Identification of a small-molecule entry inhibitor for filoviruses

Journal of Virology

Volumn 85, Issue 7, 2011, Pages 3106-3119

  Basu, Arnab ^a   Li, Bing ^a   Mills, Debra M ^a   Panchal, Rekha G ^b   Cardinale, Steven C ^a   Butler, Michelle M ^a   Peet, Norton P ^a   Majgier Baranowska, Helena ^a   Williams, John D ^a   Patel, Ishan ^a   Moir, Donald T ^a   Bavari, Sina ^b   Ray, Ranjit ^c   Farzan, Michael R ^d   Rong, Lijun ^e   Bowlin, Terry L ^a  

^a MICROBIOTIX INC   (United States)

^b UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

^c SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; ASPARAGINE; BENZODIAZEPINE DERIVATIVE; ISOLEUCINE; LEUCINE; LYSINE; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARENAVIRUS; ARTICLE; CELL ASSAY; CELL STRAIN; CELL STRAIN BHK; CONTROLLED STUDY; COWPOX VIRUS; CRYSTAL STRUCTURE; DRUG CONFORMATION; DRUG PROTEIN BINDING; DRUG STRUCTURE; EBOLA VIRUS; FILOVIRUS; HELA CELL; HEPATITIS C VIRUS; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; HYDROPHOBICITY; IC 50; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INHIBITION KINETICS; MARBURG VIRUS; MUTATIONAL ANALYSIS; NONHUMAN; PREDICTION; PRIORITY JOURNAL; RIFT VALLEY FEVER BUNYAVIRUS; SARS CORONAVIRUS; TACARIBE ARENAVIRUS; VACCINIA VIRUS; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VERO CELL; VIRUS ENTRY; VIRUS INHIBITION;

ANTIVIRAL AGENTS; BENZODIAZEPINES; DNA MUTATIONAL ANALYSIS; DRUG EVALUATION, PRECLINICAL; DRUG RESISTANCE, VIRAL; EBOLAVIRUS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; INHIBITORY CONCENTRATION 50; MARBURGVIRUS; MODELS, MOLECULAR; MUTATION, MISSENSE; PROTEIN BINDING; VIRUS INTERNALIZATION;

EBOLA VIRUS; LAKE VICTORIA MARBURGVIRUS;

EID: 79952590815     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01456-10     Document Type: Article

References (64)

