Peptide inhibitors of viral assembly: A novel route to broad-spectrum antivirals

Journal of Chemical Information and Modeling

Volumn 52, Issue 3, 2012, Pages 770-776

  Elsawy, Karim M ^a   Twarock, Reidun ^a   Verma, Chandra S ^b,c,d   Caves, Leo S D ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b BIOINFORMATICS INSTITUTE   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BIOINFORMATICS; DRUG THERAPY; VIRUSES;

BLOCK INTERFACES; COMPETITIVE INTERACTIONS; DOCKING SIMULATIONS; INTERFACE REGIONS; PEPTIDE INHIBITORS; PROTEIN INTERFACES; PROTEIN-PROTEIN INTERFACE; SECONDARY STRUCTURES;

PEPTIDES;

ANTIVIRUS AGENT; CAPSID PROTEIN; OLIGOPEPTIDE; PEPTIDE FRAGMENT;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG DEVELOPMENT; DRUG EFFECT; METABOLISM; PROTEIN CONFORMATION; SPECIES DIFFERENCE; VIRUS; VIRUS ASSEMBLY;

AMINO ACID SEQUENCE; ANTIVIRAL AGENTS; CAPSID PROTEINS; DRUG DISCOVERY; MODELS, MOLECULAR; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; SPECIES SPECIFICITY; VIRUS ASSEMBLY; VIRUSES;

EID: 84859184542     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci200467s     Document Type: Article

References (52)

