Monoclonal antibody against g glycoprotein increases respiratory syncytial virus clearance in vivo and prevents vaccineenhanced diseases

PLoS ONE

Volumn 12, Issue 1, 2017, Pages

  Lee, Hyo Jeong ^a   Lee, Jeong Yoon ^a   Park, Min Hee ^a   Kim, Joo Young ^a   Chang, Jun ^a  

^a Ewha Womans University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CYSTEINE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 3A5; MONOCLONAL ANTIBODY 5H6; PALIVIZUMAB; THROMBOSPONDIN; UNCLASSIFIED DRUG; G GLYCOPROTEIN, RESPIRATORY SYNCYTIAL VIRUS; RESPIRATORY SYNCYTIAL VIRUS VACCINE; VIRUS FUSION PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHEMOTAXIS; CONTROLLED STUDY; DRUG PROTEIN BINDING; EPITOPE MAPPING; FEMALE; HUMAN; HUMAN CELL; HUMAN RESPIRATORY SYNCYTIAL VIRUS; HUMAN RESPIRATORY SYNCYTIAL VIRUS A; HUMAN RESPIRATORY SYNCYTIAL VIRUS B; IN VIVO STUDY; MOUSE; NONHUMAN; RESPIRATORY SYNCYTIAL VIRUS INFECTION; VIRAL CLEARANCE; VIRUS LOAD; WEIGHT REDUCTION; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; DISEASE COURSE; IMMUNOLOGY; PATHOLOGY; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS;

ANIMALS; ANTIBODIES, MONOCLONAL; CELLS, CULTURED; DISEASE PROGRESSION; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS VACCINES; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; VIRAL FUSION PROTEINS;

EID: 85009250357     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0169139     Document Type: Article

References (43)