1. Aman, M. J., et al. 2009. Development of a broad-spectrum antiviral with activity against Ebola virus. Antiviral Res. 83:245-251.
2. Barnard, D. L., et al. 1999. 2-5A-DNA conjugate inhibition of respiratory syncytial virus replication: effects of oligonucleotide structure modifications and RNA target site selection. Antiviral Res. 41:119-134. (Pubitemid 29146124)
3. Barnard, D. L., et al. 2002. Coumarins and pyranocoumarins, potential novel pharmacophores for inhibition of measles virus replication. Antivir. Chem. Chemother. 13:39-59.
4. Basu, A., et al. 2007. Sulfated homologues of heparin inhibit hepatitis C virus entry into mammalian cells. J. Virol. 81:3933-3941. (Pubitemid 46586889)
5. Basu, A., et al. 2006. Stellate cell apoptosis by a soluble mediator from immortalized human hepatocytes. Apoptosis 11:1391-1400. (Pubitemid 44035950)
6. Bosio, C. M., et al. 2004. Ebola and Marburg virus-like particles activate human myeloid dendritic cells. Virology 326:280-287. (Pubitemid 39078259)
7. Bray, M. 2003. Defense against filoviruses used as biological weapons. Antiviral Res. 57:53-60. (Pubitemid 36254721)
8. Bray, M., and J. Paragas. 2002. Experimental therapy of filovirus infections. Antiviral Res. 54:1-17. (Pubitemid 34219170)
9. Bray, M., J. L. Raymond, T. Geisbert, and R. O. Baker. 2002. 3-Deazaneplanocin A induces massively increased interferon-alpha production in Ebola virus-infected mice. Antiviral Res. 55:151-159. (Pubitemid 34655650)
10. Chan, S. Y., et al. 2001. Folate receptor-alpha is a cofactor for cellular entry by Marburg and Ebola viruses. Cell 106:117-126. (Pubitemid 32709963)
11. Chandran, K., N. J. Sullivan, U. Felbor, S. P. Whelan, and J. M. Cunningham. 2005. Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308:1643-1645.
12. Cianci, C., et al. 2004. Orally active fusion inhibitor of respiratory syncytial virus. Antimicrob. Agents Chemother. 48:413-422.
13. Guo, Q., et al. 2003. Biochemical and genetic characterizations of a novel human immunodeficiency virus type 1 inhibitor that blocks gp120-CD4 interactions. J. Virol. 77:10528-10536. (Pubitemid 37129696)
14. Guo, Y., et al. 2009. Analysis of hemagglutinin-mediated entry tropism of H5N1 avian influenza. Virol. J. 6:39.
15. 2 phase of the cell cycle by inhibiting p34cdc2 activity. J. Virol. 69:6705-6711.
16. Ito, H., S. Watanabe, A. Takada, and Y. Kawaoka. 2001. Ebola virus glycoprotein: proteolytic processing, acylation, cell tropism, and detection of neutralizing antibodies. J. Virol. 75:1576-1580. (Pubitemid 32094718)
17. Jane-Valbuena, J., L. A. Breun, L. A. Schiff, and M. L. Nibert. 2002. Sites and determinants of early cleavages in the proteolytic processing pathway of reovirus surface protein sigma3. J. Virol. 76:5184-5197.
18. Jeffers, S. A., D. A. Sanders, and A. Sanchez. 2002. Covalent modifications of the Ebola virus glycoprotein. J. Virol. 76:12463-12472. (Pubitemid 35386932)
19. Kondru, R., et al. 2008. Molecular interactions of CCR5 with major classes of small-molecule anti-HIV CCR5 antagonists. Mol. Pharmacol. 73:789-800.
20. Kuhn, J. H., W. Li, S. R. Radoshitzky, H. Choe, and M. Farzan. 2007. Severe acute respiratory syndrome coronavirus entry as a target of antiviral therapies. Antivir. Ther. 12:639-650.
21. Kuhn, J. H., et al. 2006. Conserved receptor-binding domains of Lake Victoria marburgvirus and Zaire ebolavirus bind a common receptor. J. Biol. Chem. 281:15951-15958.
22. Larson, R. A., et al. 2008. Identification of a broad-spectrum arenavirus entry inhibitor. J. Virol. 82:10768-10775. (Pubitemid 352691167)
23. Lasala, F., E. Arce, J. R. Otero, J. Rojo, and R. Delgado. 2003. Mannosyl glycodendritic structure inhibits DC-SIGN-mediated Ebola virus infection in cis and in trans. Antimicrob. Agents Chemother. 47:3970-3972.
24. Lee, A. M., et al. 2008. Unique small molecule entry inhibitors of hemorrhagic fever arenaviruses. J. Biol. Chem. 283:18734-18742.
25. Lee, J. E., et al. 2008. Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 454:177-182. (Pubitemid 351969896)
26. Lee, J. E., et al. 2008. Complex of a protective antibody with its Ebola virus GP peptide epitope: unusual features of a V lambda x light chain. J. Mol. Biol. 375:202-216.
27. Leroy, E. M., et al. 2009. Human Ebola outbreak resulting from direct exposure to fruit bats in Luebo, Democratic Republic of Congo, 2007. Vector Borne Zoonotic Dis. 9:723-728.
28. Lipinski, C. A., F. Lombardo, B. W. Dominy, and P. J. Feeney. 2001. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv Rev. 46:3-26.
29. Manicassamy, B., J. Wang, H. Jiang, and L. Rong. 2005. Comprehensive analysis of Ebola virus GP1 in viral entry. J. Virol. 79:4793-4805. (Pubitemid 40464230)
30. Manicassamy, B., et al. 2007. Characterization of Marburg virus glycoprotein in viral entry. Virology 358:79-88. (Pubitemid 46061428)
31. Martinez, O., et al. 2010. Zaire Ebola virus entry into human dendritic cells is insensitive to cathepsin L inhibition. Cell. Microbiol. 12:148-157.
32. Meyer, K., A. Basu, and R. Ray. 2000. Functional features of hepatitis C virus glycoproteins for pseudotype virus entry into mammalian cells. Virology 276:214-226.
