Easily accessible polycyclic amines that inhibit the wild-type and amantadine-resistant mutants of the M2 channel of influenza A virus

Journal of Medicinal Chemistry

Volumn 57, Issue 13, 2014, Pages 5738-5747

  Rey Carrizo, Matias ^a   Barniol Xicota, Marta ^a   Ma, Chunlong ^b   Frigolé Vivas, Marta ^a   Torres, Eva ^a   Naesens, Lieve ^d   Llabrés, Salomé ^a   Juárez Jiménez, Jordi ^a   Luque, Francisco J ^a   Degrado, William F ^c   Lamb, Robert A ^b   Pinto, Lawrence H ^b   Vázquez, Santiago ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMANTADINE; AMANTADINE DERIVATIVE; AMINE; ASPARAGINE; ION CHANNEL; LEUCINE; PHENYLALANINE; PROTEIN M2; PYRROLIDINE DERIVATIVE; RIMANTADINE; SERINE; VALINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; ARTICLE; CONTROLLED STUDY; DRUG INHIBITION; DRUG SYNTHESIS; ELECTRODE; IC 50; INFLUENZA VIRUS A; MOLECULAR MODEL; NONHUMAN; OOCYTE; VIRUS STRAIN; VOLTAGE CLAMP TECHNIQUE; WILD TYPE; XENOPUS;

AMANTADINE; AMINES; ANIMALS; DOGS; DRUG RESISTANCE, VIRAL; INFLUENZA A VIRUS; ION CHANNELS; MADIN DARBY CANINE KIDNEY CELLS; MODELS, MOLECULAR; MUTATION; ORTHOMYXOVIRIDAE INFECTIONS; PATCH-CLAMP TECHNIQUES; PYRROLIDINES; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL MATRIX PROTEINS; XENOPUS;

EID: 84904338014     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm5005804     Document Type: Article

References (41)