1. Gonzalez PA, Bueno SM, Carreno LJ, Riedel CA, Kalergis AM. Respiratory syncytial virus infection and immunity. Rev Med Virol. 2012; 22(4):230-44. doi: 10.1002/rmv.1704 PMID: 22290692
2. Afonso CL, Amarasinghe GK, Banyai K, Bao Y, Basler CF, Bavari S, et al. Taxonomy of the order Mononegavirales: update 2016. Arch Virol. 2016; 161(8):2351-60. Pub Med Central PMCID: PMCPMC4947412. doi: 10.1007/s00705-016-2880-1 PMID: 27216929
3. Kim TH, Lee HK. Innate immune recognition of respiratory syncytial virus infection. BMB Rep. 2014; 47:184-91. Pub Med Central PMCID: PMCPMC4163887. doi: 10.5483/BMBRep.2014.47.4.050 PMID: 24568879
4. Lambert L, Sagfors AM, Openshaw PJ, Culley FJ. Immunity to RSV in Early-Life. Front Immunol. 2014; 5:466. Pub Med Central PMCID: PMCPMC4179512. doi: 10.3389/fimmu.2014.00466 PMID: 25324843
5. Hall CB, Weinberg GA, Iwane MK, Blumkin AK, Edwards KM, Staat MA, et al. The burden of respiratory syncytial virus infection in young children. N Engl J Med. 2009; 360(6):588-98. Pub Med Central PMCID: PMCPMC4829966. doi: 10.1056/NEJMoa0804877 PMID: 19196675
6. Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ, et al. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and metaanalysis. Lancet. 2010; 375(9725):1545-55. Pub Med Central PMCID: PMCPMC2864404. doi: 10. 1016/S0140-6736(10)60206-1 PMID: 20399493
7. Knudson CJ, Hartwig SM, Meyerholz DK, Varga SM. RSV vaccine-enhanced disease is orchestrated by the combined actions of distinct CD4 T cell subsets. PLoS Pathog. 2015; 11(3):e1004757. Pub Med Central PMCID: PMCPMC4358888. doi: 10.1371/iournal.ppat.1004757 PMID: 25769044
8. Kim HW, Canchola JG, Brandt CD, Pyles G, Chanock RM, Jensen K, et al. Respiratory syncytial virus disease in infants despite prior administration of antigenic inactivated vaccine. Am J Epidemiol. 1969; 89(4):422-34. PMID: 4305198
9. Chin J, Magoffin RL, Shearer LA, Schieble JH, Lennette EH. Field evaluation of a respiratory syncytial virus vaccine and a trivalent parainfluenza virus vaccine in a pediatric population. Am J Epidemiol. 1969; 89(4):449-63. PMID: 4305200
10. Fulginiti VA, Eller JJ, Sieber OF, Joyner JW, Minamitani M, Meiklejohn G. Respiratory virus immunization. I. A field trial of two inactivated respiratory virus vaccines; an aqueous trivalent parainfluenza virus vaccine and an alum-precipitated respiratory syncytial virus vaccine. Am J Epidemiol. 1969; 89(4):435-48. PMID: 4305199
11. Simoes EA. Immunoprophylaxis of respiratory syncytial virus: global experience. Respir Res. 2002; 3 Suppl 1:S26-33. Pub Med Central PMCID: PMCPMC1866370.
12. Johnson S, Oliver C, Prince GA, Hemming VG, Pfarr DS, Wang SC, et al. Development of a humanized monoclonal antibody (MEDI-493) with potent in vitro and in vivo activity against respiratory syncytial virus. J Infect Dis. 1997; 176(5):1215-24. PMID: 9359721
13. Bourgeois C, Bour JB, Lidholt K, Gauthray C, Pothier P. Heparin-like structures on respiratory syncytial virus are involved in its infectivity in vitro. J Virol. 1998; 72(9):7221-7. Pub Med Central PMCID: PMCPMC109944. PMID: 9696816
14. Malhotra R, Ward M, Bright H, Priest R, Foster MR, Hurle M, et al. Isolation and characterisation of potential respiratory syncytial virus receptor(s) on epithelial cells. Microbes Infect. 2003; 5(2):123-33. PMID: 12650770
15. Tripp RA, Jones LP, Haynes LM, Zheng H, Murphy PM, Anderson LJ. CX3C chemokine mimicry by respiratory syncytial virus G glycoprotein. Nat Immunol. 2001; 2(8):732-8. doi: 10.1038/90675 PMID: 11477410
16. Johnson TR, Mc Lellan JS, Graham BS. Respiratory syncytial virus glycoprotein G interacts with DC-SIGN and L-SIGN to activate ERK1 and ERK2. J Virol. 2012; 86(3):1339-47. Pub Med Central PMCID: PMCPMC3264376. doi: 10.1128/JVI.06096-11 PMID: 22090124
17. Choi Y, Mason CS, Jones LP, Crabtree J, Jorquera PA, Tripp RA. Antibodies to the central conserved region of respiratory syncytial virus (RSV) G protein block RSV G protein CX3C-CX3CR1 binding and cross-neutralize RSV A and B strains. Viral Immunol. 2012; 25(3):193-203. Pub Med Central PMCID: PMCPMC3366338. doi: 10.1089/vim.2011.0094 PMID: 22551066
18. Melero JA, Garcia-Barreno B, Martinez I, Pringle CR, Cane PA. Antigenic structure, evolution and immunobiology of human respiratory syncytial virus attachment (G) protein. J Gen Virol. 1997; 78 (Pt 10):2411-8.
19. Fields BN, Knipe DM, Howley PM. Fields virology. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins Health; 2013.
20. Kim S, Joo DH, Lee JB, Shim BS, Cheon IS, Jang JE, et al. Dual role of respiratory syncytial virus glycoprotein fragment as a mucosal immunogen and chemotactic adjuvant. PLoS One. 2012; 7(2):e32226. Pub Med Central PMCID: PMCPMC3288084. doi: 10.1371/iournal.pone.0032226 PMID: 22384186
21. Chirkova T, Boyoglu-Barnum S, Gaston KA, Malik FM, Trau SP, Oomens AG, et al. Respiratory syncytial virus G protein CX3C motif impairs human airway epithelial and immune cell responses. J Virol. 2013; 87(24):13466-79. Pub Med Central PMCID: PMCPMC3838285. doi: 10.1128/JVI.01741-13 PMID: 24089561
22. Fong AM, Robinson LA, Steeber DA, Tedder TF, Yoshie O, Imai T, et al. Fractalkine and CX3CR1 mediate a novel mechanism of leukocyte capture, firm adhesion, and activation under physiologic flow. J Exp Med. 1998; 188(8):1413-9. Pub Med Central PMCID: PMCPMC2213407. PMID: 9782118
