Discovery of a prefusion respiratory syncytial virus F-specific monoclonal antibody that provides greater in vivo protection than the murine precursor of palivizumab

Journal of Virology

Volumn 91, Issue 15, 2017, Pages

  Zhao, Min ^a,b   Zheng, Zi Zheng ^a   Chen, Man ^b   Modjarrad, Kayvon ^c   Zhang, Wei ^a   Zhan, Lu Ting ^a   Cao, Jian Li ^a   Sun, Yong Peng ^a   McLellan, Jason S ^d   Graham, Barney S ^b   Xia, Ning Shao ^a  

^a XIAMEN UNIVERSITY   (China)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^d DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Bronchiolitis; Fusion glycoprotein; Monoclonal antibody; Neutralizing antibody; Passive immunization; Respiratory syncytial virus; Therapeutic antibody; Viral pneumonia

Indexed keywords

ANTIVIRUS AGENT; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 1129; MONOCLONAL ANTIBODY 5C4; NEUTRALIZING ANTIBODY; PALIVIZUMAB; PROTEIN F; UNCLASSIFIED DRUG; VIRAL PROTEIN; F PROTEIN, HUMAN RESPIRATORY SYNCYTIAL VIRUS; PROTEIN BINDING; VIRUS ANTIBODY; VIRUS FUSION PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIBODY TITER; ANTIGEN BINDING; ANTIVIRAL ACTIVITY; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; HISTOPATHOLOGY; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IN VITRO STUDY; IN VIVO STUDY; INFECTION PREVENTION; INHIBITION KINETICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; RESPIRATORY SYNCYTIAL VIRUS INFECTION; VIRUS INHIBITION; VIRUS LOAD; WEIGHT CHANGE; WEIGHT REDUCTION; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; DISEASE MODEL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; ISOLATION AND PURIFICATION; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; SERODIAGNOSIS; TREATMENT OUTCOME;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; ANTIVIRAL AGENTS; CELL LINE; DISEASE MODELS, ANIMAL; HUMANS; MICE, INBRED BALB C; NEUTRALIZATION TESTS; PALIVIZUMAB; PROTEIN BINDING; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; TREATMENT OUTCOME; VIRAL FUSION PROTEINS;

EID: 85023182502     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00176-17     Document Type: Article

References (21)

