Complete mapping of viral escape from neutralizing antibodies

PLoS Pathogens

Volumn 13, Issue 3, 2017, Pages

  Doud, Michael B ^a,b   Hensley, Scott E ^c   Bloom, Jesse D ^a,b  

^a USA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; GREEN FLUORESCENT PROTEIN; HEMAGGLUTININ; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; VIRAL PROTEIN; INFLUENZA VIRUS HEMAGGLUTININ; VIRUS ANTIBODY; VIRUS ANTIGEN;

ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ESCAPE BEHAVIOR; GENETIC VARIATION; HIGH THROUGHPUT SCREENING; INFLUENZA; INFLUENZA VIRUS; MUTATION RATE; MUTATIONAL ANALYSIS; NONHUMAN; POINT MUTATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; VIRUS IMMUNITY; VIRUS MUTATION; VIRUS NEUTRALIZATION; VIRUS REPLICATION; GENETICS; HIGH THROUGHPUT SEQUENCING; IMMUNE EVASION; IMMUNOLOGY; MUTATION; ORTHOMYXOVIRIDAE; SERODIAGNOSIS;

ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; GENETIC VARIATION; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; IMMUNE EVASION; MUTATION; NEUTRALIZATION TESTS; ORTHOMYXOVIRIDAE;

EID: 85016515562     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006271     Document Type: Article

References (54)

