A Potent Anti-influenza Compound Blocks Fusion through Stabilization of the Prefusion Conformation of the Hemagglutinin Protein

ACS Infectious Diseases

Volumn 1, Issue 2, 2016, Pages 98-109

  White, Kris M ^a   De Jesus, Paul ^b   Chen, Zhong ^c   Abreu, Pablo ^a   Barile, Elisa ^b   Mak, Puiying A ^c   Anderson, Paul ^c   Nguyen, Quy T ^b   Inoue, Atsushi ^b   Stertz, Silke ^a,d   Koenig, Renate ^b,e   Pellecchia, Maurizio ^b   Palese, Peter ^a   Kuhen, Kelli ^c   García Sastre, Adolfo ^a   Chanda, Sumit K ^b   Shaw, Megan L ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b BURNHAM INSTITUTE   (United States)

^c GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e PAUL EHRLICH INSTITUT   (Germany)

Author keywords

antiviral; docking; fusion; hemagglutinin; influenza; screen

Indexed keywords

ANTIVIRUS AGENT; HEMAGGLUTININ; S 20; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; AVIAN INFLUENZA (H5N1); BINDING SITE; CC50; COMPUTER MODEL; CONTROLLED STUDY; CORRELATIONAL STUDY; DRUG CONFORMATION; DRUG MECHANISM; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IC50; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H5N1); MEMBRANE FUSION; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; SELECTIVITY INDEX; VIRUS INFECTION;

EID: 84964385320     PISSN: None     EISSN: 23738227     Source Type: Journal    
DOI: 10.1021/id500022h     Document Type: Article

References (49)