1. Klug, A. From virus structure to chromatin: X-ray diffraction to three-dimensional electron microscopy Annu. Rev. Biochem. 2010, 79, 1-35
2. Matsui, T.; Tsuruta, H.; Johnson, J. E. Balanced electrostatic and structural forces guide the large conformational change associated with maturation of T = 4 virus Biophys. J. 2010, 98 (7) 1337-1343
3. Seibert, M. M.; Ekeberg, T.; Maia, F. R. N. C.; Svenda, M.; Andreasson, J.; Jonsson, O.; Odic, D.; Iwan, B.; Rocker, A.; Westphal, D.; Hantke, M.; DePonte, D. P.; Barty, A.; Schulz, J.; Gumprecht, L.; Coppola, N.; Aquila, A.; Liang, M.; White, T. A.; Martin, A.; Caleman, C.; Stern, S.; Abergel, C.; Seltzer, V.; Claverie, J.-M.; Bostedt, C.; Bozek, J. D.; Boutet, S.; Miahnahri, A. A.; Messerschmidt, M.; Krzywinski, J.; Williams, G.; Hodgson, K. O.; Bogan, M. J.; Hampton, C. Y.; Sierra, R. G.; Starodub, D.; Andersson, I.; Bajt, S.; Barthelmess, M.; Spence, J. C. H.; Fromme, P.; Weierstall, U.; Kirian, R.; Hunter, M.; Doak, R. B.; Marchesini, S.; Hau-Riege, S. P.; Frank, M.; Shoeman, R. L.; Lomb, L.; Epp, S. W.; Hartmann, R.; Rolles, D.; Rudenko, A.; Schmidt, C.; Foucar, L.; Kimmel, N.; Holl, P.; Rudek, B.; Erk, B.; Homke, A.; Reich, C.; Pietschner, D.; Weidenspointner, G.; Struder, L.; Hauser, G.; Gorke, H.; Ullrich, J.; Schlichting, I.; Herrmann, S.; Schaller, G.; Schopper, F.; Soltau, H.; Kuhnel, K.-U.; Andritschke, R.; Schroter, C.-D.; Krasniqi, F.; Bott, M.; Schorb, S.; Rupp, D.; Adolph, M.; Gorkhover, T.; Hirsemann, H.; Potdevin, G.; Graafsma, H.; Nilsson, B.; Chapman, H. N.; Hajdu, J. Single mimivirus particles intercepted and imaged with an X-ray laser Nature 2011, 470 (7332) 78-81
4. Zhang, X.; Jin, L.; Fang, Q.; Hui, W. H.; Zhou, Z. H. 3.3 Å Cryo-EM Structure of a Nonenveloped Virus Reveals a Priming Mechanism for Cell Entry Cell 2010, 141 (3) 472-482
5. Toropova, K.; Basnak, G.; Twarock, R.; Stockley, P. G.; Ranson, N. A. The Three-dimensional Structure of Genomic RNA in Bacteriophage MS2: Implications for Assembly J. Mol. Biol. 2008, 375 (3) 824-836
6. Kuhn, R. J.; Zhang, W.; Rossmann, M. G.; Pletnev, S. V.; Corver, J.; Lenches, E.; Jones, C. T.; Mukhopadhyay, S.; Chipman, P. R.; Strauss, E. G.; Baker, T. S.; Strauss, J. H. Structure of Dengue Virus: Implications for Flavivirus Organization, Maturation, and Fusion Cell 2002, 108 (5) 717-725
7. Bamford, D. H.; Grimes, J. M.; Stuart, D. I. What does structure tell us about virus evolution? Curr. Opin. Struct. Biol. 2005, 15 (6) 655-663
8. Jones, K. E.; Patel, N. G.; Levy, M. A.; Storeygard, A.; Balk, D.; Gittleman, J. L.; Daszak, P. Global trends in emerging infectious diseases Nature 2008, 451 (7181) 990-993
9. Joachim, D. Transspecies transmissions of retroviruses: New cases Virology 2007, 369 (2) 229-233
10. Gao, F.; Bailes, E.; Robertson, D. L.; Chen, Y.; Rodenburg, C. M.; Michael, S. F.; Cummins, L. B.; Arthur, L. O.; Peeters, M.; Shaw, G. M.; Sharp, P. M.; Hahn, B. H. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes Nature 1999, 397 (6718) 436-441
11. The Chinese, S. M. E. C. Molecular Evolution of the SARS Coronavirus During the Course of the SARS Epidemic in China Science 2004, 303 (5664) 1666-1669
12. Wolf, M. C.; Freiberg, A. N.; Zhang, T.; Akyol-Ataman, Z.; Grock, A.; Hong, P. W.; Li, J.; Watson, N. F.; Fang, A. Q.; Aguilar, H. C.; Porotto, M.; Honko, A. N.; Damoiseaux, R.; Miller, J. P.; Woodson, S. E.; Chantasirivisal, S.; Fontanes, V.; Negrete, O. A.; Krogstad, P.; Dasgupta, A.; Moscona, A.; Hensley, L. E.; Whelan, S. P.; Faull, K. F.; Holbrook, M. R.; Jung, M. E.; Lee, B. A broad-spectrum antiviral targeting entry of enveloped viruses Proc. Natl. Acad. Sci. U. S. A. 2010, 10.1073/pnas.0909587107
