Metal-chelating 2-hydroxyphenyl amide pharmacophore for inhibition of influenza virus endonuclease

Molecular Pharmaceutics

Volumn 11, Issue 1, 2014, Pages 304-316

  Carcelli, Mauro ^a   Rogolino, Dominga ^a   Bacchi, Alessia ^a   Rispoli, Gabriele ^a   Fisicaro, Emilia ^a   Compari, Carlotta ^a   Sechi, Mario ^b   Stevaert, Annelies ^c   Naesens, Lieve ^c  

^a UNIVERSITY OF PARMA   (Italy)

^b UNIVERSITY OF SASSARI   (Italy)

^c REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

antiviral; influenza virus endonuclease; magnesium complexes; metal chelation; metalloenzymes

Indexed keywords

ANTIVIRUS AGENT; BENZAMIDE DERIVATIVE; CHELATING AGENT; ENDONUCLEASE; ENZYME INHIBITOR; ESSENTIAL AMINO ACID; LIGAND; MAGNESIUM DERIVATIVE; N (4 FLUOROBENZYL) 2 HYDROXYBENZAMIDE; N (4 FLUOROBENZYL) 2 METHOXYBENZAMIDE; N (4 FLUOROBENZYL) 2,3 DIHYDROXYBENZAMIDE; N (4 FLUOROBENZYL) 2,3 DIMETHOXYBENZAMIDE; N1,N3 BIS(4 FLUOROBENZYL) 2 HYDROXYISOPHTHALAMIDE; N1,N3 BIS(4 FLUOROBENZYL) 2 METHOXYISOPHTHALAMIDE; UNCLASSIFIED DRUG; VIRUS ENZYME;

ARTICLE; ATOM; CHELATION; CHEMICAL STRUCTURE; CRYSTAL STRUCTURE; DRUG SYNTHESIS; ENZYMATIC ASSAY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; HYDROGEN BOND; IC 50; INFLUENZA VIRUS; IONIC STRENGTH; MOLECULAR DOCKING; MOLECULAR MODEL; PHARMACOPHORE; POTENTIOMETRY; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SOLID STATE; STOICHIOMETRY; X RAY DIFFRACTION;

BENZAMIDES; CATALYTIC DOMAIN; CHELATING AGENTS; COORDINATION COMPLEXES; CRYSTALLOGRAPHY, X-RAY; MAGNESIUM; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; RECOMBINANT PROTEINS; RNA REPLICASE; VIRAL PROTEINS; X-RAY DIFFRACTION;

EID: 84891806570     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp400482a     Document Type: Article

References (50)

