Respiratory syncytial virus-neutralizing monoclonal antibodies motavizumab and palivizumab inhibit fusion

Journal of Virology

Volumn 84, Issue 16, 2010, Pages 8132-8140

  Huang, Kelly ^a   Incognito, Len ^a   Cheng, Xing ^a   Ulbrandt, Nancy D ^a   Wu, Herren ^a  

^a MEDIMMUNE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MOTAVIZUMAB; PALIVIZUMAB; PROTEIN F; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CELL FUSION; CELL MEMBRANE; DRUG MECHANISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN TARGETING; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; VIRUS ATTACHMENT; VIRUS INHIBITION; VIRUS NEUTRALIZATION; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; ANTIVIRAL AGENTS; CELL FUSION; CELL LINE; CERCOPITHECUS AETHIOPS; HUMANS; PROTEIN BINDING; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; VIRAL FUSION PROTEINS; VIRUS ATTACHMENT; VIRUS INTERNALIZATION; VIRUS REPLICATION;

RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 77954995414     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02699-09     Document Type: Article

References (57)

1. Bachelder, R. E., J. Bilancieri, W. Lin, and N. L. Letvin. 1995. A human recombinant Fab identifies a human immunodeficiency virus type 1-induced conformational change in cell surface-expressed CD4. J. Virol. 69:5734-5742.
2. Barbas, C. F., III, E. Bjorling, F. Chiodi, N. Dunlop, D. Cababa, T. M. Jones, S. L. Zebedee, M. A. Persson, P. L. Nara, and E. Norrby. 1992. Recombinant human Fab fragments neutralize human type 1 immunodeficiency virus in vitro. Proc. Natl. Acad. Sci. U. S. A. 89:9339-9343.
3. Barbato, G., E. Bianchi, P. Ingallinella, W. H. Hurni, M. D. Miller, G. Ciliberto, R. Cortese, R. Bazzo, J. W. Shiver, and A. Pessi. 2003. Structural analysis of the epitope of the anti-HIV antibody 2F5 sheds light into its mechanism of neutralization and HIV fusion. J. Mol. Biol. 330:1101-1115.
4. Beeler, J. A., and K. van Wyke Coelingh. 1989. Neutralization epitopes of the F glycoprotein of respiratory syncytial virus: effect of mutation upon fusion function. J. Virol. 63:2941-2950.
5. Blumenthal, R., S. A. Gallo, M. Viard, Y. Raviv, and A. Puri. 2002. Fluorescent lipid probes in the study of viral membrane fusion. Chem. Phys. Lipids 116:39-55.
6. Boukhvalova, M. S., G. A. Prince, and J. C. Blanco. 2007. Respiratory syncytial virus infects and abortively replicates in the lungs in spite of preexisting immunity. J. Virol. 81:9443-9450.
7. Boyce, T. G., B. G. Mellen, E. F. Mitchel, Jr., P. F. Wright, and M. R. Griffin. 2000. Rates of hospitalization for respiratory syncytial virus infection among children in Medicaid. J. Pediatr. 137:865-870.
8. Branigan, P. J., C. Liu, N. D. Day, L. L. Gutshall, R. T. Sarisky, and A. M. Del Vecchio. 2005. Use of a novel cell-based fusion reporter assay to explore the host range of human respiratory syncytial virus F protein. Virol. J. 2:54.
9. Budge, P. J., Y. Li, J. A. Beeler, and B. S. Graham. 2004. RhoA-derived peptide dimers share mechanistic properties with other polyanionic inhibitors of respiratory syncytial virus (RSV), including disruption of viral attachment and dependence on RSV G. J. Virol. 78:5015-5022.
10. Calder, L. J., L. Gonzalez-Reyes, B. Garcia-Barreno, S. A. Wharton, J. J. Skehel, D. C. Wiley, and J. A. Melero. 2000. Electron microscopy of the human respiratory syncytial virus fusion protein and complexes that it forms with monoclonal antibodies. Virology 271:122-131.
11. Castilow, E. M., and S. M. Varga. 2008. Overcoming T cell-mediated immunopathology to achieve safe RSV vaccination. Future Virol. 3:445-454.
