Heterosubtypic protection conferred by the human monoclonal antibody PN-SIA28 against influenza A virus lethal infections in mice

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 5, 2015, Pages 2647-2653

  Retamal, Miguel ^a   Abed, Yacine ^a   Rhéaume, Chantal ^a   Cappelletti, Francesca ^b   Clementi, Nicola ^b   Mancini, Nicasio ^b   Clementi, Massimo ^b   Burioni, Roberto ^b   Boivin, Guy ^a  

^a LAVAL UNIVERSITY   (Canada)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HUMAN MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY PN SIA28; UNCLASSIFIED DRUG; ANTIVIRUS AGENT; MONOCLONAL ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ARTICLE; BINDING AFFINITY; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; IMMUNOTHERAPY; IN VIVO STUDY; INFLUENZA A (H1N1); INFLUENZA A (H3N2); LETHAL DOSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; WEIGHT GAIN; WEIGHT REDUCTION; ANIMAL; BAGG ALBINO MOUSE; DRUG EFFECTS; HUMAN; INFLUENZA A VIRUS; INFLUENZA, HUMAN; ORTHOMYXOVIRIDAE INFECTIONS; PATHOGENICITY;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIVIRAL AGENTS; FEMALE; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE INFECTIONS;

EID: 84931274816     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00118-15     Document Type: Article

References (34)