1. Reid, A. H.; Taubenberger, J. K.; Fanning, T. G. The 1918 Spanish influenza: integrating history and biology Microbes Infect. 2001, 3, 81-87
2. Smith, G. J. D.; Vijaykrishna, D.; Bahl, J.; Lycett, S. J.; Worobey, M.; Pybus, O. G.; Ma, S. K.; Cheung, C. L.; Raghwani, J.; Bhatt, S.; Peiris, J. S. M.; Guan, Y.; Rambaut, A. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic Nature 2009, 459, 1122-1125
3. Chowell, G.; Bertozzi, S. M.; Colchero, M. A.; Lopez-Gatell, H.; Alpuche-Aranda, C.; Hernandez, M.; Miller, M. A severe respiratory disease concurrent with the circulation of H1N1 influenza N. Engl. J. Med. 2009, 361, 674-679
4. Garten, R. J.; Davis, C. T.; Russell, C. A; Shu, B.; Lindstrom, S.; Balish, A.; Sessions, W. M.; Xu, X.; Skepner, E.; Deyde, V.; Okomo-Adhiambo, M.; Gubareva, L.; Barnes, J.; Smith, C. B.; Emery, S. L.; Hillman, M. J.; Rivailler, P.; Smagala, J.; De Graaf, M.; Burke, D. F.; Fouchier, R. A. M.; Pappas, C.; Alpuche-Aranda, C. M.; López-Gatell, H.; Olivera, H.; López, I.; Myers, C. A.; Faix, D.; Blair, P. J.; Yu, C.; Keene, K. M.; Dotson, P. D.; Boxrud, D.; Sambol, A. R.; Abid, S. H.; St George, K.; Bannerman, T.; Moore, A. L.; Stringer, D. J.; Blevins, P.; Demmler-Harrison, G. J.; Ginsberg, M.; Kriner, P.; Waterman, S.; Smole, S.; Guevara, H. F.; Belongia, E. A.; Clark, P. A.; Beatrice, S. T.; Donis, R.; Katz, J.; Finelli, L.; Bridges, C. B.; Shaw, M.; Jernigan, D. B.; Uyeki, T. M.; Smith, D. J.; Klimov, A. I.; Cox, N. J. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans Science 2009, 325, 197-201
5. Gao, R.; Cao, B.; Hu, Y.; Feng, Z.; Wang, D.; Hu, W.; Chen, J.; Jie, Z.; Qiu, H.; Xu, K.; Xu, X.; Lu, H.; Zhu, W.; Gao, Z.; Xiang, N.; Shen, Y.; He, Z.; Gu, Y.; Zhang, Z.; Yang, Y.; Zhao, X.; Zhou, L.; Li, X.; Zou, S.; Zhang, Y.; Li, X.; Yang, L.; Guo, J.; Dong, J.; Li, Q.; Dong, L.; Zhu, Y.; Bai, T.; Wang, S.; Hao, P.; Yang, W.; Zhang, Y.; Han, J.; Yu, H.; Li, D.; Gao, G. F.; Wu, G.; Wang, Y.; Yuan, Z.; Shu, Y. Human infection with a novel avian-origin influenza A (H7N9) virus N. Engl. J. Med. 2013, 368, 1888-1897
6. Krug, R. M.; Aramini, J. M. Emerging antiviral targets for influenza A virus Trends Phramacol. Sci. 2009, 30, 269-277
7. Du, J.; Cross, T. A.; Zhou, H.-X. Recent progress in structure-based anti-influenza drug design Drug Discovery Today 2012, 17, 1111-1120
8. Reece, P. A. Neuraminidase inhibitor resistance in influenza viruses J. Med. Virol. 2007, 1586, 1577-1586
9. Collins, P. J.; Haire, L. F.; Lin, Y. P.; Liu, J.; Russell, R. J.; Walker, P. A.; Skehel, J. J.; Martin, S. R.; Hay, A. J.; Gamblin, S. J. Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants Nature 2008, 453, 1258-1261
10. Honda, A.; Ishiama, A. Biol. Chem. 1997, 378, 483-488
11. Honda, A.; Mizumoto, K.; Ishihama, A. Minimum molecular architectures for transcription Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 1-6
12. Plotch, S. J.; Bouloy, M.; Ulmanen, I.; Krug, R. M. Cell 1981, 23, 847-858
13. Dias, A.; Bouvier, D.; Crépin, T.; McCarthy, A.; Hart, D. J.; Baudin, F.; Cusack, S.; Ruigrok, R. W. H. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit Nature 2009, 458, 914-918