12. Cianci, C., N. Meanwell, and M. Krystal. 2005. Antiviral activity and molecular mechanism of an orally active respiratory syncytial virus fusion inhibitor. J. Antimicrob. Chemother. 55:289-292.
13. Collins, P. L., and J. E. Crowe, Jr. 2007. Respiratory syncytial virus and metapneumovirus, p. 1601-1645. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 5th ed., vol. II. Lippincott/The Williams & Wilkins Co., Philadelphia, PA.
14. Collins, P. L., and G. W. Wertz. 1983. cDNA cloning and transcriptional mapping of nine polyadenylylated RNAs encoded by the genome of human respiratory syncytial virus. Proc. Natl. Acad. Sci. U. S. A. 80:3208-3212.
15. Douglas, J. L., M. L. Panis, E. Ho, K. Y. Lin, S. H. Krawczyk, D. M. Grant, R. Cai, S. Swaminathan, X. Chen, and T. Cihlar. 2005. Small molecules VP-14637 and JNJ-2408068 inhibit respiratory syncytial virus fusion by similar mechanisms. Antimicrob. Agents Chemother. 49:2460-2466.
16. Douglas, J. L., M. L. Panis, E. Ho, K. Y. Lin, S. H. Krawczyk, D. M. Grant, R. Cai, S. Swaminathan, and T. Cihlar. 2003. Inhibition of respiratory syncytial virus fusion by the small molecule VP-14637 via specific interactions with F protein. J. Virol. 77:5054-5064.
17. Edwards, M. J., and N. J. Dimmock. 2000. Two influenza A virus-specific Fabs neutralize by inhibiting virus attachment to target cells, while neutralization by their IgGs is complex and occurs simultaneously through fusion inhibition and attachment inhibition. Virology 278:423-435.
18. Glezen, W. P., L. H. Taber, A. L. Frank, and J. A. Kasel. 1986. Risk of primary infection and reinfection with respiratory syncytial virus. Am. J. Dis. Child. 140:543-546.
19. Gower, T. L., M. K. Pastey, M. E. Peeples, P. L. Collins, L. H. McCurdy, T. K. Hart, A. Guth, T. R. Johnson, and B. S. Graham. 2005. RhoA signaling is required for respiratory syncytial virus-induced syncytium formation and filamentous virion morphology. J. Virol. 79:5326-5336.
20. Hallak, L. K., P. L. Collins, W. Knudson, and M. E. Peeples. 2000. Iduronic acid-containing glycosaminoglycans on target cells are required for efficient respiratory syncytial virus infection. Virology 271:264-275.
21. Hansbro, N. G., J. C. Horvat, P. A. Wark, and P. M. Hansbro. 2008. Understanding the mechanisms of viral induced asthma: new therapeutic directions. Pharmacol. Ther. 117:313-353.
22. Hardy, R. W., S. B. Harmon, and G. W. Wertz. 1999. Diverse gene junctions of respiratory syncytial virus modulate the efficiency of transcription termination and respond differently to M2-mediated antitermination. J. Virol. 73:170-176.
23. Hosoya, M., J. Balzarini, S. Shigeta, and E. De Clercq. 1991. Differential inhibitory effects of sulfated polysaccharides and polymers on the replication of various myxoviruses and retroviruses, depending on the composition of the target amino acid sequences of the viral envelope glycoproteins. Antimicrob. Agents Chemother. 35:2515-2520.
24. Huerta, L., E. Lamoyi, A. Baez-Saldana, and C. Larralde. 2002. Human immunodeficiency virus envelope-dependent cell-cell fusion: a quantitative fluorescence cytometric assay. Cytometry 47:100-106.
25. Imai, M., K. Sugimoto, K. Okazaki, and H. Kida. 1998. Fusion of influenza virus with the endosomal membrane is inhibited by monoclonal antibodies to defined epitopes on the hemagglutinin. Virus Res. 53:129-139.
26. Jin, H., D. Clarke, H. Z. Zhou, X. Cheng, K. Coelingh, M. Bryant, and S. Li. 1998. Recombinant human respiratory syncytial virus (RSV) from cDNA and construction of subgroup A and B chimeric RSV. Virology 251:206-214.
