A highly potent and broadly neutralizing H1 influenza-specific human monoclonal antibody

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Nogales, Aitor ^a   Piepenbrink, Michael S ^b   Wang, Jiong ^b   Ortega, Sandra ^a   Basu, Madhubanti ^b   Fucile, Christopher F ^c   Treanor, John J ^b   Rosenberg, Alexander F ^c   Zand, Martin S ^b   Keefer, Michael C ^b   Martinez Sobrido, Luis ^a   Kobie, James J ^b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VACCINE; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY;

ANIMAL; HUMAN; HUMORAL IMMUNITY; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); MORTALITY; MOUSE; ORTHOMYXOVIRUS INFECTION; SPECIES DIFFERENCE; SURVIVAL RATE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; HUMANS; IMMUNITY, HUMORAL; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; MICE; ORTHOMYXOVIRIDAE INFECTIONS; SPECIES SPECIFICITY; SURVIVAL RATE;

EID: 85045002424     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-22307-8     Document Type: Article

References (75)

1. Girard, M. P., Cherian, T., Pervikov, Y. & Kieny, M. P. A review of vaccine research and development: human acute respiratory infections. Vaccine 23, 5708-5724, https://doi.org/10.1016/j.vaccine.2005.07.046 (2005).
2. Nogales, A. & Martinez-Sobrido, L. Reverse Genetics Approaches for the Development of Influenza Vaccines. Int J Mol Sci 18, https://doi.org/10.3390/ijms18010020 (2016).
3. Dushoff, J., Plotkin, J. B., Viboud, C., Earn, D. J. & Simonsen, L. Mortality due to influenza in the United States-an annualized regression approach using multiple-cause mortality data. Am J Epidemiol 163, 181-187, https://doi.org/10.1093/aje/kwj024 (2006).
4. Doshi, P. Trends in recorded influenza mortality: United States, 1900-2004. Am J Public Health 98, 939-945, https://doi.org/10.2105/AJPH.2007.119933(2008).
5. Thompson, W. W. et al. Estimating influenza-associated deaths in the United States. Am J Public Health 99(Suppl 2), S225-S230, https://doi.org/10.2105/AJPH.2008.151944 (2009).
6. Molinari, N. A. et al. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine 25, 5086-5096, https://doi.org/10.1016/j.vaccine.2007.03.046 (2007).
7. Gasparini, R., Amicizia, D., Lai, P. L. & Panatto, D. Clinical and socioeconomic impact of seasonal and pandemic influenza in adults and the elderly. Hum Vaccin Immunother 8, 21-28, https://doi.org/10.4161/hv.8.1.17622 (2012).
8. Keech, M. & Beardsworth, P. The impact of influenza on working days lost: A review of the literature. Pharmacoeconomics 26, 911-924 (2008).
9. Taubenberger, J. K. & Morens, D. M. 1918 Influenza: The mother of all pandemics. Emerg Infect Dis 12, 15-22, https://doi.org/10.3201/eid1201.050979 (2006).
10. Smith, G. J. et al. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459, 1122-1125, https://doi.org/10.1038/nature08182 (2009).
11. Kilbourne, E. D. Influenza pandemics of the 20th century. Emerg Infect Dis 12, 9-14, https://doi.org/10.3201/eid1201.051254 (2006).
12. Centers for Disease, C. & Prevention. Update: infections with a swine-origin influenza A (H1N1) virus-United States and other countries, April 28, 2009. MMWR Morb Mortal Wkly Rep 58, 431-433 (2009).
13. Beigel, J. & Bray, M. Current and future antiviral therapy of severe seasonal and avian influenza. Antiviral Res 78, 91-102, https://doi.org/10.1016/j.antiviral.2008.01.003 (2008).
14. Garcia-Sastre, A. Antiviral response in pandemic influenza viruses. Emerg Infect Dis 12, 44-47, https://doi.org/10.3201/eid1201.051186 (2006).
15. Marathe, B. M. et al. Combinations of Oseltamivir and T-705 Extend the Treatment Window for Highly Pathogenic Influenza A(H5N1) Virus Infection in Mice. Sci Rep 6, 26742, https://doi.org/10.1038/srep26742 (2016).
