplak, P., Luo, R., Lee, T., Caldwell, J., Wang, J., and Kollman, P. (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations J. Comput. Chem. 24, 1999-2012
52. Magotti, P., Ricklin, D., Qu, H., Wu, Y.-Q., Kaznessis, Y. N., and Lambris, J. D. (2009) Structure-kinetic relationship analysis of the therapeutic complement inhibitor compstatin J. Mol. Recognit. 22, 495-505
53. Gorham, R. D., Jr, Forest, D. L., Tamamis, P., López de Victoria, A., Kraszni, M., Kieslich, C. A., Banna, C. D., Bellows-Peterson, M. L., Larive, C. K., Floudas, C. A., Archontis, G., Johnson, L. V., and Morikis, D. (2013) Novel compstatin family peptides inhibit complement activation by drusen-like deposits in human retinal pigmented epithelial cell cultures Exp. Eye Res. 116C, 96-108
54. Brooks, B. R. 2009, CHARMM: The biomolecular simulation program J. Comput. Chem. 30, 1545-1614
55. Janssen, B. J. C., Halff, E. F., Lambris, J. D., and Gros, P. (2007) Structure of compstatin in complex with complement component C3c reveals a new mechanism of complement inhibition J. Biol. Chem. 282, 29241-29247
56. Tamamis, P., Morikis, D., Floudas, C. A., and Archontis, G. (2010) Species specificity of the complement inhibitor compstatin investigated by all-atom molecular dynamics simulations Proteins: Struct., Funct., Bioinf. 78, 2655-2667
57. Tamamis, P., Pierou, P., Mytidou, C., Floudas, C. A., Morikis, D., and Archontis, G. (2011) Design of a modified mouse protein with ligand binding properties of its human analog by molecular dynamics simulations: The case of C3 inhibition by compstatin Proteins: Struct., Funct., Bioinf. 79, 3166-3179
58. Zhang, Y. and Skolnick, J. (2005) TM-align: A protein structure alignment algorithm based on the TM-score Nucleic Acids Res. 33, 2302-2309
59. MarvinSketch, version 6.0.3; (2010) ChemAxon, Budapest, Hungary.
60. TINKER, version 5.0; (2010) Washington University, St. Louis, MO.
61. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules J. Am. Chem. Soc. 117, 5179-5197
62. Frisch, M. J. (2004) Gaussian 03, Revision C.02; Gaussian Inc., Wallingford, CT.
63. Lee, C., Yang, W., and Parr, R. G. (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density Phys. Rev. B 37, 785
64. Miehlich, B., Savin, A., Stoll, H., and Preuss, H. (1989) Results obtained with the correlation energy density functionals of Becke and Lee, Yang, and Parr Chem. Phys. Lett. 157, 200-206
65. Becke, A. D. (1993) Density-functional thermochemistry. III. The role of exact exchange J. Chem. Phys. 98, 5648-5652
66. Kendall, R. A., Thom H. Dunning, J., and Harrison, R. J. (1992) Electron affinities of the first-row atoms revisited. Systematic basis sets and wave functions J. Chem. Phys. 96, 6796-6806
67. Mennucci, B., Cammi, R., and Tomasi, J. (1999) Analytical free energy second derivatives with respect to nuclear coordinates: Complete formulation for electrostatic continuum solvation models J. Chem. Phys. 110, 6858-6870
68. Tomasi, J., Mennucci, B., and Cances, E. (1999) The IEF version of the PCM solvation method: An overview of a new method addressed to study molecular solutes at the QM ab initio level J. Mol. Struct.: THEOCHEM 464, 211-226
69. Richards, F. M. (1977) Areas, Volumes, Packing, and Protein Structure Annu. Rev. Biophys. Bioeng. 6, 151-176
70. Wang, J., Wang, W., Kollman, P. A., and Case, D. A. (2006) Automatic atom type and bond type perception in molecular mechanical calculations J. Mol. Graph. Model. 25, 247-260
71. Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., and Case, D. A. (2004) Development and testing of a general Amber force field J. Comput. Chem. 25, 1157-1174
72. Janeway, C. A., Travers, P., Walport, M., and Shlomchik, M. J. (2001) Immunobiology; Garland Science, New York.
73. Sahu, A., Morikis, D., and Lambris, J. D. (2003) Compstatin, a peptide inhibitor of complement, exhibits species-specific binding to complement component C3 Mol. Immunol. 39, 557-566
74. Kovacs, G. G., Gasque, P., Ströbel, T., Lindeck-Pozza, E., Strohschneider, M., Ironside, J. W., Budka, H., and Guentchev, M. (2004) Complement activation in human prion disease Neurobiol. Dis. 15, 21-28
75. Java, A., Atkinson, J., and Salmon, J. (2013) Defective complement inhibitory function predisposes to renal disease Annu. Rev. Med. 64, 307-324
76. Ricklin, D. and Lambris, J. D. (2013) Complement in immune and inflammatory disorders: Therapeutic interventions J. Immunol. 190, 3839-3847
77. Rensen, S. S., Slaats, Y., Driessen, A., Peutz-Kootstra, C. J., Nijhuis, J., Steffensen, R., Greve, J. W., and Buurman, W. A. (2009) Activation of the complement system in human nonalcoholic fatty liver disease Hepatology 50, 1809-1817
78. PyMOL, version 1.3; Delano Scientific LLC, 2008.
79. Chiu, T.-L., Mulakala, C., Lambris, J. D., and Kaznessis, Y. N. (2008) Development of a new pharmacophore model that discriminates active compstatin analogs Chem. Biol. Drug Des. 72, 249-256
80. Case, D. A. (2010) Amber 11, University of California, San Francisco.
81. Onufriev, A., Bashford, D., and Case, D. A. (2000) Modification of the generalized Born Model suitable for macromolecules J. Phys. Chem. B 104, 3712-3720
82. Onufriev, A., Bashford, D., and Case, D. A. (2004) Exploring protein native states and large-scale conformational changes with a modified generalized born model Proteins: Struct., Funct., Bioinf. 55, 383-394
83. Hou, T., Wang, J., Li, Y., and Wang, W. (2011) Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations J. Chem. Inf. Model. 51, 69-82
84. Xu, L., Sun, H., Li, Y., Wang, J., and Hou, T. (2013) Assessing the performance of MM/PBSA and MM/GBSA methods. 3. The impact of force fields and ligand charge models J. Phys. Chem. B 117, 8408-8421
85. Lilien, R. H., Stevens, B. W., Anderson, A. C., and Donald, B. R. (2005) A novel ensemble-based scoring and search algorithm for protein redesign and its application to modify the substrate specificity of the gramicidin synthetase a phenylalanine adenylation enzyme J. Comput. Biol. 12, 740-761
86. Lidl, R. and Neiderreiter, H. (1983) Finite fields. In Encyclopedia of Mathematics and its Applications, Addision-Wesley, Reading, MA.
87. Miller, B. R., III, McGee, T. D., Jr, Swails, J. M., Homeyer, N., Gohlke, H., and Roitberg, A. E. (2012) MMPBSA. py: An efficient program for end-state free energy calculations J. Chem. Theory Comput. 8, 3314-3321
88. Katragadda, M., Magotti, P., Sfyroera, G., and Lambris, J. D. (2006) Hydrophobic effect and hydrogen bonds account for the improved activity of a complement inhibitor, compstatin J. Med. Chem. 49, 4616-4622