1. Bright, R. A.; Shay, D. K.; Shu, B.; Cox, N. J.; Klimov, A. I. Adamantane resistance among influenza A viruses isolated early during the 2005-2006 influenza season in the United States JAMA, J. Am. Med. Assoc. 2006, 295, 891-894
2. Fiore, A. E.; Shay, D. K.; Haber, P.; Iskander, J. K.; Uyeki, T. M.; Mootrey, G.; Bresee, J. S.; Cox, N. J. Prevention and control of influenza. Recommendations of the Advisory Committee on Immunization Practices (ACIP), 2007 MMWR Recomm. Rep. 2007, 56, 1-54
3. Lamb, R. A.; Zebedee, S. L.; Richardson, C. D. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface Cell 1985, 40, 627-633 (Pubitemid 15076578)
4. Hong, M.; DeGrado, W. F. Structural basis for proton conduction and inhibition by the influenza M2 protein Protein Sci. 2012, 21, 1620-1633
5. Wang, J.; Qiu, J. X.; Soto, C. S.; DeGrado, W. F. Structural and dynamic mechanisms for the function and inhibition of the M2 proton cannel from influenza A virus Curr. Opin. Struct. Biol. 2011, 21, 68-80
6. Balannik, V.; Carnevale, V.; Fiorin, G.; Levine, B. G.; Lamb, R. A.; Klein, M. L.; DeGrado, W. F.; Pinto, L. H. Functional studies and modeling of pore-lining residue mutants of the influenza a virus M2 ion channel Biochemistry 2010, 49, 696-708
7. Furuse, Y.; Suzuki, A.; Oshitani, H. Large-scale sequence analysis of M gene of influenza A viruses from different species: mechanisms for emergence and spread of amantadine resistance Antimicrob. Agents Chemother. 2009, 53, 4457-4463
8. Balannik, V.; Wang, J.; Ohigashi, Y.; Jing, X.; Magavern, E.; Lamb, R. A.; DeGrado, W. F.; Pinto, L. H. Design and pharmacological characterization of inhibitors of amantadine-resistant mutants of the M2 ion channel of influenza A virus Biochemistry 2009, 48, 11872-11882
9. Wang, J.; Ma, C.; Fiorin, G.; Carnevale, V.; Wang, T.; Hu, F.; Lamb, R. A.; Pinto, L. H.; Hong, M.; Klein, M. L.; DeGrado, W. F. Molecular dynamics simulation directed rational design of inhibitors targeting drug-resistant mutants of influenza A virus M2 J. Am. Chem. Soc. 2011, 133, 12834-12841
10. Wang, J.; Ma, C.; Wu, Y.; Lamb, R. A.; Pinto, L. H.; DeGrado, W. F. Exploring organosilane amines as potent inhibitors and structural probes of influenza A virus M2 proton channel J. Am. Chem. Soc. 2011, 133, 13844-13847
11. 1,5]undecane derivatives: from wild-type inhibitors of the M2 ion channel of influenza A virus to derivatives with potent activity against the V27A mutant J. Med. Chem. 2013, 56, 9265-9274
12. Camps, P.; Duque, M. D.; Vázquez, S.; Naesens, L.; De Clercq, E.; Sureda, F. S.; López-Querol, M.; Camins, A.; Pallàs, M.; Prathalingam, S. R.; Kelly, J. M.; Romero, V.; Ivorra, D.; Cortés, D. Synthesis and pharmacological evaluation of several ring-contracted amantadine analogs Bioorg. Med. Chem. 2008, 16, 9925-9936
13. Duque, M. D.; Ma, C.; Torres, E.; Wang, J.; Naesens, L.; Juárez-Jiménez, J.; Camps, P.; Luque, F. J.; DeGrado, W. F.; Lamb, R. A.; Pinto, L. H.; Vázquez, S. Exploring the size limit of templates for inhibitors of the M2 ion channel of influenza A virus J. Med. Chem. 2011, 54, 2646-2657
14. Torres, E.; Vanderlinden, E.; Fernández, R.; Miquet, S.; Font-Bardia, M.; Naesens, L.; Vázquez, S. Synthesis and anti-influenza activity of 2,2-dialkylamantadines and related compounds ACS Med. Chem. Lett. 2012, 3, 1065-1069
15. Torres, E.; Duque, M. D.; Vanderlinden, E.; Ma, C.; Pinto, L. H.; Camps, P.; Froeyen, M.; Vázquez, S.; Naesens, L. Role of the viral hemagglutinin in the anti-influenza virus activity of newly synthesized polycyclic amine compounds Antiviral Res. 2013, 99, 281-291
16. 1A receptor ligands and potential anxiolytic agents: synthesis and structure-activity relationship studies J. Med. Chem. 1988, 31, 1382-1392
17. Pielak, R. M.; Chou, J. J. Solution NMR structure of the V27A drug resistant mutant of influenza A M2 channel Biochem. Biophys. Res. Commun. 2010, 401, 58-63
18. Gu, R.-X.; Liu, L. A.; Wang, Y.-H.; Xu, Q.; Wei, D. Q. Structural comparison of the wild-type and drug-resistant mutants of the influenza A M2 proton channel by molecular dynamics simulations J. Phys. Chem. B 2013, 117, 6042-6051
19. Gu, R.-X.; Liu, L. A.; Wang, Y.-H.; Wei, D.-Q. Structural and energetic analysis of drug inhibition of the influenza A M2 proton channel Trends Pharmacol. Sci. 2013, 34, 571-580
20. Mousseron-Canet, M.; Mousseron, M.; Brown, G. Rev. Chim., Acad. Rep. Populaire Roumaine 1962, 7, 1089-1101