1. Fouchier RA, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus AD. 2005. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 79:2814-2822. http://dx.doi.org/10.1128/JVI.79.5.2814-2822.2005.
2. Reid AH, Fanning TG, Janczewski TA, Taubenberger JK. 2000. Characterization of the 1918 Spanish influenza virus neuraminidase gene. Proc Natl Acad Sci U S A 97:6785-6790. http://dx.doi.org/10.1073/pnas.100140097.
3. Viboud C, Grais RF, Lafont BA, Miller MA, Simonsen L. 2005. Multinational impact of the 1968 Hong Kong influenza pandemic: evidence for a smoldering pandemic. J Infect Dis 192:233-248. http://dx.doi.org/10.1086/431150.
4. WHO. 2014. Recommended composition of influenza virus vaccines for use in the 2015 southern hemisphere influenza season. Wkly Epidemiol Rec 89:441-452.
5. CDC. 2014. Selecting the viruses in the seasonal influenza (flu) vaccine. CDC, Atlanta, GA. http://www.cdc.gov/flu/professionals/vaccination/virusqa.htm.
6. Halder N, Kelso JK, Milne GJ. 2014. A model-based economic analysis of pre-pandemic influenza vaccination cost-effectiveness. BMC Infect Dis 14:266. http://dx.doi.org/10.1186/1471-2334-14-266.
7. Cheung CL, Rayner JM, Smith GJ, Wang P, Naipospos TS, Zhang J, Yuen KY, Webster RG, Peiris JS, Guan Y, Chen H. 2006. Distribution of amantadine-resistant H5N1 avian influenza variants in Asia. J Infect Dis 193:1626-1629. http://dx.doi.org/10.1086/504723.
8. Bright RA, Shay DK, Shu B, Cox NJ, Klimov AI. 2006. Adamantane resistance among influenza A viruses isolated early during the 2005-2006 influenza season in the United States. JAMA 295:891-894. http://dx.doi.org/10.1001/jama.295.8.joc60020.
9. CDC. 2009. Oseltamivir-resistant 2009 pandemic influenza A (H1N1) virus infection in two summer campers receiving prophylaxis - North Carolina, 2009. MMWR Morb Mortal Wkly Rep 58:969-972.
10. Hurt AC, Chotpitayasunondh T, Cox NJ, Daniels R, Fry AM, Gubareva LV, Hayden FG, Hui DS, Hungnes O, Lackenby A, Lim W, Meijer A, Penn C, Tashiro M, Uyeki TM, Zambon M. 2012. Antiviral resistance during the 2009 influenza A H1N1 pandemic: public health, laboratory, and clinical perspectives. Lancet Infect Dis 12:240-248. http://dx.doi.org/10.1016/S1473-3099(11)70318-8.
11. Kiso M, Mitamura K, Sakai-Tagawa Y, Shiraishi K, Kawakami C, Kimura K, Hayden FG, Sugaya N, Kawaoka Y. 2004. Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet 364:759-765. http://dx.doi.org/10.1016/S0140-6736(04)16934-1.
12. Eshaghi A, Shalhoub S, Rosenfeld P, Li A, Higgins RR, Stogios PJ, Savchenko A, Bastien N, Li Y, Rotstein C, Gubbay JB. 2014. Multiple influenza A (H3N2) mutations conferring resistance to neuraminidase inhibitors in a bone marrow transplant recipient. Antimicrob Agents Chemother 58:7188-7197. http://dx.doi.org/10.1128/AAC.03667-14.
13. Ren J, Ellis J, Li J. 2014. Influenza A HA's conserved epitopes and broadly neutralizing antibodies: a prediction method. J Bioinform Comput Biol 12:1450023. http://dx.doi.org/10.1142/S0219720014500231.
14. Krystal M, Elliott RM, Benz EW, Jr, Young JF, Palese P. 1982. Evolution of influenza A and B viruses: conservation of structural features in the hemagglutinin genes. Proc Natl Acad Sci USA79:4800-4804. http://dx.doi.org/10.1073/pnas.79.15.4800.
15. De Marco D, Clementi N, Mancini N, Solforosi L, Moreno GJ, Sun X, Tumpey TM, Gubareva LV, Mishin V, Clementi M, Burioni R. 2012. A non-VH1-69 heterosubtypic neutralizing human monoclonal antibody protects mice against H1N1 and H5N1 viruses. PLoS One 7:e34415. http://dx.doi.org/10.1371/journal.pone.0034415.
16. Clementi N, De Marco D, Mancini N, Solforosi L, Moreno GJ, Gubareva LV, Mishin V, Di Pietro A, Vicenzi E, Siccardi AG, Clementi M, Burioni R. 2011. A human monoclonal antibody with neutralizing activity against highly divergent influenza subtypes. PLoS One 6:e28001. http://dx.doi.org/10.1371/journal.pone.0028001.
17. Canadian Council on Animal Care (CCAC). 2014. Standards and Guidance from CCAC. Canadian Council on Animal Care, Ottawa, Ontario, Canada. http://www.ccac.ca/en-/standards.
18. Burioni R, Canducci F, Mancini N, Clementi N, Sassi M, De Marco D, Diotti RA, Saita D, Sampaolo M, Sautto G, Pianezze M, Clementi M. 2010. Monoclonal antibodies isolated from human B cells neutralize a broad range of H1 subtype influenza A viruses, including swine-origin influenza virus (S-OIV). Virology 399:144-152. http://dx.doi.org/10.1016/j.virol.2009.12.014.