13. Melikyan, G. B. Driving a wedge between viral lipids blocks infection Proc. Natl. Acad. Sci. U. S. A. 2010, 107 (40) 17069-17070
14. Rider, T. H.; Zook, C. E.; Boettcher, T. L.; Wick, S. T.; Pancoast, J. S.; Zusman, B. D. Broad-Spectrum Antiviral Therapeutics PLoS One 2011, 6 (7) e22572
15. Zutshi, R.; Brickner, M.; Chmielewski, J. Inhibiting the assembly of protein-protein interfaces Curr. Opin. Chem. Biol. 1998, 2 (1) 62-66
16. Arkin, M. R.; Wells, J. A. Small-molecule inhibitors of protein-protein interactions: progressing towards the dream Nat. Rev. Drug Discovery 2004, 3 (4) 301-317
17. Moreira, I. S.; Fernandes, P. A.; Ramos, M. J. Hot spots-A review of the protein-protein interface determinant amino-acid residues Proteins: Struct., Funct., Bioinf. 2007, 68 (4) 803-812
18. Gonzalez-Ruiz, D.; Gohlke, H. Targeting protein-protein interactions with small molecules: Challenges and perspectives for computational binding epitope detection and ligand finding Curr. Med. Chem. 2006, 13 (22) 2607-2625
19. Fox, J. L. Antivirals become a broader enterprise Nat. Biotechnol. 2007, 25 (12) 1395-1402
20. Cejka, D.; Losert, D.; Wacheck, V. Short interfering RNA (siRNA): Tool or therapeutic? Clin. Sci. (London) 2006, 110 (1) 47-58
21. Verma, C.; Seebah, S.; Low, S. M.; Zhou, L.; Liu, S. P.; Li, J.; Beuerman, R. W. Defensins: antimicrobial peptides for therapeutic development Biotechnol. J. 2007, 2 (11) 1353-1359
22. Heizmann, J.; Langguth, P.; Biber, A.; Oschmann, R.; Merkle, H. P.; Wolffram, S. Enzymatic cleavage of thymopoietin oligopeptides by pancreatic and intestinal brush-border enzymes Peptides 1996, 17 (7) 1083-1089
23. Taki, Y.; Sakane, T.; Nadai, T.; Sezaki, H.; Amidon, G. L.; Langguth, P.; Yamashita, S. Gastrointestinal absorption of peptide drug: quantitative evaluation of the degradation and the permeation of metkephamid in rat small intestine J. Pharmacol. Exp. Ther. 1995, 274 (1) 373-377
24. Branco, M. C.; Schneider, J. P. Self-assembling materials for therapeutic delivery Acta Biomater. 2009, 5 (3) 817-831
25. Kogan, M. J.; Olmedo, I.; Hosta, L.; Guerrero, A. R.; Cruz, L. J.; Albericio, F. Peptides and metallic nanoparticles for biomedical applications Nanomedicine 2007, 2 (3) 287-306
26. Maher, S.; Brayden, D. J.; Feighery, L.; McClean, S. Cracking the junction: Update on the progress of gastrointestinal absorption enhancement in the delivery of poorly absorbed drugs Crit. Rev. Ther. Drug Carrier Syst. 2008, 25 (2) 117-168
27. Guo, Z.; Mohanty, U.; Noehre, J.; Sawyer, T. K.; Sherman, W.; Krilov, G. Probing the α-Helical Structural Stability of Stapled p53 Peptides: Molecular Dynamics Simulations and Analysis Chem. Biol. Drug Des. 2010, 75 (4) 348-359
28. Walensky, L. D.; Kung, A. L.; Escher, I.; Malia, T. J.; Barbuto, S.; Wright, R. D.; Wagner, G.; Verdine, G. L.; Korsmeyer, S. J. Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix Science 2004, 305, 1466-1470
29. Otvos, L., Jr. Peptide-based drug design: here and now Methods Mol. Biol. 2008, 494, 1-8
30. Kritzer, J. A. Stapled peptides: Magic bullets in nature's arsenal Nat. Chem. Biol. 2010, 6 (8) 566-567
31. Jochim, A. L.; Arora, P. S. Systematic analysis of helical protein interfaces reveals targets for synthetic inhibitors ACS Chem. Biol. 2010, 5 (10) 919-923
32. Qureshi, N. M.; Coy, D. H.; Garry, R. F.; Henderson, L. A. Characterization of a putative cellular receptor for HIV-1 transmembrane glycoprotein using synthetic peptides AIDS 1990, 4 (6) 553-558