1. Wiley DC, Skehel JJ, The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annual Review of Biochemistry. 1987;56(1):365–394. doi: 10.1146/annurev.bi.56.070187.0020533304138
2. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD, et al. Mapping the Antigenic and Genetic Evolution of Influenza Virus. Science. 2004;305(5682):371–376. doi: 10.1126/science.109721115218094
3. Bedford T, Riley S, Barr IG, Broor S, Chadha M, Cox NJ, et al. Global circulation patterns of seasonal influenza viruses vary with antigenic drift. Nature. 2015;523(7559):217–220. doi: 10.1038/nature1446026053121
4. Łuksza M, Lässig M, A predictive fitness model for influenza. Nature. 2014;507(7490):57–61. doi: 10.1038/nature1308724572367
5. Neher RA, Bedford T, nextflu: real-time tracking of seasonal influenza virus evolution in humans. Bioinformatics. 2015;31(21):3546–3548. doi: 10.1093/bioinformatics/btv38126115986
6. Balazs AB, Chen J, Hong CM, Rao DS, Yang L, Baltimore D, Antibody-based protection against HIV infection by vectored immunoprophylaxis. Nature. 2012;481(7379):81–84. doi: 10.1038/nature10660
7. Ledgerwood J, Coates E, Yamshchikov G, Saunders J, Holman L, Enama M, et al. Safety, pharmacokinetics and neutralization of the broadly neutralizing HIV-1 human monoclonal antibody VRC01 in healthy adults. Clinical & Experimental Immunology. 2015;182(3):289–301. doi: 10.1111/cei.12692
8. Hedestam GBK, Fouchier RA, Phogat S, Burton DR, Sodroski J, Wyatt RT, The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nature Reviews Microbiology. 2008;6(2):143–155. doi: 10.1038/nrmicro1819
9. Krammer F, Palese P, Advances in the development of influenza virus vaccines. Nature Reviews Drug Discovery. 2015;14(3):167–182. doi: 10.1038/nrd452925722244
10. Webster R, Laver W, Determination of the number of nonoverlapping antigenic areas on Hong Kong (H3N2) influenza virus hemagglutinin with monoclonal antibodies and the selection of variants with potential epidemiological significance. Virology. 1980;104(1):139–148. doi: 10.1016/0042-6822(80)90372-46156537
11. Gerhard W, Yewdell J, Frankel ME, Webster R, Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies. Nature. 1981;290(5808):713–717. doi: 10.1038/290713a06163993
12. Caton AJ, Brownlee GG, Yewdell JW, Gerhard W, The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell. 1982;31(2):417–427. doi: 10.1016/0092-8674(82)90135-06186384
13. Pantophlet R, Saphire EO, Poignard P, Parren PW, Wilson IA, Burton DR, Fine mapping of the interaction of neutralizing and nonneutralizing monoclonal antibodies with the CD4 binding site of human immunodeficiency virus type 1 gp120. Journal of Virology. 2003;77(1):642–658. doi: 10.1128/JVI.77.1.642-658.200312477867
14. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, Goss JL, et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science. 2009;326(5950):285–289. doi: 10.1126/science.117874619729618
15. Pierce BG, Keck ZY, Lau P, Fauvelle C, Gowthaman R, Baumert TF, et al. Global mapping of antibody recognition of the hepatitis C virus E2 glycoprotein: Implications for vaccine design. Proceedings of the National Academy of Sciences. 2016; p. E6946–E6954. doi: 10.1073/pnas.1614942113
16. Verschoor CP, Singh P, Russell ML, Bowdish DM, Brewer A, Cyr L, et al. Microneutralization assay titres correlate with protection against seasonal influenza H1N1 and H3N2 in children. PloS One. 2015;10(6):e0131531. doi: 10.1371/journal.pone.013153126107625
17. Polonis VR, Brown BK, Borges AR, Zolla-Pazner S, Dimitrov DS, Zhang MY, et al. Recent advances in the characterization of HIV-1 neutralization assays for standardized evaluation of the antibody response to infection and vaccination. Virology. 2008;375(2):315–320. doi: 10.1016/j.virol.2008.02.00718367229
18. Chai N, Swem LR, Reichelt M, Chen-Harris H, Luis E, Park S, et al. Two escape mechanisms of influenza A virus to a broadly neutralizing stalk-binding antibody. PLoS Pathogens. 2016;12(6):e1005702. doi: 10.1371/journal.ppat.100570227351973
19. Zhang M, Gaschen B, Blay W, Foley B, Haigwood N, Kuiken C, et al. Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology. 2004;14(12):1229–1246. doi: 10.1093/glycob/cwh10615175256
20. Munro JB, Gorman J, Ma X, Zhou Z, Arthos J, Burton DR, et al. Conformational dynamics of single HIV-1 envelope trimers on the surface of native virions. Science. 2014;346(6210):759–763. doi: 10.1126/science.125442625298114
21. Jin L, Fendly BM, Wells JA, High resolution functional analysis of antibody-antigen interactions. Journal of Molecular Biology. 1992;226(3):851–865. doi: 10.1016/0022-2836(92)90636-X1380563
22. Muller YA, Chen Y, Christinger HW, Li B, Cunningham BC, Lowman HB, et al. VEGF and the Fab fragment of a humanized neutralizing antibody: crystal structure of the complex at 2.4 Å resolution and mutational analysis of the interface. Structure. 1998;6(9):1153–1167. doi: 10.1016/S0969-2126(98)00116-69753694
23. Dall’Acqua W, Goldman ER, Lin W, Teng C, Tsuchiya D, Li H, et al. A mutational analysis of binding interactions in an antigen-antibody protein-protein complex. Biochemistry. 1998;37(22):7981–7991. doi: 10.1021/bi980148j9609690
24. Pons J, Rajpal A, Kirsch JF, Energetic analysis of an antigen/antibody interface: alanine scanning mutagenesis and double mutant cycles on the HyHEL-10/lysozyme interaction. Protein Science. 1999;8(05):958–968. doi: 10.1110/ps.8.5.95810338006
25. Cunningham BC, Wells JA, Comparison of a structural and a functional epitope. Journal of Molecular Biology. 1993;234(3):554–563. doi: 10.1006/jmbi.1993.16117504735
26. Clackson T, Wells JA, A hot spot of binding energy in a hormone-receptor interface. Science. 1995;267(5196):383. doi: 10.1126/science.75299407529940