27. Johnson, S., C. Oliver, G. A. Prince, V. G. Hemming, D. S. Pfarr, S. C. Wang, M. Dormitzer, J. O'Grady, S. Koenig, J. K. Tamura, R. Woods, G. Bansal, D. Couchenour, E. Tsao, W. C. Hall, and J. F. Young. 1997. Development of a humanized monoclonal antibody (MEDI-493) with potent in vitro and in vivo activity against respiratory syncytial virus. J. Infect. Dis. 176:1215-1224.
28. Lamb, R. A., and T. S. Jardetzky. 2007. Structural basis of viral invasion: lessons from paramyxovirus F. Curr. Opin. Struct. Biol. 17:427-436.
29. Law, M., and L. Hangartner. 2008. Antibodies against viruses: passive and active immunization. Curr. Opin. Immunol. 20:486-492.
30. Leyssen, P., E. De Clercq, and J. Neyts. 2008. Molecular strategies to inhibit the replication of RNA viruses. Antivir. Res. 78:9-25.
31. Lopez, J. A., R. Bustos, C. Orvell, M. Berois, J. Arbiza, B. Garcia-Barreno, and J. A. Melero. 1998. Antigenic structure of human respiratory syncytial virus fusion glycoprotein. J. Virol. 72:6922-6928.
32. McInerney, T. L., L. McLain, S. J. Armstrong, and N. J. Dimmock. 1997. A human IgG1 (b12) specific for the CD4 binding site of HIV-1 neutralizes by inhibiting the virus fusion entry process, but b12 Fab neutralizes by inhibiting a postfusion event. Virology 233:313-326.
33. McLellan, J. S., M. Chen, A. Kim, Y. Yang, B. S. Graham, and P. D. Kwong. 2010. Structural basis of respiratory syncytial virus neutralization by motavizumab. Nat. Struct. Mol. Biol. 17:248-250.
34. Meissner, H. C., M. B. Rennels, L. K. Pickering, and C. B. Hall. 2004. Risk of severe respiratory syncytial virus disease, identification of high risk infants and recommendations for prophylaxis with palivizumab. Pediatr. Infect. Dis. J. 23:284-285.
35. Morton, C. J., R. Cameron, L. J. Lawrence, B. Lin, M. Lowe, A. Luttick, A. Mason, J. McKimm-Breschkin, M. W. Parker, J. Ryan, M. Smout, J. Sullivan, S. P. Tucker, and P. R. Young. 2003. Structural characterization of respiratory syncytial virus fusion inhibitor escape mutants: homology model of the F protein and a syncytium formation assay. Virology 311:275-288.
36. Ohki, S., J. Z. Liu, J. Schaller, and R. C. Welliver. 2003. The compound DATEM inhibits respiratory syncytial virus fusion activity with epithelial cells. Antivir. Res. 58:115-124.
37. Osiowy, C., and R. Anderson. 1995. Neutralization of respiratory syncytial virus after cell attachment. J. Virol. 69:1271-1274.
38. Peeples, M. E., and P. L. Collins. 2000. Mutations in the 5′ trailer region of a respiratory syncytial virus minigenome which limit RNA replication to one step. J. Virol. 74:146-155.
39. Razinkov, V., A. Gazumyan, A. Nikitenko, G. Ellestad, and G. Krishnamurthy. 2001. RFI-641 inhibits entry of respiratory syncytial virus via interactions with fusion protein. Chem. Biol. 8:645-659.
40. Ruiz-Arguello, M. B., D. Martin, S. A. Wharton, L. J. Calder, S. R. Martin, O. Cano, M. Calero, B. Garcia-Barreno, J. J. Skehel, and J. A. Melero. 2004. Thermostability of the human respiratory syncytial virus fusion protein before and after activation: implications for the membrane-fusion mechanism. J. Gen. Virol. 85:3677-3687.
41. Shay, D. K., R. C. Holman, R. D. Newman, L. L. Liu, J. W. Stout, and L. J. Anderson. 1999. Bronchiolitis-associated hospitalizations among US children, 1980-1996. JAMA 282:1440-1446.
42. Sidwell, R. W., and D. L. Barnard. 2006. Respiratory syncytial virus infections: recent prospects for control. Antivir. Res. 71:379-390.