21. s intramolecular cycloaddition Chem. Commun. 1970, 94-95
22. Wang, J.; Wu, Y.; Ma, C.; Fiorin, G.; Wang, J.; Pinto, L. H.; Lamb, R. A.; Klein, M. L.; DeGrado, W. F. Structure and Inhibition of the Drug-Resistant S31N Mutant of the M2 Ion Channel of Influenza A Virus Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 1315-1320
23. Cady, S. D.; Schmidt-Rohr, K.; Wang, J.; Soto, C. S.; DeGrado, W. F.; Hong, M. Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers Nature 2010, 463, 689-692
24. Kolocouris, A.; Tzitzoglaki, C.; Johnson, F. B.; Zell, R.; Wright, A. K.; Cross, T. A.; Tietjen, I.; Fedida, D.; Busath, D. D. Aminoadamantanes with persistent in vitro efficacy against H1N1 (2009) influenza A J. Med. Chem. 2014, 57, 4629-4639
25. Stevaert, A.; Dallocchio, R.; Dessì, A.; Pala, N.; Rogolino, D.; Sechi, M.; Naesens, L. Mutational analysis of the binding pockets of the diketo acid inhibitor L-742,001 in the influenza virus PA endonuclease J. Virol. 2013, 87, 10524-10538
26. Ma, C.; Soto, C. S.; Ohigashi, Y.; Taylor, A.; Bournas, V.; Glawe, B.; Udo, M. K.; DeGrado, W. F.; Lamb, R. A.; Pinto, L. H. Identification of the pore-lining residues of the BM2 ion channel protein of influenza B virus J. Biol. Chem. 2008, 283, 15921-15931
27. Vanderlinden, E.; Göktas, F.; Cesur, Z.; Froeyen, M.; Reed, M. L.; Russell, C. J.; Cesur, N.; Naesens, L. Novel inhibitors of influenza virus fusion: structure-activity relationship and interaction with the viral hemagglutinin J. Virol. 2010, 84, 4277-4288
28. Sharma, M.; Yi, M.; Dong, H.; Qin, H.; Peterson, E.; Busath, D. D.; Zhou, H. X.; Cross, T. A. Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer Science 2010, 330, 509-512
29. Lomize, M. A.; Lomize, A. L.; Pogozheva, I. D.; Mosberg, H. I. OPM: Orientations of Proteins in Membranes Database Bioinformatics 2006, 22, 623-625 (Pubitemid 43372827)
30. Acharya, R.; Carnevale, V.; Florin, G.; Levine, B. G.; Polishchuk, A. L.; Balannik, V.; Samish, I.; Lamb, R. A.; Pinto, L. H.; DeGrado, W. F.; Klein, M. L. Structure and mechanism of proton transport through the transmembrane tetrameric M2 protein bundle of the influenza A virus Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 15075-15080
31. Jo, S.; Kim, T.; Iyer, V. G.; Im, W. CHARMM-GUI: A Web-based Graphical User Interface for CHARMM J. Comput. Chem. 2008, 29, 1859-1865
32. Jo, S.; Lim, J. B.; Klauda, J. B.; Im, W. CHARMM-GUI Membrane Builder for Mixed Bilayers and Its Application to Yeast Membranes Biophys. J. 2009, 97, 50-58
33. Jo, S.; Kim, T.; Im, W. Automated Builder and Database of Protein/Membrane Complexes for Molecular Dynamics Simulations PLoS One 2007, 2, e880
34. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 1983, 79, 926-935
35. Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of multiple Amber force fields and development of improved protein backbone parameters Proteins 2006, 65, 712-725 (Pubitemid 44583220)
36. Wang, J. M.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and testing of a general amber force field J. Comput. Chem. 2005, 26, 1157-1174
37. Bayly, C. I.; Cieplak, P.; Cornell, W.; Kollman, P. A. A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model J. Phys. Chem. 1993, 97, 10269-10280
38. Case, D. A.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Walker, R. C.; Zhang, W.; Merz, K. M.; Roberts, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Swails, J.; Goetz, A. W.; Kolossváry, I.; Wong, K. F.; Paesani, F.; Vanicek, J.; Wolf, R. M.; Liu, J.; Wu, X.; Brozell, S. R.; Steinbrecher, T.; Gohlke, H.; Cai, Q.; Ye, X.; Wang, J.; Hsieh, M.-J.; Cui, G.; Roe, D. R.; Mathews, D. H.; Seetin, M. G.; Salomon- Ferrer, R.; Sagui, C.; Babin, V.; Luchko, T.; Gusarov, S.; Kovalenko, A.; Kollman, P. A. AMBER 12; University of California: San Francisco, 2012.
39. Callum, J. D.; Rosso, L.; Betz, R. M.; Walker, R. C.; Gould, I. R. GAFFlipid: a General Amber Force Field for the accurate molecular dynamics simulation of phospholipid Soft Matter 2012, 8, 9617-9627
40. Joung, I. S.; Cheatham, T. E. Molecular dynamics simulations of the dynamic and energetic properties of alkali and halide ions using wáter-model-specific ion parameters J. Phys. Chem. B 2009, 113, 13279-13290
41. Salomon-Ferrer, R.; Goetz, A. W.; Poole, D.; Le Grand, S.; Walker, R. C. Routine microsecond molecular dynamics simulations with AMBER on GPUs. 2. Explicit solvent Particle Mesh Ewald J. Chem. Theory Comput. 2013, 9, 3878-3888