19. Burioni R, Canducci F, Mancini N, Clementi N, Sassi M, De Marco D, Saita D, Diotti RA, Sautto G, Sampaolo M, Clementi M. 2009. Molecular cloning of the first human monoclonal antibodies neutralizing with high potency swine-origin influenza A pandemic virus (S-OIV). New Microbiol 32:319-324. http://dx.doi.org/10.1016/j.virol.2009.12.014.
20. Sautto G, Mancini N, Diotti RA, Solforosi L, Clementi M, Burioni R. 2012. Anti-hepatitis C virus E2 (HCV/E2) glycoprotein monoclonal antibodies and neutralization interference. Antiviral Res 96:82-89. http://dx.doi.org/10.1016/j.antiviral.2012.07.013.
21. Perotti M, Mancini N, Diotti RA, Tarr AW, Ball JK, Owsianka A, Adair R, Patel AH, Clementi M, Burioni R. 2008. Identification of a broadly cross-reacting and neutralizing human monoclonal antibody directed against the hepatitis C virus E2 protein. J Virol 82:1047-1052. http://dx.doi.org/10.1128/JVI.01986-07.
22. Abed Y, Goyette N, Boivin G. 2004. A reverse genetics study of resistance to neuraminidase inhibitors in an influenza A/H1N1 virus. Antivir Ther 9:577-581.
23. Pizzorno A, Abed Y, Plante PL, Carbonneau J, Baz M, Hamelin ME, Corbeil J, Boivin G. 2014. Evolution of oseltamivir resistance mutations in influenza A(H1N1) and A(H3N2) viruses during selection in experimentally infected mice. Antimicrob Agents Chemother 58:6398-6405. http://dx.doi.org/10.1128/AAC.02956-14.
24. Pizzorno A, Bouhy X, Abed Y, Boivin G. 2011. Generation and characterization of recombinant pandemic influenza A (H1N1) viruses resistant to neuraminidase inhibitors. J Infect Dis 203:25-31. http://dx.doi.org/10.1093/infdis/jiq010.
25. Hatakeyama S, Sakai-Tagawa Y, Kiso M, Goto H, Kawakami C, Mitamura K, Sugaya N, Suzuki Y, Kawaoka Y. 2005. Enhanced expression of an alpha2,6-linked sialic acid on MDCK cells improves isolation of human influenza viruses and evaluation of their sensitivity to a neuraminidase inhibitor. J Clin Microbiol 43:4139-4146. http://dx.doi.org/10.1128/JCM.43.8.4139-4146.2005.
26. Pan W, Dong Z, Li F, Meng W, Feng L, Niu X, Li C, Luo Q, Li Z, Sun C, Chen L. 2013. Visualizing influenza virus infection in living mice. Nat Commun 4:2369. http://dx.doi.org/10.1038/ncomms3369.
27. Itoh Y, Shinya K, Kiso M, Watanabe T, Sakoda Y, Hatta M, Muramoto Y, Tamura D, Sakai-Tagawa Y, Noda T, Sakabe S, Imai M, Hatta Y, Watanabe S, Li C, Yamada S, Fujii K, Murakami S, Imai H, Kakugawa S, Ito M, Takano R, Iwatsuki-Horimoto K, Shimojima M, Horimoto T, Goto H, Takahashi K, Makino A, Ishigaki H, Nakayama M, Okamatsu M, Warshauer D, Shult PA, Saito R, Suzuki H, Furuta Y, Yamashita M, Mitamura K, Nakano K, Nakamura M, Brockman-Schneider R, Mitamura H, Yamazaki M, Sugaya N, Suresh M, Ozawa M, Neumann G, Gern J, Kida H, Ogasawara K, Kawaoka Y. 2009. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 460:1021-1025. http://dx.doi.org/10.1038/nature08260.
28. Nabel GJ, Fauci AS. 2010. Induction of unnatural immunity: prospects for a broadly protective universal influenza vaccine. Nat Med 16:1389-1391. http://dx.doi.org/10.1038/nm1210-1389.
29. Margine I, Hai R, Albrecht RA, Obermoser G, Harrod AC, Banchereau J, Palucka K, Garcia-Sastre A, Palese P, Treanor JJ, Krammer F. 2013. H3N2 influenza virus infection induces broadly reactive hemagglutinin stalk antibodies in humans and mice. J Virol 87:4728-4737. http://dx.doi.org/10.1128/JVI.03509-12.
30. Ekiert DC, Friesen RH, Bhabha G, Kwaks T, Jongeneelen M, Yu W, Ophorst C, Cox F, Korse HJ, Brandenburg B, Vogels R, Brakenhoff JP, Kompier R, Koldijk MH, Cornelissen LA, Poon LL, Peiris M, Koudstaal W, Wilson IA, Goudsmit J. 2011. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333:843-850. http://dx.doi.org/10.1126/science.1204839.
31. Corti D, Suguitan AL, Jr, Pinna D, Silacci C, Fernandez-Rodriguez BM, Vanzetta F, Santos C, Luke CJ, Torres-Velez FJ, Temperton NJ, Weiss RA, Sallusto F, Subbarao K, Lanzavecchia A. 2010. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J Clin Invest 120:1663-1673. http://dx.doi.org/10.1172/JCI41902.
32. Wang TT, Tan GS, Hai R, Pica N, Petersen E, Moran TM, Palese P. 2010. Broadly protective monoclonal antibodies against H3 influenza viruses following sequential immunization with different hemagglutinins. PLoS Pathog 6:e1000796. http://dx.doi.org/10.1371/journal.ppat.1000796.
33. Matsuoka Y, Lamirande EW, Subbarao K. 2009. The mouse model for influenza. Curr Protoc Microbiol 15:15G.3. http://dx.doi.org/10.1002/9780471729259.mc15g03s13.
34. Pizzorno A, Abed Y, Rheaume C, Boivin G. 2014. Oseltamivirzanamivir combination therapy is not superior to zanamivir monotherapy in mice infected with influenza A (H3N2) and A (H1N1) pdm09 viruses. Antiviral Res 105:54-58. http://dx.doi.org/10.1016/j.antiviral.2014.02.017.