16. Reichert, J. M. Antibodies to watch in 2017. MAbs 9, 167-181, https://doi.org/10.1080/19420862.2016.1269580 (2017).
17. Catapano, A. L. & Papadopoulos, N. The safety of therapeutic monoclonal antibodies: implications for cardiovascular disease and targeting the PCSK9 pathway. Atherosclerosis 228, 18-28, https://doi.org/10.1016/j.atherosclerosis.2013.01.044 (2013).
18. Singh, J. A. et al. Adverse effects of biologics: A network meta-analysis and Cochrane overview. Cochrane Database Syst Rev, CD008794, https://doi.org/10.1002/14651858.CD008794.pub2 (2011).
19. Shriver, Z., Trevejo, J. M. & Sasisekharan, R. Antibody-Based Strategies to Prevent and Treat Influenza. Front Immunol 6, 315, https://doi.org/10.3389/fimmu.2015.00315 (2015).
20. Sparrow, E., Friede, M., Sheikh, M., Torvaldsen, S. & Newall, A. T. Passive immunization for influenza through antibody therapies, a review of the pipeline, challenges and potential applications. Vaccine 34, 5442-5448, https://doi.org/10.1016/j.vaccine.2016.08.057 (2016).
21. Krause, J. C. et al. A broadly neutralizing human monoclonal antibody that recognizes a conserved, novel epitope on the globular head of the influenza H1N1 virus hemagglutinin. J Virol 85, 10905-10908, https://doi.org/10.1128/JVI.00700-11 (2011).
22. Tsibane, T. et al. Influenza human monoclonal antibody 1F1 interacts with three major antigenic sites and residues mediating human receptor specificity in H1N1 viruses. PLoS Pathog 8, e1003067, https://doi.org/10.1371/journal.ppat.1003067 (2012).
23. Whittle, J. R. et al. Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc Natl Acad Sci USA 108, 14216-14221, https://doi.org/10.1073/pnas.1111497108 (2011).
24. Sui, J. et al. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 16, 265-273, https://doi.org/10.1038/nsmb.1566(2009).
25. Ekiert, D. C. et al. Antibody recognition of a highly conserved influenza virus epitope. Science 324, 246-251, https://doi.org/10.1126/science.1171491 (2009).
26. Ekiert, D. C. et al. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333, 843-850, https://doi.org/10.1126/science.1204839 (2011).
27. Henry Dunand, C. J. et al. Preexisting human antibodies neutralize recently emerged H7N9 influenza strains. J Clin Invest 125, 1255-1268, https://doi.org/10.1172/JCI74374 (2015).
28. Corti, D. et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333, 850-856, https://doi.org/10.1126/science.1205669 (2011).
29. Kallewaard, N. L. et al. Structure and Function Analysis of an Antibody Recognizing All Influenza A Subtypes. Cell 166, 596-608, https://doi.org/10.1016/j.cell.2016.05.073 (2016).
30. Fu, Y. et al. A broadly neutralizing anti-influenza antibody reveals ongoing capacity of haemagglutinin-specific memory B cells to evolve. Nat Commun 7, 12780, https://doi.org/10.1038/ncomms12780 (2016).
31. Tharakaraman, K. et al. A broadly neutralizing human monoclonal antibody is effective against H7N9. Proc Natl Acad Sci USA 112, 10890-10895, https://doi.org/10.1073/pnas.1502374112 (2015).
32. Dreyfus, C. et al. Highly conserved protective epitopes on influenza B viruses. Science 337, 1343-1348, https://doi.org/10.1126/science.1222908 (2012).
33. Laursen, N. S. & Wilson, I. A. Broadly neutralizing antibodies against influenza viruses. Antiviral Res 98, 476-483, https://doi.org/10.1016/j.antiviral.2013.03.021 (2013).
34. Neu, K. E., Henry Dunand, C. J. & Wilson, P. C. Heads, stalks and everything else: how can antibodies eradicate influenza as a human disease? Curr Opin Immunol 42, 48-55, https://doi.org/10.1016/j.coi.2016.05.012 (2016).
35. Margine, I. et al. Hemagglutinin stalk-based universal vaccine constructs protect against group 2 influenza A viruses. J Virol 87, 10435-10446, https://doi.org/10.1128/JVI.01715-13 (2013).
36. Gonzalez-Garcia, I., Ocana, E., Jimenez-Gomez, G., Campos-Caro, A. & Brieva, J. A. Immunization-induced perturbation of human blood plasma cell pool: progressive maturation, IL-6 responsiveness, and high PRDI-BF1/BLIMP1 expression are critical distinctions between antigen-specific and nonspecific plasma cells. J Immunol 176, 4042-4050 (2006).