1. 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. https://doi.org/10.1542/peds.102.3.531
2. MedImmune Group. 1998. Full prescribing information for Synagis. MedImmune, LLC, Gaithersburg, MD
3. Johnson S, Oliver C, Prince GA, Hemming VG, Pfarr DS, Wang SC, Dormitzer M, O'Grady J, Koenig S, Tamura JK, Woods R, Bansal G, Couchenour D, Tsao E, Hall WC, Young JF. 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. https://doi.org/10.1086/514115
4. Beeler JA, van Wyke Coelingh K. 1989. Neutralization epitopes of the F glycoprotein of respiratory syncytial virus: effect of mutation upon fusion function. J Virol 63:2941-2950
5. Liljeroos L, Krzyzaniak MA, Helenius A, Butcher SJ. 2013. Architecture of respiratory syncytial virus revealed by electron cryotomography. Proc Natl Acad Sci U S A 110:11133-11138. https://doi.org/10.1073/pnas.1309070110
6. Mejias A, Chavez-Bueno S, Rios AM, Aten MF, Raynor B, Peromingo E, Soni P, Olsen KD, Kiener PA, Gomez AM, Jafri HS, Ramilo O. 2005. Comparative effects of two neutralizing anti-respiratory syncytial virus (RSV) monoclonal antibodies in the RSV murine model: time versus potency. Antimicrob Agents Chemother 49:4700-4707. https://doi.org/ 10.1128/AAC.49.11.4700-4707.2005
7. Wu H, Pfarr DS, Johnson S, Brewah YA, Woods RM, Patel NK, White WI, Young JF, Kiener PA. 2007. Development of motavizumab, an ultrapotent antibody for the prevention of respiratory syncytial virus infection in the upper and lower respiratory tract. J Mol Biol 368:652-665. https://doi.org/10.1016/j.jmb.2007.02.024
8. McLellan JS, Chen M, Kim A, Yang Y, Graham BS, Kwong PD. 2010. Structural basis of respiratory syncytial virus neutralization by motavizumab. Nat Struct Mol Biol 17:248-250. https://doi.org/10.1038/nsmb.1723
9. Ngwuta JO, Chen M, Modjarrad K, Joyce MG, Kanekiyo M, Kumar A, Yassine HM, Moin SM, Killikelly AM, Chuang GY, Druz A, Georgiev IS, Rundlet EJ, Sastry M, Stewart-Jones GB, Yang Y, Zhang B, Nason MC, Capella C, Peeples ME, Ledgerwood JE, McLellan JS, Kwong PD, Graham BS. 2015. Prefusion F-specific antibodies determine the magnitude of RSV neutralizing activity in human sera. Sci Transl Med 7:309ra162. https://doi.org/10.1126/scitranslmed.aac4241
10. McLellan JS, Chen M, Leung S, Graepel KW, Du X, Yang Y, Zhou T, Baxa U, Yasuda E, Beaumont T, Kumar A, Modjarrad K, Zheng Z, Zhao M, Xia N, Kwong PD, Graham BS. 2013. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340: 1113-1117. https://doi.org/10.1126/science.1234914
11. Killikelly AM, Kanekiyo M, Graham BS. 2016. Pre-fusion F is absent on the surface of formalin-inactivated respiratory syncytial virus. Sci Rep 6:34108. https://doi.org/10.1038/srep34108
12. Chen M, Chang JS, Nason M, Rangel D, Gall JG, Graham BS, Ledgerwood JE. 2010. A flow cytometry-based assay to assess RSV-specific neutralizing antibody is reproducible, efficient and accurate. J Immunol Methods 362:180-184. https://doi.org/10.1016/j.jim.2010.08.005
13. Mejias A, Chavez-Bueno S, Rios AM, Saavedra-Lozano J, Fonseca Aten M, Hatfield J, Kapur P, Gomez AM, Jafri HS, Ramilo O. 2004. Anti-respiratory syncytial virus (RSV) neutralizing antibody decreases lung inflammation, airway obstruction, and airway hyperresponsiveness in a murine RSV model. Antimicrob Agents Chemother 48:1811-1822. https://doi.org/10.1128/AAC.48.5.1811-1822.2004
14. McLellan JS, Chen M, Joyce MG, Sastry M, Stewart-Jones GB, Yang Y, Zhang B, Chen L, Srivatsan S, Zheng A, Zhou T, Graepel KW, Kumar A, Moin S, Boyington JC, Chuang GY, Soto C, Baxa U, Bakker AQ, Spits H, Beaumont T, Zheng Z, Xia N, Ko SY, Todd JP, Rao S, Graham BS, Kwong PD. 2013. Structure-based design of a fusion glycoprotein vaccine for respiratory syncytial virus. Science 342:592-598. https://doi.org/10.1126/ science.1243283
15. O'Brien KL, Chandran A, Weatherholtz R, Jafri HS, Griffin MP, Bellamy T, Millar EV, Jensen KM, Harris BS, Reid R, Moulton LH, Losonsky GA, Karron RA, Santosham M, Respiratory Syncytial Virus (RSV) Prevention Study Group. 2015. Efficacy of motavizumab for the prevention of respiratory syncytial virus disease in healthy Native American infants: a phase 3 randomised double-blind placebo-controlled trial. Lancet Infect Dis 15: 1398-1408. https://doi.org/10.1016/S1473-3099(15)00247-9
16. Graham BS, Perkins MD, Wright PF, Karzon DT. 1988. Primary respiratory syncytial virus infection in mice. J Med Virol 26:153-162. https://doi.org/ 10.1002/jmv.1890260207
17. Hotard AL, Shaikh FY, Lee S, Yan D, Teng MN, Plemper RK, Crowe JE, Jr, Moore ML. 2012. A stabilized respiratory syncytial virus reverse genetics system amenable to recombination-mediated mutagenesis. Virology 434:129-136. https://doi.org/10.1016/j.virol.2012.09.022
18. Hallak LK, Collins PL, Knudson W, Peeples ME. 2000. Iduronic acidcontaining glycosaminoglycans on target cells are required for efficient respiratory syncytial virus infection. Virology 271:264-275. https://doi.org/10.1006/viro.2000.0293
19. McLellan JS, Yang Y, Graham BS, Kwong PD. 2011. Structure of respiratory syncytial virus fusion glycoprotein in the postfusion conformation reveals preservation of neutralizing epitopes. J Virol 85:7788-7796. https://doi.org/10.1128/JVI.00555-11
20. Fisher RG, Johnson JE, Dillon SB, Parker RA, Graham BS. 1999. Prophylaxis with respiratory syncytial virus F-specific humanized monoclonal antibody delays and moderately suppresses the native antibody response but does not impair immunity to late rechallenge. J Infect Dis 180: 708-713. https://doi.org/10.1086/314965
21. Graham BS, Davis TH, Tang YW, Gruber WC. 1993. Immunoprophylaxis and immunotherapy of respiratory syncytial virus-infected mice with respiratory syncytial virus-specific immune serum. Pediatric Res 34: 167-172. https://doi.org/10.1203/00006450-199308000-00013