14. Yuan, P.; Bartlam, M.; Lou, Z.; Chen, S.; Zhou, J.; He, X.; Lv, Z.; Ge, R.; Li, X.; Deng, T.; Fodor, E.; Rao, Z.; Liu, Y. Crystal structure of an avian influenza polymerase PA N reveals an endonuclease active site Nature 2009, 458, 909-913
15. Crépin, T.; Dias, A.; Palencia, A.; Swale, C.; Cusack, S.; Ruigrok, R. W. H. Mutational and metal binding analysis of the endonuclease domain of the influenza virus polymerase PA subunit J. Virol. 2010, 84, 9096-9104
16. Steitz, T.; Steitz, J. A general two-metal-ion mechanism for catalytic RNA Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 6498-6502
17. Doan, L.; Handa, B.; Roberts, N.; Klumpp, K. Metal ion catalysis of RNA cleavage by the influenza virus endonuclease Biochemistry 1999, 38, 5612-9
18. Rogolino, D.; Carcelli, M.; Sechi, M.; Neamati, N. Viral enzymes containing magnesium: metal binding as a successful strategy in drug design Coord. Chem. Rev. 2012, 256, 3063-3086
19. Kirschberg, T.; Parrish, J. Metal chelators as antiviral agents Curr. Opin. Drug Discovery Dev. 2007, 10, 460-472
20. Liao, C.; Marchand, C.; Burke, T. R., Jr; Pommier, Y.; Nicklaus, M. C. NIH Public Access Future Med. Chem. 2010, 2, 1107-1122
21. Tomassini, J.; Selnick, H.; Davies, M. E.; Armstrong, M. E.; Baldwin, J.; Bourgeois, M.; Hastings, J.; Hazuda, D.; Lewis, J.; Mcclements, W.; Ponticello, G.; Radzilowski, E.; Smith, G.; Tebben, A.; Wolfe, A. Inhibition of cap (m7GpppXm)-dependent endonuclease of influenza virus by 4-substituted 2,4-dioxobutanoic acid compounds Antimicrob. Agents Chemother. 1994, 38, 2827-2837
22. Hastings, J. C.; Selnick, H.; Wolanski, B.; Tomassini, J. E. Anti-influenza virus activities of 4-substituted 2,4-dioxobutanoic acid inhibitors Antimicrob. Agents Chemother. 1996, 40, 1304-1307
23. Tomassini, J. E.; Davies, M. E.; Hastings, J. C.; Lingham, R.; Mojena, M.; Raghoobar, S. L.; Singh, S. B.; Tkacz, J. S.; Goetz, M. A novel antiviral agent which inhibits the endonuclease of influenza viruses Antimicrob. Agents Chemother. 1996, 40, 1189-1193
24. Hensens, O. D.; Goetz, M. A.; Liesch, J. M.; Zink, D. L.; Raghoobar, S. L.; Helms, G. L.; Singh, S. B. Isolation and structure of Flutimide, a novel endonuclease inhibitor of influenza virus Tetrahedron Lett. 1995, 36, 2005-2008
25. Cianci, C.; Chung, T. D. Y.; Meanwell, N.; Putz, H.; Hagen, M.; Colonno, R. J.; Krystal, M. Identification of N -hydroxamic acid and N -hydroxyimide compounds that inhibit the influenza virus polymerase Antiviral Chem. Chemother. 1996, 7, 353-360
26. Parkes, K. E.; Ermert, P.; Fässler, J.; Ives, J.; Martin, J. A.; Merrett, J. H.; Obrecht, D.; Williams, G.; Klumpp, K. Use of a pharmacophore model to discover a new class of influenza endonuclease inhibitors J. Med. Chem. 2003, 1153-1164
27. Iwai, Y.; Murakami, K.; Gomi, Y.; Hashimoto, T.; Asakawa, Y. Anti-influenza activity of marchantins, macrocyclic bisbibenzyls contained in liverworts PLoS One 2011, 6, e19825
28. Kuzuhara, T.; Iwai, Y.; Takahashi, H.; Hatakeyama, D.; Echigo, N.; Bunri, T. Green tea catechins inhibit the endonuclease activity of influenza A virus RNA polymerase PLoS One Currents 2012, 1-8
29. Song, J.-M.; Lee, K.-H.; Seong, B.-L. Antiviral effect of catechins in green tea on influenza virus Antiviral Res. 2005, 68, 66-74