37. Wang, J. et al. Multi-Dimensional Measurement of Antibody-Mediated Heterosubtypic Immunity to Influenza. PLoS One 10, e0129858, https://doi.org/10.1371/journal.pone.0129858 (2015).
38. Nogales, A. et al. Replication-competent fluorescent-expressing influenza B virus. Virus Res 213, 69-81, https://doi.org/10.1016/j.virusres.2015.11.014 (2016).
39. Nogales, A., Baker, S. F. & Martinez-Sobrido, L. Replication-competent influenza A viruses expressing a red fluorescent protein. Virology 476, 206-216, https://doi.org/10.1016/j.virol.2014.12.006 (2015).
40. Pica, N. et al. The DBA.2 mouse is susceptible to disease following infection with a broad, but limited, range of influenza A and B viruses. J Virol 85, 12825-12829, https://doi.org/10.1128/JVI.05930-11 (2011).
41. Nogales, A. et al. Influenza A Virus Attenuation by Codon Deoptimization of the NS Gene for Vaccine Development. J Virol 88, 10525-10540, https://doi.org/10.1128/JVI.01565-14 (2014).
42. Rozo, M. & Gronvall, G. K. The Reemergent 1977 H1N1 Strain and the Gain-of-Function Debate. MBio 6, https://doi.org/10.1128/mBio.01013-15 (2015).
43. Ren, H. & Zhou, P. Epitope-focused vacc ine design against influenza A and B viruses. Curr Opin Immunol 42, 83-90, https://doi. org/10.1016/j.coi.2016.06.002 (2016).
44. Lee, P. S. et al. Heterosubtypic antibody recognition of the influenza virus hemagglutinin receptor binding site enhanced by avidity. Proc Natl Acad Sci USA 109, 17040-17045, https://doi.org/10.1073/pnas.1212371109 (2012).
45. Yoshida, R. et al. Cross-protective potential of a novel monoclonal antibody directed against antigenic site B of the hemagglutinin of influenza A viruses. PLoS Pathog 5, e1000350, https://doi.org/10.1371/journal.ppat.1000350 (2009).
46. Ekiert, D. C. et al. Cross-neutralization of influenza A viruses mediated by a single antibody loop. Nature 489, 526-532, https://doi.org/10.1038/nature11414 (2012).
47. Yu, X. et al. Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature 455, 532-536, https://doi.org/10.1038/nature07231 (2008).
48. Heaton, N. S. et al. In vivo bioluminescent imaging of influenza a virus infection and characterization of novel cross-protective monoclonal antibodies. J Virol 87, 8272-8281, https://doi.org/10.1128/JVI.00969-13 (2013).
49. Wang, S. F. et al. Generation and characterization of new monoclonal antibodies against swine origin 2009 influenza A (H1N1) virus and evaluation of their prophylactic and therapeutic efficacy in a mouse model. Dev Comp Immunol. https://doi.org/10.1016/j.dci.2016.10.010 (2016).
50. Marjuki, H. et al. Human Monoclonal Antibody 81.39a Effectively Neutralizes Emerging Influenza A Viruses of Group 1 and 2 Hemagglutinins. J Virol 90, 10446-10458, https://doi.org/10.1128/JVI.01284-16 (2016).
51. Song, A. et al. Evaluation of a fully human monoclonal antibody against multiple influenza A viral strains in mice and a pandemic H1N1 strain in nonhuman primates. Antiviral Res 111, 60-68, https://doi.org/10.1016/j.antiviral.2014.08.016 (2014).
52. DiLillo, D. J., Tan, G. S., Palese, P. & Ravetch, J. V. Broadly neutralizing hemagglutinin stalk-specific antibodies require FcgammaR interactions for protection against influenza virus in vivo. Nat Med 20, 143-151, https://doi.org/10.1038/nm.3443 (2014).
53. Wrammert, J. et al. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 208, 181-193, https://doi.org/10.1084/jem.20101352 (2011).
54. Xu, R. et al. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 328, 357-360, https://doi. org/10.1126/science.1186430 (2010).
55. Krause, J. C. et al. Naturally occurring human monoclonal antibodies neutralize both 1918 and 2009 pandemic influenza A (H1N1) viruses. J Virol 84, 3127-3130, https://doi.org/10.1128/JVI.02184-09 (2010).