23. Harcourt J, Alvarez R, Jones LP, Henderson C, Anderson LJ, Tripp RA. Respiratory syncytial virus G protein and G protein CX3C motif adversely affect CX3CR1 + T cell responses. J Immunol. 2006; 176 (3):1600-8. PMID: 16424189
24. Tripp RA. Pathogenesis of respiratory syncytial virus infection. Viral Immunol. 2004; 17(2):165-81. doi: 10.1089/0882824041310513 PMID: 15279697
25. Tripp RA, Moore D, Jones L, Sullender W, Winter J, Anderson LJ. Respiratory syncytial virus G and/or SH protein alters Th1 cytokines, natural killer cells, and neutrophils responding to pulmonary infection in BALB/c mice. J Virol. 1999; 73(9):7099-107. Pub Med Central PMCID: PMCPMC104227. PMID: 10438795
26. Kammann M, Laufs J, Schell J, Gronenborn B. Rapid insertional mutagenesis of DNA by polymerase chain reaction (PCR). Nucleic Acids Res. 1989; 17(13):5404. Pub Med Central PMCID: PMCPMC318143. PMID: 2548160
27. Shim BS, Choi YK, Yun CH, Lee EG, Jeon YS, Park SM, et al. Sublingual immunization with M2-based vaccine induces broad protective immunity against influenza. PLoS One. 2011; 6(11):e27953. Pub Med Central PMCID: PMCPMC3227615. doi: 10.1371/iournal.pone.0027953 PMID: 22140491
28. Power UF, Plotnicky-Gilquin H, Goetsch L, Champion T, Beck A, Haeuw JF, et al. Identification and characterisation of multiple linear B cell protectopes in the respiratory syncytial virus G protein. Vaccine. 2001; 19(17-19):2345-51. PMID: 11257359
29. Beatty JD, Beatty BG, Vlahos WG. Measurement of monoclonal antibody affinity by non-competitive enzyme immunoassay. J Immunol Methods. 1987; 100(1-2):173-9. PMID: 2439600
30. Yu JR, Kim S, Lee JB, Chang J. Single intranasal immunization with recombinant adenovirus-based vaccine induces protective immunity against respiratory syncytial virus infection. J Virol. 2008; 82:2350-7. Pub Med Central PMCID: PMCPMC2258907. doi: 10.1128/JVI.02372-07 PMID: 18094185
31. Martinez I, Melero JA. Binding of human respiratory syncytial virus to cells: implication of sulfated cell surface proteoglycans. J Gen Virol. 2000; 81(Pt 11):2715-22. doi: 10.1099/0022-1317-81-11-2715 PMID: 11038384
32. Bueno SM, Gonzalez PA, Pacheco R, Leiva ED, Cautivo KM, Tobar HE, et al. Host immunity during RSV pathogenesis. Int Immunopharmacol. 2008; 8(10):1320-9. doi: 10.1016/i.intimp.2008.03.012 PMID: 18687294
33. Openshaw PJ, Clarke SL, Record FM. Pulmonary eosinophilic response to respiratory syncytial virus infection in mice sensitized to the major surface glycoprotein G. Int Immunol. 1992; 4(4):493-500. PMID: 1591217
34. Johnson TR, Johnson JE, Roberts SR, Wertz GW, Parker RA, Graham BS. Priming with secreted glycoprotein G of respiratory syncytial virus (RSV) augments interleukin-5 production and tissue eosino-philia after RSV challenge. J Virol. 1998; 72(4):2871-80. Pub Med Pub Med Central PMCID: PMCPMC109732. PMID: 9525607
35. Hancock GE, Speelman DJ, Heers K, Bortell E, Smith J, Cosco C. Generation of atypical pulmonary inflammatory responses in BALB/c mice after immunization with the native attachment (G) glycoprotein of respiratory syncytial virus. J Virol. 1996; 70(11):7783-91. Pub Med Central PMCID: PMCPMC190848. PMID: 8892899
36. Levine S, Klaiber-Franco R, Paradiso PR. Demonstration that glycoprotein G is the attachment protein of respiratory syncytial virus. J Gen Virol. 1987; 68 (Pt 9):2521-4.
37. Boyoglu-Barnum S, Gaston KA, Todd SO, Boyoglu C, Chirkova T, Barnum TR, et al. A respiratory syncytial virus (RSV) anti-G protein F(ab')2 monoclonal antibody suppresses mucous production and breathing effort in RSV rA2-line19F-infected BALB/c mice. J Virol. 2013; 87(20):10955-67. Pub Med Central PMCID: PMCPMC3807296. doi: 10.1128/JVI.01164-13 PMID: 23885067
38. Corbeil S, Seguin C, Trudel M. Involvement of the complement system in the protection of mice from challenge with respiratory syncytial virus Long strain following passive immunization with monoclonal antibody 18A2B2. Vaccine. 1996; 14(6):521-5. PMID: 8782350
39. Miao C, Radu GU, Caidi H, Tripp RA, Anderson LJ, Haynes LM. Treatment with respiratory syncytial virus G glycoprotein monoclonal antibody or F(ab')2 components mediates reduced pulmonary inflammation in mice. J Gen Virol. 2009; 90(Pt 5):1119-23 Pub Med Central PMCID: PMCPMC2887562. doi: 10.1099/vir.0.009308-0 PMID: 19264600
40. Stievano L, Piovan E, Amadori A. C and CX3C chemokines: cell sources and physiopathological implications. Crit Rev Immunol. 2004; 24(3):205-28. PMID: 15482255
41. Fraticelli P, Sironi M, Bianchi G, D'Ambrosio D, Albanesi C, Stoppacciaro A, et al. Fractalkine (CX3CL1) as an amplification circuit of polarized Th1 responses. J Clin Invest. 2001; 107(9):1173-81. Pub Med Central PMCID: PMCPMC209276. doi: 10.1172/JCI11517 PMID: 11342581
42. Boyoglu-Barnum S, Chirkova T, Todd SO, Barnum TR, Gaston KA, Jorquera P, et al. Prophylaxis with a respiratory syncytial virus (RSV) anti-G protein monoclonal antibody shifts the adaptive immune response to RSV rA2-line19F infection from Th2toTh1 in BALB/c mice. J Virol. 2014; 88(18):10569-83. Pub Med Central PMCID: PMCPMC4178873. doi: 10.1128/JVI.01503-14 PMID: 24990999
43. Johnson SM, Mc Nally BA, Ioannidis I, Flano E, Teng MN, Oomens AG, et al. Respiratory Syncytial Virus Uses CX3CR1 as a Receptor on Primary Human Airway Epithelial Cultures. PLoS Pathog. 2015; 11(12):e1005318. Pub Med Central PMCID: PMCPMC4676609. doi: 10.1371/iournal.ppat.1005318 PMID: 26658574