30. Agrawal, A.; DeSoto, J.; Fullagar, J. L.; Maddali, K.; Rostami, S.; Richman, D. D.; Pommier, Y.; Cohen, S. M. Probing chelation motifs in HIV integrase inhibitors Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 2251-2256
31. Dubois, R. M.; Slavish, P. J.; Baughman, B. M.; Yun, M.; Bao, J.; Webby, R. J.; Webb, T. R.; White, S. W. Structural and biochemical basis for development of influenza virus inhibitors targeting the PA endonuclease PLoS Pathogens 2012, 8 (8) e1002830
32. Kowalinski, E.; Zubieta, C.; Wolkerstorfer, A.; Szolar, O. H. J.; Ruigrok, R. W. H.; Cusack, S. Structural analysis of specific metal chelating inhibitor binding to the endonuclease domain of influenza pH1N1 (2009) Polymerase PLoS Pathogens 2012, 8 (8) e1002831
33. Fan, X.; Zhang, F.-H.; Al-Safi, R. I.; Zeng, L.-F.; Shabaik, Y.; Debnath, B.; Sanchez, T. W.; Odde, S.; Neamati, N.; Long, Y.-Q. Design of HIV-1 integrase inhibitors targeting the catalytic domain as well as its interaction with LEDGF/p75: a scaffold hopping approach using salicylate and catechol groups Bioorg. Med. Chem. 2011, 19, 4935-4952
34. SAINT: SAX, Area Detector Integration. Siemens Analytical instruments, Inc.: Madison, WI.
35. SADABS: Area-Detector Absorption Correction. Siemens Industrial Automation, Inc.: Madison, WI, 1996.
36. Burla, M. C.; Caliandro, R.; Camalli, M.; Carrozzini, B.; Cascarano, G. L.; De Caro, L.; Giacovazzo, C.; Polidori, G.; Spagna, R. SIR2004: an improved tool for crystal structure determination and refinement J. Appl. Crystallogr. 2005, 38, 381-388
37. SHELXL97; Sheldrick, G. M. Acta Crystallogr. 2008, A64, 112
38. Allen, F. H. The Cambridge Structural Database: a quarter of a million crystal structures and rising Acta Crystallogr. 2002, B58, 380-388
39. Dolomanov, O. V.; Bourhis, L. J.; Gildea, R. J.; Howard, J. A. K.; Puschmann, H. OLEX2: a complete structure solution, refinement and analysis program J. Appl. Crystallogr. 2009, 42, 339-341
40. Fisicaro, E.; Braibanti, A. Talanta 1988, 10, 769
41. Gran, G. Analyst 1952, 77, 661
42. Gans, P.; Sabatini, A.; Vacca, A. Talanta 1996, 43, 1739
43. Molecular Operating Environment (MOE 2010.11). Chemical Computing Group, Inc.: Montreal, Quebec, Canada.
44. Feher, M.; Williams, C. I. J. Chem. Infect. Model 2009, 49, 1704
45. Zhang, Q. X.; Zhang, B. Acta Crystallogr. 2008, E 64, o884
46. Sechi, M.; Bacchi, A.; Carcelli, M.; Compari, C.; Duce, E.; Fisicaro, E.; Rogolino, D.; Gates, P.; Derudas, M.; Al-Mawsawi, L. Q.; Neamati, N. From ligand to complexes: Inhibition of human immunodeficiency virus type 1 integrase by β-diketo acid metal complexes J. Med. Chem. 2006, 49, 4248-4260
47. Cowan, J. Metal activation of enzymes in nucleic acid biochemistry Chem. Rev. 1998, 98, 1067-1088
48. Dudev, T.; Cowan, J.; Lim, C. Competitive binding in magnesium coordination chemistry: water versus ligands of biological interest J. Am. Chem. Soc. 1999, 121, 7665-7673
49. Cowan, J. Structural and catalytic chemistry of magnesium-dependent enzymes Biometals: an international journal on the role of metal ions in biology, biochemistry, and medicine 2002, 15, 225-235
50. Noble, E.; Cox, A.; Deval, J.; Kim, B. Endonuclease substrate selectivity characterized with full-length PA of influenza A virus polymerase Virology 2012, 433, 27-34