43. Simoes, E., X. Carbonell, G. Losonsky, M. Hultquist, B. Harris, and E. Connor. 2007. Phase III trial of motavizumab, an enhanced potency respiratory syncytial virus (RSV)-specific monoclonal antibody for the prevention of serious RSV disease in high risk infants. Abstr. 48th Annu. Meet. Eur. Soc. Paediatr. Res.
44. Smith, B. J., M. C. Lawrence, and P. M. Colman. 2002. Modelling the structure of the fusion protein from human respiratory syncytial virus. Protein Eng. 15:365-371.
45. Srinivasakumar, N., P. L. Ogra, and T. D. Flanagan. 1991. Characteristics of fusion of respiratory syncytial virus with HEp-2 cells as measured by R18 fluorescence dequenching assay. J. Virol. 65:4063-4069.
46. Stegmann, T., P. Schoen, R. Bron, J. Wey, I. Bartoldus, A. Ortiz, J. L. Nieva, and J. Wilschut. 1993. Evaluation of viral membrane fusion assays. Comparison of the octadecylrhodamine dequenching assay with the pyrene excimer assay. Biochemistry 32:11330-11337.
47. Sui, J., W. C. Hwang, S. Perez, G. Wei, D. Aird, L. M. Chen, E. Santelli, B. Stec, G. Cadwell, M. Ali, H. Wan, A. Murakami, A. Yammanuru, T. Han, N. J. Cox, L. A. Bankston, R. O. Donis, R. C. Liddington, and W. A. Marasco. 2009. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 16:265-273.
48. Techaarpornkul, S., N. Barretto, and M. E. Peeples. 2001. Functional analysis of recombinant respiratory syncytial virus deletion mutants lacking the small hydrophobic and/or attachment glycoprotein gene. J. Virol. 75:6825-6834.
49. Teng, M. N., and P. L. Collins. 1998. Identification of the respiratory syncytial virus proteins required for formation and passage of helper-dependent infectious particles. J. Virol. 72:5707-5716.
50. The IMpact-RSV Study Group. 1998. Palivizumab, a humanized respiratory syncytial virus monoclonal antibody, reduces hospitalization from respiratory syncytial virus infection in high-risk infants. Pediatrics 102:531-537.
51. Wu, H., D. S. Pfarr, S. Johnson, Y. A. Brewah, R. M. Woods, N. K. Patel, W. I. White, J. F. Young, and P. A. Kiener. 2007. Development of motavizumab, an ultra-potent antibody for the prevention of respiratory syncytial virus infection in the upper and lower respiratory tract. J. Mol. Biol. 368: 652-665.
52. Wu, H., D. S. Pfarr, G. A. Losonsky, and P. A. Kiener. 2008. Immunoprophylaxis of RSV infection: advancing from RSV-IGIV to palivizumab and motavizumab. Curr. Top. Microbiol. Immunol. 317:103-123.
53. Wu, H., D. S. Pfarr, Y. Tang, L. L. An, N. K. Patel, J. D. Watkins, W. D. Huse, P. A. Kiener, and J. F. Young. 2005. Ultra-potent antibodies against respiratory syncytial virus: effects of binding kinetics and binding valence on viral neutralization. J. Mol. Biol. 350:126-144.
54. Wunderli-Allenspach, H., M. Gunthert, and S. Ott. 1993. Inactivation of PR8 influenza virus through the octadecylrhodamine B chloride membrane marker. Biochemistry 32:900-907.
55. Wunderli-Allenspach, H., and S. Ott. 1990. Kinetics of fusion and lipid transfer between virus receptor containing liposomes and influenza viruses as measured with the octadecylrhodamine B chloride assay. Biochemistry 29:1990-1997.
56. Xie, Y. Y., X. D. Zhao, L. P. Jiang, H. L. Liu, L. J. Wang, P. Fang, K. L. Shen, Z. D. Xie, Y. P. Wu, and X. Q. Yang. 2006. Inhibition of respiratory syncytial virus in cultured cells by nucleocapsid gene targeted deoxyribozyme (DNAzyme). Antivir. Res. 71:31-41.
57. Zhao, X., M. Singh, V. N. Malashkevich, and P. S. Kim. 2000. Structural characterization of the human respiratory syncytial virus fusion protein core. Proc. Natl. Acad. Sci. U. S. A. 97:14172-14177.