56. Cho, K. J. et al. Insight into highly conserved H1 subtype-specific epitopes in influenza virus hemagglutinin. PLoS One 9, e89803, https://doi.org/10.1371/journal.pone.0089803 (2014).
57. Chai, N. et al. A broadly protective therapeutic antibody against influenza B virus with two mechanisms of action. Nat Commun 8, 14234, https://doi.org/10.1038/ncomms14234 (2017).
58. Srivastava, V. et al. Identification of dominant antibody-dependent cell-mediated cytotoxicity epitopes on the hemagglutinin antigen of pandemic H1N1 influenza virus. J Virol 87, 5831-5840, https://doi.org/10.1128/JVI.00273-13 (2013).
59. DiLillo, D. J., Palese, P., Wilson, P. C. & Ravetch, J. V. Broadly neutralizing anti-influenza antibodies require Fc receptor engagement for in vivo protection. J Clin Invest 126, 605-610, https://doi.org/10.1172/JCI84428 (2016).
60. Nogales, A. et al. Replication-competent fluorescent-expressing influenza B virus. Virus Res 213, 69-81, https://doi.org/10.1016/j.virusres.2015.11.014 (2015).
61. Nogales, A., Baker, S. F. & Martinez-Sobrido, L. Replication-competent influenza A viruses expressing a red fluorescent protein. Virology 476C, 206-216, https://doi.org/10.1016/j.virol.2014.12.006 (2014).
62. Martinez-Sobrido, L. & Garcia-Sastre, A. Generation of recombinant influenza virus from plasmid DNA. Journal of visualized experiments: JoVE, https://doi.org/10.3791/2057 (2010).
63. Kobie, J. J. et al. Functional and Molecular Characteristics of Novel and Conserved Cross-Clade HIV Envelope Specific Human Monoclonal Antibodies. Monoclon Antib Immunodiagn Immunother 34, 65-72, https://doi.org/10.1089/mab.2014.0064 (2015).
64. Tiller, T. et al. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J Immunol Methods 329, 112-124, https://doi.org/10.1016/j.jim.2007.09.017 (2008).
65. Scheid, J. F. et al. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333, 1633-1637, https://doi.org/10.1126/science.1207227 (2011).
66. Richardson, C. et al. Molecular basis of 9G4 B cell autoreactivity in human systemic lupus erythematosus. J Immunol 191, 4926-4939, https://doi.org/10.4049/jimmunol.1202263 (2013).
67. Tipton, C. M. et al. Diversity, cellular origin and autoreactivity of antibody-secreting cell population expansions in acute systemic lupus erythematosus. Nat Immunol 16, 755-765, https://doi.org/10.1038/ni.3175 (2015).
68. Aouinti, S. et al. IMGT/StatClonotype for Pairwise Evaluation and Visualization of NGS IG and TR IMGT Clonotype (AA) Diversity or Expression from IMGT/HighV-QUEST. Front Immunol 7, 339, https://doi.org/10.3389/fimmu.2016.00339 (2016).
69. Felsenstein, J. PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle (2005).
70. Myszka, D. G. Improving biosensor analysis. J Mol Recognit 12, 279-284, https://doi.org/10.1002/(SICI)1099-1352(199909/10)12:5<279::AID-JMR473>3.0.CO;2-3 (1999).
71. National Research Council (U.S.). Committee for the Update of the Guide for the Care and Use of Laboratory Animals., Institute for Laboratory Animal Research (U.S.) & National Academies Press (U.S.). Guide for the care and use of laboratory animals. 8th edn, (National Academies Press, 2011).
72. Nogales, A., DeDiego, M. L., Topham, D. J. & Martinez-Sobrido, L. Rearrangement of Influenza Virus Spliced Segments for the Development of Live-Attenuated Vaccines. J Virol 90, 6291-6302, https://doi.org/10.1128/JVI.00410-16 (2016).
73. Baker, S. F. et al. Protection against lethal influenza with a viral mimic. J Virol 87, 8591-8605, https://doi.org/10.1128/JVI.01081-13 (2013).
74. Niwa, H., Yamamura, K. & Miyazaki, J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199 (1991).
75. Manicassamy, B. et al. Protection of mice against lethal challenge with 2009 H1N1 influenza A virus by 1918-like and classical swine H1N1 based vaccines. PLoS Pathog 6, e1000745, https://doi.org/10.1371/journal.ppat.1000745 (2010).