33. Panchal, R. G., K. P. Kota, K. B. Spurgers, G. Ruthel, J. P. Tran, R. C. Boltz, and S. Bavari. Development of high-content imaging assays for lethal viral pathogens. J. Biomol. Screen. 15:755-765.
34. Peterson, A. T., D. S. Carroll, J. N. Mills, and K. M. Johnson. 2004. Potential mammalian filovirus reservoirs. Emerg. Infect. Dis. 10:2073-2081.
35. Plemper, R. K., et al. 2005. Design of a small-molecule entry inhibitor with activity against primary measles virus strains. Antimicrob. Agents Chemother. 49:3755-3761.
36. Plemper, R. K., et al. 2004. A target site for template-based design of measles virus entry inhibitors. Proc. Natl. Acad. Sci. U. S. A. 101:5628-5633.
37. Radoshitzky, S. R., et al. 2007. Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature 446:92-96. (Pubitemid 46348039)
38. Radoshitzky, S. R., et al. 2008. Receptor determinants of zoonotic transmission of New World hemorrhagic fever arenaviruses. Proc. Natl. Acad. Sci. U. S. A. 105:2664-2669.
39. Ray, R. B., et al. 2004. Ebola virus glycoprotein-mediated anoikis of primary human cardiac microvascular endothelial cells. Virology 321:181-188. (Pubitemid 38406033)
40. Roche, S., S. Bressanelli, F. A. Rey, and Y. Gaudin. 2006. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313:187-191. (Pubitemid 44066243)
41. Roche, S., F. A. Rey, Y. Gaudin, and S. Bressanelli. 2007. Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science 315:843-848.
42. Rumschlag-Booms, E., Y. Guo, J. Wang, M. Caffrey, and L. Rong. 2009. Comparative analysis between a low pathogenic and a high pathogenic influenza H5 hemagglutinin in cell entry. Virol. J. 6:76.
43. Russell, C. A., et al. 2008. Influenza vaccine strain selection and recent studies on the global migration of seasonal influenza viruses. Vaccine 26(Suppl. 4):D31-D34.
44. Sanchez, A., et al. 2001. Filoviridae: Marburg and Ebola viruses, p. 1279-1304. In D. M. Knipe and P. M. Howley (ed.), Fields virology. Lippincott, Williams & Wilkins, Philadelphia PA.
45. Sanchez, A., et al. (ed.). 2001. Filoviridae: Marburg and Ebola viruses, vol. 1. Lippincott, Williams & Wilkins, Philadelphia, PA.
46. Schornberg, K., et al. 2006. Role of endosomal cathepsins in entry mediated by the Ebola virus glycoprotein. J. Virol. 80:4174-4178.
47. Shah, P. P., et al. 2010. A small-molecule oxocarbazate inhibitor of human cathepsin L blocks severe acute respiratory syndrome and Ebola pseudotype virus infection into human embryonic kidney 293T cells. Mol. Pharmacol. 78:319-324.
48. Shimojima, M., et al. 2006. Tyro3 family-mediated cell entry of Ebola and Marburg viruses. J. Virol. 80:10109-10116. (Pubitemid 44522604)
49. Sidwell, R. W., and D. F. Smee. 2000. In vitro and in vivo assay systems for study of influenza virus inhibitors. Antiviral Res. 48:1-16.
50. Silvestri, L. S., et al. 2007. Involvement of vacuolar protein sorting pathway in Ebola virus release independent of TSG101 interaction. J. Infect. Dis. 196(Suppl. 2):S264-S270.
51. Simmons, G., et al. 2003. DC-SIGN and DC-SIGNR bind Ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 305:115-123. (Pubitemid 36062817)
52. Simmons, G., et al. 2003. Folate receptor alpha and caveolae are not required for Ebola virus glycoprotein-mediated viral infection. J. Virol. 77:13433-13438. (Pubitemid 37494340)
53. Simmons, G., R. J. Wool-Lewis, F. Baribaud, R. C. Netter, and P. Bates. 2002. Ebola virus glycoproteins induce global surface protein down-modulation and loss of cell adherence. J. Virol. 76:2518-2528. (Pubitemid 34150720)
54. Stroher, U., et al. 2001. Infection and activation of monocytes by Marburg and Ebola viruses. J. Virol. 75:11025-11033. (Pubitemid 33031570)
55. Sullivan, N. J., A. Sanchez, P. E. Rollin, Z. Y. Yang, and G. J. Nabel. 2000. Development of a preventive vaccine for Ebola virus infection in primates. Nature 408:605-609.
56. Takada, A., and Y. Kawaoka. 2001. The pathogenesis of Ebola hemorrhagic fever. Trends Microbiol. 9:506-511. (Pubitemid 32939359)
57. Tilton, J. C., and R. W. Doms. 2010. Entry inhibitors in the treatment of HIV-1 infection. Antiviral Res. 85:91-100.
58. van Kooyk, Y., A. Engering, A. N. Lekkerkerker, I. S. Ludwig, and T. B. Geijtenbeek. 2004. Pathogens use carbohydrates to escape immunity induced by dendritic cells. Curr. Opin. Immunol. 16:488-493.
59. Volchkov, V. E., et al. 1995. GP mRNA of Ebola virus is edited by the Ebola virus polymerase and by T7 and vaccinia virus polymerases. Virology 214:421-430. (Pubitemid 26029511)
60. Wang, Q. Y., et al. 2009. A small-molecule dengue virus entry inhibitor. Antimicrob. Agents Chemother. 53:1823-1831.
61. Warren, T. K., et al. 2010. Antiviral activity of a small-molecule inhibitor of filovirus infection. Antimicrob. Agents Chemother. 54:2152-2159.
62. Yang, Z. Y., et al. 2000. Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury. Nat. Med. 6:886-889.
63. Zhang, J. H., T. D. Chung, and K. R. Oldenburg. 1999. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J. Biomol. Scree.n. 4:67-73.
64. Zhang, N., et al. 2002. In vitro inhibition of the measles virus by novel ring-expanded ('fat') nucleoside analogues containing the imidazo[4,5-e]- diazepine ring system. Bioorg. Med. Chem. Lett. 12:3391-3394.