1. Wang, T. T. and Palese, P. (2009) Unraveling the mystery of swine influenza virus Cell 137, 983-985 10.1016/j.cell.2009.05.032
2. Smith, G. J., 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., Guan, Y., and Rambaut, A. (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic Nature 459, 1122-1125 10.1038/nature08182
3. Tang, J. W., Shetty, N., and Lam, T. T. (2010) Features of the new pandemic influenza A/H1N1/2009 virus: virology, epidemiology, clinical and public health aspects Curr. Opin Pulm. Med. 16, 235-241 10.1097/MCP.0b013e3283375727
4. Morens, D. M., Taubenberger, J. K., Harvey, H. A., and Memoli, M. J. (2010) The 1918 influenza pandemic: lessons for 2009 and the future Crit. Care Med. 38, e10-20 10.1097/CCM.0b013e3181ceb25b
5. Hamilton, B. S., Whittaker, G. R., and Daniel, S. (2012) Influenza virus-mediated membrane fusion: determinants of hemagglutinin fusogenic activity and experimental approaches for assessing virus fusion Viruses 4, 1144-1168 10.3390/v4071144
6. Fineberg, H. V. (2014) Pandemic preparedness and response-lessons from the H1N1 influenza of 2009 N. Engl. J. Med. 370, 1335-1342 10.1056/NEJMra1208802
7. Pizzorno, A., Abed, Y., and Boivin, G. (2011) Influenza drug resistance Semin. Respir. Crit. Care Med. 32, 409-422 10.1055/s-0031-1283281
8. Takashita, E., Ejima, M., Itoh, R., Miura, M., Ohnishi, A., Nishimura, H., Odagiri, T., and Tashiro, M. (2014) A community cluster of influenza A(H1N1)pdm09 virus exhibiting cross-resistance to oseltamivir and peramivir in Japan, November to December 2013 Eurosurveillance 19, article 2, http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20666.
9. Yang, J. R., Huang, Y. P., Chang, F. Y., Hsu, L. C., Huang, H. Y., Pan, Y. T., Lin, Y. C., Wu, H. S., and Liu, M. T. (2013) Characterization of oseltamivir-resistant influenza A(H1N1)pdm09 viruses in Taiwan in 2009-2011 J. Med. Virol. 85, 379-387 10.1002/jmv.23482
10. Wang, B., Taylor, J., Ratnamohan, M., McPhie, K., Kesson, A., Dixit, R., Booy, R., Hurt, A., Saksena, N., and Dwyer, D. E. (2012) Frequency of oseltamivir resistance in Sydney, during the Newcastle outbreak of community transmitted oseltamivir-resistant influenza A(H1N1)pdm09 virus, Australia, June to August 2011. Eurosurveillance 17, article 4, http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20210.
11. Renaud, C., Kuypers, J., and Englund, J. A. (2011) Emerging oseltamivir resistance in seasonal and pandemic influenza A/H1N1 J. Clin. Virol. 52, 70-78 10.1016/j.jcv.2011.05.019
12. Hurt, A. C., Hardie, K., Wilson, N. J., Deng, Y. M., Osbourn, M., Leang, S. K., Lee, R. T., Iannello, P., Gehrig, N., Shaw, R., Wark, P., Caldwell, N., Givney, R. C., Xue, L., Maurer-Stroh, S., Dwyer, D. E., Wang, B., Smith, D. W., Levy, A., Booy, R., Dixit, R., Merritt, T., Kelso, A., Dalton, C., Durrheim, D., and Barr, I. G. (2012) Characteristics of a widespread community cluster of H275Y oseltamivir-resistant A(H1N1)pdm09 influenza in Australia J. Infect. Dis. 206, 148-157 10.1093/infdis/jis337
13. Carr, A. and Amin, J. (2009) Efficacy and tolerability of initial antiretroviral therapy: a systematic review AIDS 23, 343-353 (discussion 355-346), 10.1097/QAD.0b013e32831db232
14. Liu, S., Li, R., Zhang, R., Chan, C. C., Xi, B., Zhu, Z., Yang, J., Poon, V. K., Zhou, J., Chen, M., Munch, J., Kirchhoff, F., Pleschka, S., Haarmann, T., Dietrich, U., Pan, C., Du, L., Jiang, S., and Zheng, B. (2011) CL-385319 inhibits H5N1 avian influenza A virus infection by blocking viral entry Eur. J. Pharmacol. 660, 460-467 10.1016/j.ejphar.2011.04.013
15. Luo, G., Torri, A., Harte, W. E., Danetz, S., Cianci, C., Tiley, L., Day, S., Mullaney, D., Yu, K. L., Ouellet, C., Dextraze, P., Meanwell, N., Colonno, R., and Krystal, M. (1997) Molecular mechanism underlying the action of a novel fusion inhibitor of influenza A virus J. Virol. 71, 4062-4070
16. Zhu, L., Li, Y., Li, S., Li, H., Qiu, Z., Lee, C., Lu, H., Lin, X., Zhao, R., Chen, L., Wu, J. Z., Tang, G., and Yang, W. (2011) Inhibition of influenza A virus (H1N1) fusion by benzenesulfonamide derivatives targeting viral hemagglutinin PLoS One 6 e29120 10.1371/journal.pone.0029120
