Molecular engineering of RANTES peptide mimetics with potent anti-HIV-1 activity

FASEB Journal

Volumn 25, Issue 4, 2011, Pages 1230-1243

  Lusso, Paolo ^a,b,e   Vangelista, Luca ^a   Cimbro, Raffaello ^a,e   Secchi, Massimiliano ^a   Sironi, Francesca ^a   Longhi, Renato ^c   Faiella, Marina ^d   Maglio, Ornella ^d,f   Pavone, Vincenzo ^d  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF CAGLIARI   (Italy)

^c CNR   (Italy)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^f CNR   (Italy)

Author keywords

AIDS; Antivirals; CCR5; Chemokines; Rational design; Viral receptors

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; GUANINE NUCLEOTIDE BINDING PROTEIN; RANTES;

ALGORITHM; ALPHA HELIX; ANTIVIRAL ACTIVITY; ARTICLE; BETA 1 PROTEIN STRAND; CARBOXY TERMINAL SEQUENCE; COMPUTER MODEL; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHOBICITY; N LOOP; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANTI-HIV AGENTS; BIOMIMETIC MATERIALS; CHEMOKINE CCL5; CHEMOTAXIS; HIV-1; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEPTIDES; PROTEIN CONFORMATION; PROTEIN ENGINEERING; RECEPTORS, CCR5; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79954597305     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-167627     Document Type: Article

References (40)