27. Bogan AA, Thorn KS, Anatomy of hot spots in protein interfaces. Journal of Molecular Biology. 1998;280(1):1–9. doi: 10.1006/jmbi.1998.18439653027
28. Firnberg E, Ostermeier M, PFunkel: efficient, expansive, user-defined mutagenesis. PLoS One. 2012;7(12):e52031. doi: 10.1371/journal.pone.005203123284860
29. Kitzman JO, Starita LM, Lo RS, Fields S, Shendure J, Massively parallel single-amino-acid mutagenesis. Nature Methods. 2015;12(3):203–206. doi: 10.1038/nmeth.322325559584
30. Wrenbeck EE, Klesmith JR, Stapleton JA, Adeniran A, Tyo KE, Whitehead TA, Plasmid-based one-pot saturation mutagenesis. Nature Methods. 2016;13(11):928–930. doi: 10.1038/nmeth.402927723752
31. Thyagarajan B, Bloom JD, The inherent mutational tolerance and antigenic evolvability of influenza hemagglutinin. eLife. 2014;3:e03300. doi: 10.7554/eLife.03300
32. Doud MB, Bloom JD, Accurate measurement of the effects of all amino-acid mutations to influenza hemagglutinin. Viruses. 2016;8:155. doi: 10.3390/v8060155
33. Wu NC, Young AP, Al-Mawsawi LQ, Olson CA, Feng J, Qi H, et al. High-throughput profiling of influenza A virus hemagglutinin gene at single-nucleotide resolution. Scientific reports. 2014;4:4942. doi: 10.1038/srep0494224820965
34. Li C, Hatta M, Burke DF, Ping J, Zhang Y, Ozawa M, et al. Selection of antigenically advanced variants of seasonal influenza viruses. Nature Microbiology. 2016;1:16058. doi: 10.1038/nmicrobiol.2016.5827572841
35. Haddox HK, Dingens AS, Bloom JD, Experimental Estimation of the Effects of All Amino-Acid Mutations to HIV’s Envelope Protein on Viral Replication in Cell Culture. PLoS Pathogens. 2016;12(12):e1006114. doi: 10.1371/journal.ppat.100611427959955
36. Fazekas S, et al. Antigenic, adaptive and adsorptive variants of the influenza A hemagglutinin. In: The Influenza Virus Hemagglutinin. Springer; 1978. p. 25–48.
37. Yewdell JW, Caton AJ, Gerhard W, Selection of influenza A virus adsorptive mutants by growth in the presence of a mixture of monoclonal antihemagglutinin antibodies. Journal of virology. 1986;57(2):623–628. 2418215
38. Hensley SE, Das SR, Bailey AL, Schmidt LM, Hickman HD, Jayaraman A, et al. Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science. 2009;326(5953):734–736. doi: 10.1126/science.117825819900932
39. Hooper KA, Bloom JD, A mutant influenza virus that uses an N1 neuraminidase as the receptor-binding protein. Journal of Virology. 2013;87(23):12531–12540. doi: 10.1128/JVI.01889-1324027333
40. Koel BF, Burke DF, Bestebroer TM, van der Vliet S, Zondag GC, Vervaet G, et al. Substitutions near the receptor binding site determine major antigenic change during influenza virus evolution. Science. 2013;342(6161):976–979. doi: 10.1126/science.124473024264991
41. Magadán JG, Khurana S, Das SR, Frank GM, Stevens J, Golding H, et al. Influenza A virus hemagglutinin trimerization completes monomer folding and antigenicity. Journal of virology. 2013;87(17):9742–9753. doi: 10.1128/JVI.00471-1323824811
42. Das SR, Hensley SE, Ince WL, Brooke CB, Subba A, Delboy MG, et al. Defining influenza a virus hemagglutinin antigenic drift by sequential monoclonal antibody selection. Cell host & microbe. 2013;13(3):314–323. doi: 10.1016/j.chom.2013.02.008
43. Doud MB, Ashenberg O, Bloom JD, Site-specific amino acid preferences are mostly conserved in two closely related protein homologs. Mol Biol Evol. 2015;32:2944–2960. doi: 10.1093/molbev/msv16726226986
44. Wu NC, Du Y, Le S, Young AP, Zhang TH, Wang Y, et al. Coupling high-throughput genetics with phylogenetic information reveals an epistatic interaction on the influenza A virus M segment. BMC genomics. 2016;17(1):1. doi: 10.1186/s12864-015-2358-7
45. Kowalsky CA, Faber MS, Nath A, Dann HE, Kelly VW, Liu L, et al. Rapid fine conformational epitope mapping using comprehensive mutagenesis and deep sequencing. Journal of Biological Chemistry. 2015;290(44): 26457–26470. doi: 10.1074/jbc.M115.67663526296891
46. Adams RM, Kinney JB, Mora T, Walczak AM, Measuring the sequence-affinity landscape of antibodies with massively parallel titration curves. eLife. 2016;5:e23156. doi: 10.7554/eLife.2315628035901
47. Gaiotto T, Hufton SE, Cross-Neutralising Nanobodies Bind to a Conserved Pocket in the Hemagglutinin Stem Region Identified Using Yeast Display and Deep Mutational Scanning. PloS One. 2016;11(10):e0164296. doi: 10.1371/journal.pone.016429627741319
48. Neumann G, Watanabe T, Ito H, Watanabe S, Goto H, Gao P, et al. Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci USA. 1999;96:9345–9350. doi: 10.1073/pnas.96.16.934510430945
49. Bloom JD, An experimentally determined evolutionary model dramatically improves phylogenetic fit. Molecular Biology and Evolution. 2014;31:1956–1978. doi: 10.1093/molbev/msu17324859245
50. Bloom JD, Software for the analysis and visualization of deep mutational scanning data. BMC Bioinformatics. 2015;16(1):1. doi: 10.1186/s12859-015-0590-4
51. Crooks GE, Hon G, Chandonia JM, Brenner SE, WebLogo: a sequence logo generator. Genome Research. 2004;14(6):1188–1190. doi: 10.1101/gr.84900415173120
52. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG, A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci USA. 2000;97:6108–6113. doi: 10.1073/pnas.10013369710801978
53. Bloom JD, Gong LI, Baltimore D, Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science. 2010;328:1272–1275. doi: 10.1126/science.118781620522774
54. Gamblin S, Haire L, Russell R, Stevens D, Xiao B, Ha Y, et al. The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science. 2004;303(5665):1838–1842. doi: 10.1126/science.109315514764886