33. Lambert, D. M.; Barney, S.; Lambert, A. L.; Guthrie, K.; Medinas, R.; Davis, D. E.; Bucy, T.; Erickson, J.; Merutka, G.; Petteway, S. R., Jr. Peptides from conserved regions of paramyxovirus fusion (F) proteins are potent inhibitors of viral fusion Proc Natl Acad Sci U S A 1996, 93 (5) 2186-2191
34. Bultmann, H.; Brandt, C. R. Peptides containing membrane-transiting motifs inhibit virus entry J. Biol. Chem. 2002, 277 (39) 36018-23
35. Okazaki, K.; Kida, H. A synthetic peptide from a heptad repeat region of herpesvirus glycoprotein B inhibits virus replication J. Gen. Virol. 2004, 85 (Pt 8) 2131-2137
36. Root, M. J.; Steger, H. K. HIV-1 gp41 as a target for viral entry inhibition Curr. Pharm. Des. 2004, 10 (15) 1805-1825
37. Hetényi, C.; van der Spoel, D. Blind docking of drug-sized compounds to proteins with up to a thousand residues FEBS Lett. 2006, 580 (5) 1447-1450
38. Reddy, V. S.; Natarajan, P.; Okerberg, B.; Li, K.; Damodaran, K. V.; Morton, R. T.; Brooks, C. L., III; Johnson, J. E. Virus particle explorer (VIPER), a website for virus capsid structures and their computational analyses J. Virol. 2001, 75 (24) 11943-11947
39. Kabsch, W.; Sander, C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features Biopolymers 1983, 22 (12) 2577-2637
40. Hetenyi, C.; van der Spoel, D. Efficient docking of peptides to proteins without prior knowledge of the binding site Protein Sci. 2002, 11 (7) 1729-1737
41. Morris, G. M.; Huey, R.; Lindstrom, W.; Sanner, M. F.; Belew, R. K.; Goodsell, D. S.; Olson, A. J. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility J. Comput. Chem. 2009, 30 (16) 2785-2791
42. Garrett, M. M.; David, S. G.; Robert, S. H.; Ruth, H.; William, E. H.; Richard, K. B.; Arthur, J. O. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function J. Comput. Chem. 1998, 19 (14) 1639-1662
43. Schafmeister, C. E.; Po, J.; Verdine, G. L. An all-hydrocarbon cross-linking system for enhancing the helicity and metabolic stability of peptides J. Am. Chem. Soc. 2000, 122 (24) 5891-5892
44. Kritzer, J. A. Stapled peptides: Magic bullets in nature's arsenal Nat. Chem. Biol. 2010, 6 (8) 566-567
45. Horton, N.; Lewis, M. Calculation of the free energy of association for protein complexes Protein Sci. 1992, 1 (1) 169-181
46. Tidor, B.; Karplus, M. The contribution of vibrational entropy to molecular association. The dimerization of insulin J. Mol. Biol. 1994, 238 (3) 405-414
47. Vincent, Z.; Markus, M.; Martin, K. Study of the insulin dimerization: Binding free energy calculations and per-residue free energy decomposition Proteins: Struct., Funct., Bioinf. 2005, 61 (1) 79-93
48. Bogan, A. A.; Thorn, K. S. Anatomy of hot spots in protein interfaces J. Mol. Biol. 1998, 280 (1) 1-9
49. Tuncbag, N.; Gursoy, A.; Keskin, O. Identification of computational hot spots in protein interfaces: Combining solvent accessibility and inter-residue potentials improves the accuracy Bioinformatics 2009, 25 (12) 1513-1520
50. Tuncbag, N.; Keskin, O.; Gursoy, A. HotPoint: Hot spot prediction server for protein interfaces Nucleic Acids Res. 2010, 38 (Web Server issue) W402-W406
51. Keskin, O.; Nussinov, R. Favorable scaffolds: Proteins with different sequence, structure and function may associate in similar ways Protein Eng., Des. Sel. 2005, 18 (1) 11-24
52. Tuncbag, N.; Gursoy, A.; Guney, E.; Nussinov, R.; Keskin, O. Architectures and functional coverage of protein-protein interfaces J. Mol. Biol. 2008, 381 (3) 785-802