17. Motohashi, Y., Igarashi, M., Okamatsu, M., Noshi, T., Sakoda, Y., Yamamoto, N., Ito, K., Yoshida, R., and Kida, H. (2013) Antiviral activity of stachyflin on influenza A viruses of different hemagglutinin subtypes Virol. J. 10, 118 10.1186/1743-422X-10-118
18. Staschke, K. A., Hatch, S. D., Tang, J. C., Hornback, W. J., Munroe, J. E., Colacino, J. M., and Muesing, M. A. (1998) Inhibition of influenza virus hemagglutinin-mediated membrane fusion by a compound related to podocarpic acid Virology 248, 264-274 10.1006/viro.1998.9273
19. Vanderlinden, E., Goktas, F., Cesur, Z., Froeyen, M., Reed, M. L., Russell, C. J., Cesur, N., and Naesens, L. (2010) Novel inhibitors of influenza virus fusion: structure-activity relationship and interaction with the viral hemagglutinin J. Virol. 84, 4277-4288 10.1128/JVI.02325-09
20. Russell, R. J., Kerry, P. S., Stevens, D. J., Steinhauer, D. A., Martin, S. R., Gamblin, S. J., and Skehel, J. J. (2008) Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion Proc. Natl. Acad. Sci. U.S.A. 105, 17736-17741 10.1073/pnas.0807142105
21. Basu, A., Antanasijevic, A., Wang, M., Li, B., Mills, D. M., Ames, J. A., Nash, P. J., Williams, J. D., Peet, N. P., Moir, D. T., Prichard, M. N., Keith, K. A., Barnard, D. L., Caffrey, M., Rong, L., and Bowlin, T. L. (2014) New small molecule entry inhibitors targeting hemagglutinin-mediated influenza A virus fusion J. Virol. 88, 1447-1460 10.1128/JVI.01225-13
22. Vanderlinden, E. and Naesens, L. (2014) Emerging antiviral strategies to interfere with influenza virus entry Med. Res. Rev. 34, 301-339 10.1002/med.21289
23. Tong, S., Zhu, X., Li, Y., Shi, M., Zhang, J., Bourgeois, M., Yang, H., Chen, X., Recuenco, S., Gomez, J., Chen, L. M., Johnson, A., Tao, Y., Dreyfus, C., Yu, W., McBride, R., Carney, P. J., Gilbert, A. T., Chang, J., Guo, Z., Davis, C. T., Paulson, J. C., Stevens, J., Rupprecht, C. E., Holmes, E. C., Wilson, I. A., and Donis, R. O. (2013) New world bats harbor diverse influenza A viruses PLoS Pathog. 9, e1003657 10.1371/journal.ppat.1003657
24. Marsh, G. A., Hatami, R., and Palese, P. (2007) Specific residues of the influenza A virus hemagglutinin viral RNA are important for efficient packaging into budding virions J. Virol. 81, 9727-9736 10.1128/JVI.01144-07
25. Hoffmann, H. H., Palese, P., and Shaw, M. L. (2008) Modulation of influenza virus replication by alteration of sodium ion transport and protein kinase C activity Antiviral Res. 80, 124-134 10.1016/j.antiviral.2008.05.008
26. Niwa, H., Yamamura, K., and Miyazaki, J. (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector Gene 108, 193-199 10.1016/0378-1119(91)90434-D
27. Konig, R., Stertz, S., Zhou, Y., Inoue, A., Hoffmann, H. H., Bhattacharyya, S., Alamares, J. G., Tscherne, D. M., Ortigoza, M. B., Liang, Y., Gao, Q., Andrews, S. E., Bandyopadhyay, S., De Jesus, P., Tu, B. P., Pache, L., Shih, C., Orth, A., Bonamy, G., Miraglia, L., Ideker, T., Garcia-Sastre, A., Young, J. A., Palese, P., Shaw, M. L., and Chanda, S. K. (2010) Human host factors required for influenza virus replication Nature 463, 813-817 10.1038/nature08699
28. Fodor, E., Devenish, L., Engelhardt, O. G., Palese, P., Brownlee, G. G., and Garcia-Sastre, A. (1999) Rescue of influenza A virus from recombinant DNA J. Virol. 73, 9679-9682
29. Krammer, F., Margine, I., Tan, G. S., Pica, N., Krause, J. C., and Palese, P. (2012) A carboxy-terminal trimerization domain stabilizes conformational epitopes on the stalk domain of soluble recombinant hemagglutinin substrates PLoS One 7 e43603 10.1371/journal.pone.0043603
30. Hoffmann, H. H., Kunz, A., Simon, V. A., Palese, P., and Shaw, M. L. (2011) Broad-spectrum antiviral that interferes with de novo pyrimidine biosynthesis Proc. Natl. Acad. Sci. U.S.A. 108, 5777-5782 10.1073/pnas.1101143108
31. Carr, C. M. and Kim, P. S. (1993) A spring-loaded mechanism for the conformational change of influenza hemagglutinin Cell 73, 823-832 10.1016/0092-8674(93)90260-W
32. Xu, R. and Wilson, I. A. (2011) Structural characterization of an early fusion intermediate of influenza virus hemagglutinin J. Virol. 85, 5172-5182 10.1128/JVI.02430-10