1. Berger, E. A., Murphy, P. M., and Farber, J. M. (1999) Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu. Rev. Immunol. 17, 657-700 (Pubitemid 29241137)
2. Lusso, P. (2006) HIV and the chemokine system: 10 years later. EMBO J. 25, 447-456
3. Lederman, M. M., Penn-Nicholson, A., Cho, M., and Mosier, D. (2006) Biology of CCR5 and its role in HIV infection and treatment. JAMA 296, 815-826 (Pubitemid 44223105)
4. Strizki, J. M., Xu, S., Wagner, N. E., Wojcik, L., Liu, J., Hou, Y., Endres, M., Palani, A., Shapiro, S., Clader, J. W., Greenlee, W. J., Tagat, J. R., McCombie, S., Cox, K., Fawzi, A. B., Chou, C. C., Pugliese-Sivo, C., Davies, L., Moreno, M. E., Ho, D. D., Trkola, A., Stoddart, C. A., Moore, J. P., Reyes, G. R., and Baroudy, B. M. (2001) SCH-C (SCH 351125), an orally bioavailable, small molecule antagonist of the chemokine receptor CCR5, is a potent inhibitor of HIV-1 infection in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 98, 12718-12723 (Pubitemid 33020012)
5. Strizki, J. M., Tremblay, C., Xu, S., Wojcik, L., Wagner, N., Gonsiorek, W., Hipkin, R. W., Chou, C. C., Pugliese-Sivo, C., Xiao, Y., Tagat, J. R., Cox, K., Priestley, T., Sorota, S., Huang, W., Hirsch, M., Reyes, G. R., and Baroudy, B. M. (2005) Discovery and characterization of vicriviroc (SCH 417690), a CCR5 antagonist with potent activity against human immunodeficiency virus type 1. Antimicrob. Agents Chemother. 49, 4911-4919 (Pubitemid 41782160)
6. Watson, C., Jenkinson, S., Kazmierski W, and Kenakin, T. (2005) The CCR5 receptor-based mechanism of action of 873140, a potent allosteric noncompetitive HIV entry inhibitor. Mol. Pharmacol. 67, 1268-1282 (Pubitemid 40410427)
7. Meanwell, N. A., and Kadow, J. F. (2007) Maraviroc, a chemokine CCR5 receptor antagonist for the treatment of HIV infection and AIDS. Curr. Opin. Investig. Drugs 8, 669-681 (Pubitemid 47205251)
8. Gulick, R. M., Lalezari, J., Goodrich, J., Clumeck, N., DeJesus, E., Horban, A., Nadler, J., Clotet, B., Karlsson, A., Wohlfeiler, M., Montana, J. B., McHale, M., Sullivan, J., Ridgway, C., Felstead, S., Dunne, M. W., van der Ryst, E., Mayer, H., and the MOTIVATE Study Teams. (2008) Maraviroc for previously treated patients with R5 HIV-1 infection. N. Engl. J. Med. 359, 1429-1441
9. Nardese, V., Longhi, R., Polo, S., Sironi, F., Arcelloni, C., Paroni, R., DeSantis, C., Sarmientos, P., Rizzi, M., Bolognesi, M., Pavone, V., and Lusso, P. (2001) Structural determinants of CCR5 recognition and HIV-1 blockade in RANTES. Nat. Struct. Biol. 8, 611-615 (Pubitemid 32613010)
10. Vangelista, L., Longhi, R., Sironi, F., Pavone, V., and Lusso, P. (2006) Critical role of the N-loop and β1-strand hydrophobic clusters of RANTES-derived peptides in anti-HIV activity. Biochem. Biophys. Res. Commun. 351, 664-668 (Pubitemid 44708859)
11. Skelton, N. J., Aspiras, F., Ogez, J., and Schall, T. J. (1995) Proton NMR assignments and solution conformation of RANTES, a chemokine of the C-C type. Biochemistry 34, 5329-5342
12. Chung, C., Cooke, R. M., Proudfoot, A. E., and Wells, T. N. C. (1995) The three-dimensional solution structure of RANTES. Biochemistry 34, 9307-9314
13. Wilken, J., Hoover, D., Thompson, D. A., Barlow, P. N., McSparron, H., Picard, L., Wlodawer, A., Lubkowski, J., and Kent, S. B. (1999) Total chemical synthesis and high-resolution crystal structure of the potent anti-HIV protein AOP-RANTES. Chem. Biol. 6, 43-51 (Pubitemid 29363044)
14. Shaw, J. P., Johnson, Z., Borlat, F., Zwahlen, C, Kungl, A., Roulin, K, Harrenga, A., Wells, T. N., and Proudfoot, A. E. (2004) The X-ray structure of RANTES: heparin-derived disaccharides allows the rational design of chemokine inhibitors. Structure 12, 2081-2093 (Pubitemid 39469405)
15. Nussbaum, O., Broder, C. C, and Berger, E. A. (1994) Fusogenic mechanisms of enveloped-virus glycoproteins analyzed by a novel recombinant vaccinia virus-based assay quantitating cell fusion-dependent reporter gene activation. J. Virol. 68, 5411-5422 (Pubitemid 24258553)
16. + T-cell clone (PM1): failure to downregulate CD4 and to interfere with cell-line-tropic HIV-1. J. Virol. 69, 3712-3720
17. Bax, A. D., and Davis. D. G. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Res. 65, 355-360
18. Jeener, J., Meier, B. H., Bachmann, P., and Ernst, R. R. (1979) Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71, 4546-4553
19. Kumar, A., Wagner, G., Ernst, R. R., and Wuthrich, K (1981) Buildup rates of the nuclear Overhauser effect measured by two-dimensional proton magnetic resonance spectroscopy implications for studies of protein conformation. J. Am. Chem. Soc. 103, 3654-3658
20. Griesinger, C., and Ernst, R. R. (1978) Frequency offset effects and their elimination in NMR rotating-frame cross-relaxation spectroscopy. Ø Magn. Res. 75, 261-271
21. Piantini, U., Srensen, O. W., and Ernst, R. R. (1982) Multiple quantum filters for elucidating NMR coupling networks. J. Am. Chem. Soc. 104, 6800-6801
22. Wuthrich, K NMR of Proteins and Nucleic Acids. (1986) Wiley, New York
23. Marion, D., and Wuthrich, K (1983) Application of phase sensitive correlated spectroscopy (COSY) for measurements of proton-proton spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 113, 967-974
24. Hwang, T. L., and Shaka, A. J. (1995) Water suppression that works. Excitation Sculpting using arbitrary wave-forms and pulsed-field gradients. J. Magn. Reson. Ser. A 112, 275-279
25. Keller, R. (2004) The Computer Aided Resonance Assignment Tutorial, ISBN 3-85600-112-3. CANTINA Verlag (available from: www.nmr.ch).
26. Güntert, P., Braun, W., and Wüthrich, K. (1991) Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J. Mol. Biol. 217, 517-530 (Pubitemid 121003298)
27. Güntert, P., Mumenthaler, C., and Wuthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273, 283-298 (Pubitemid 27460230)
28. Weiner, S. J., Kollman, P. A., Case, D. A., Chandra Singh, U., Ghio, C., Alagona, G., Profeta, S., and Weiner, P. (1984) A new force field for molecular mechanical simulation of nucleic acids and proteins. J. Am. Chem. Soc. 106, 765-784 (Pubitemid 14548426)
29. Weiner, S. J., Kollman, P. A., Nguyen, D. T., and Case, D. A. (1986) An all atom force field for simulations of proteins and nucleic acids. J. Comput. Chem. 7, 230-252
30. Simons, K. T., Bonneau, R., Ruczinski, I., and Baker, D. (1999) Ab initio protein structure prediction of CASP III targets using ROSETTA. Proteins Suppl. 3, 171-176 (Pubitemid 29463528)
31. Rohl, C. A., Strauss, C. E. M., Misura, K. M. S., and Baker, D. (2004) Protein structure prediction using Rosetta. Methods Enzymol. 383, 66-93 (Pubitemid 38401787)
32. McCammon, J. A., Gelin, B. R., and Karplus, M. (1977) Dynamics of folded proteins. Nature 267, 585-590
33. Metropolis, N., and Ulam, S. (1949) The Monte Carlo method. J. Am. Stat. Assoc. 44, 335-341
34. Bradley, P., Malmström, L., Qian, B., Schonbrun, J., Chivian, D., Kim, D. E., Meiler, J., Misura, K. M., and Baker, D. (2005) Free modeling with Rosetta in CASP6. Proteins 61 (Suppl. 7), 128-134 (Pubitemid 43069966)
35. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., 3rd, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
36. Wilmot, C. M., and Thornton, J. M. (1990) Beta-turns and their distortions: a proposed new nomenclature. Protein Eng. 3, 479-493 (Pubitemid 20290024)
37. Pavone, V., Gaeta, G., Lombardi, A., Nastri, F., Maglio, O., Isernia, C., and Saviano, M. (1996) Discovering protein secondary structures: classification and description of isolated alphaturns. Biopolymers 38, 705-721
38. Rek, A., Brandner, B., Geretti, E., and Kungl, A. J. (2009) A biophysical insight into the RANTES-glycosaminoglycan interaction. Biochem. Biophys. Acta 1794, 577-582
39. Cooper, D. A., and Lange, J. M. (2004) Peptide inhibitors of virus-cell fusion: enfuvirtide as a case study in clinical discovery and development. Lancet Infect. Dis. 4, 426-436 (Pubitemid 38844127)
40. He, Y., Xiao, Y., Song, H., Liang, Q., Ju, D., Chen, X., Lu, H., Jing, W., Jiang, S., and Zhang, L. (2008) Design and evaluation of sifuvirtide, a novel HIV-1 fusion inhibitor. J. Biol. Chem. 283, 11126-11134