33. Qiao, H., Pelletier, S. L., Hoffman, L., Hacker, J., Armstrong, R. T., and White, J. M. (1998) Specific single or double proline substitutions in the "spring-loaded" coiled-coil region of the influenza hemagglutinin impair or abolish membrane fusion activity J. Cell Biol. 141, 1335-1347 10.1083/jcb.141.6.1335
34. Wartchow, C. A., Podlaski, F., Li, S., Rowan, K., Zhang, X., Mark, D., and Huang, K. S. (2011) Biosensor-based small molecule fragment screening with biolayer interferometry J. Comput.-Aided Mol. Des 25, 669-676 10.1007/s10822-011-9439-8
35. Reed, M. L., Yen, H. L., DuBois, R. M., Bridges, O. A., Salomon, R., Webster, R. G., and Russell, C. J. (2009) Amino acid residues in the fusion peptide pocket regulate the pH of activation of the H5N1 influenza virus hemagglutinin protein J. Virol. 83, 3568-3580 10.1128/JVI.02238-08
36. Godley, L., Pfeifer, J., Steinhauer, D., Ely, B., Shaw, G., Kaufmann, R., Suchanek, E., Pabo, C., Skehel, J. J., and Wiley, D. C. et al. 1992, Introduction of intersubunit disulfide bonds in the membrane-distal region of the influenza hemagglutinin abolishes membrane fusion activity Cell 68, 635-645 10.1016/0092-8674(92)90140-8
37. Kemble, G. W., Bodian, D. L., Rose, J., Wilson, I. A., and White, J. M. (1992) Intermonomer disulfide bonds impair the fusion activity of influenza virus hemagglutinin J. Virol. 66, 4940-4950
38. Okuno, Y., Isegawa, Y., Sasao, F., and Ueda, S. (1993) A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains J. Virol. 67, 2552-2558
39. Corti, D., Voss, J., Gamblin, S. J., Codoni, G., Macagno, A., Jarrossay, D., Vachieri, S. G., Pinna, D., Minola, A., Vanzetta, F., Silacci, C., Fernandez-Rodriguez, B. M., Agatic, G., Bianchi, S., Giacchetto-Sasselli, I., Calder, L., Sallusto, F., Collins, P., Haire, L. F., Temperton, N., Langedijk, J. P., Skehel, J. J., and Lanzavecchia, A. (2011) A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins Science 333, 850-856 10.1126/science.1205669
40. Lingwood, D., McTamney, P. M., Yassine, H. M., Whittle, J. R., Guo, X., Boyington, J. C., Wei, C. J., and Nabel, G. J. (2012) Structural and genetic basis for development of broadly neutralizing influenza antibodies Nature 489, 566-570 10.1038/nature11371
41. Bommakanti, G., Citron, M. P., Hepler, R. W., Callahan, C., Heidecker, G. J., Najar, T. A., Lu, X., Joyce, J. G., Shiver, J. W., Casimiro, D. R., ter Meulen, J., Liang, X., and Varadarajan, R. (2010) Design of an HA2-based Escherichia coli expressed influenza immunogen that protects mice from pathogenic challenge Proc. Natl. Acad. Sci. U.S.A. 107, 13701-13706 10.1073/pnas.1007465107
42. Ekiert, D. C., Bhabha, G., Elsliger, M. A., Friesen, R. H., Jongeneelen, M., Throsby, M., Goudsmit, J., and Wilson, I. A. (2009) Antibody recognition of a highly conserved influenza virus epitope Science 324, 246-251 10.1126/science.1171491
43. Krammer, F. and Palese, P. (2014) Universal influenza virus vaccines: need for clinical trials Nat. Immunol. 15, 3-5 10.1038/ni.2761
44. Krammer, F. and Palese, P. (2013) Influenza virus hemagglutinin stalk-based antibodies and vaccines Curr. Opin. Virol. 3, 521-530 10.1016/j.coviro.2013.07.007
45. Shaw, M. L. and Palese, P. (2013) Orthomyxoviridae: the viruses and their replication. In Fields Virology (Knipe, D. M. and Howley, P. M., Eds.), 6 th ed., pp 1151-1185, Wolters Kluwer/Lippincott Williams & Wilkins Health, Philadelphia, PA, USA.
46. Feeney, E. R. and Chung, R. T. (2014) Antiviral treatment of hepatitis C BMJ 349, g3308 10.1136/bmj.g3308
47. Pellecchia, M., Bertini, I., Cowburn, D., Dalvit, C., Giralt, E., Jahnke, W., James, T. L., Homans, S. W., Kessler, H., Luchinat, C., Meyer, B., Oschkinat, H., Peng, J., Schwalbe, H., and Siegal, G. (2008) Perspectives on NMR in drug discovery: a technique comes of age Nat. Rev. Drug Discovery 7, 738-745 10.1038/nrd2606
48. Mayer, M. and Meyer, B. (1999) Characterization of ligand binding by saturation transfer difference NMR spectroscopy Angew. Chem. Int. Ed. 38, 1784-1788 10.1002/(SICI)1521-3773(19990614)38:12<1784::AID-ANIE1784>3.0.CO;2-Q
49. Mayer, M. and Meyer, B. (2001) Group epitope mapping by saturation transfer difference NMR to identify segments of a ligand in direct contact with a protein receptor J. Am. Chem. Soc. 123, 6108-6117 10.1021/ja0100120