Lamprey VLRB response to influenza virus supports universal rules of immunogenicity and antigenicity

eLife

Volumn 4, Issue AUGUST2015, 2015, Pages

  Altman, Meghan O ^a   Bennink, Jack R ^a   Yewdell, Jonathan W ^a   Herrin, Brantley R ^b  

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

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; B LYMPHOCYTE RECEPTOR; CYTIDINE DEAMINASE; HEMAGGLUTININ; FISH PROTEIN; IMMUNOGLOBULIN RECEPTOR; VIRUS ANTIGEN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN SPECIFICITY; ANTIGENICITY; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOGENICITY; INFLUENZA VIRUS; LAMPREY; MOUSE; NONHUMAN; PETROMYZON; POLYACRYLAMIDE GEL ELECTROPHORESIS; VIRUS INFECTIVITY; ADAPTIVE IMMUNITY; ANIMAL; FISH DISEASE; GENETICS; IMMUNOLOGY; INFLUENZA A VIRUS; LYMPHOCYTE; ORTHOMYXOVIRUS INFECTION; VETERINARY;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, VIRAL; FISH DISEASES; FISH PROTEINS; INFLUENZA A VIRUS; LAMPREYS; LYMPHOCYTES; MICE; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTORS, IMMUNOLOGIC;

EID: 84940498938     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.07467     Document Type: Article

References (31)

1. Alder MN, Rogozin IB, Iyer LM, Glazko GV, Cooper MD, Pancer Z. 2005. Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 310:1970-1973. doi: 10.1126/science.1119420.
2. Alder MN, Herrin BR, Sadlonova A, Stockard CR, Grizzle WE, Gartland LA, Gartland GL, Boydston JA, Turnbough CL Jr, Cooper MD. 2008. Antibody responses of variable lymphocyte receptors in the lamprey. Nature Immunology 9:319-327. doi: 10.1038/ni1562.
3. Castro R, Jouneau L, Pham HP, Bouchez O, Giudicelli V, Lefranc MP, Quillet E, Benmansour A, Cazals F, Six A, Fillatreau S, Sunyer O, Boudinot P. 2013. Teleost fish mount complex clonal IgM and IgT responses in spleen upon systemic viral infection. PLOS Pathogens 9:e1003098. doi: 10.1371/journal.ppat.1003098.
4. Couch RB, Kasel JA. 1983. Immunity to influenza in man. Annual Review of Microbiology 37:529-549. doi: 10.1146/ annurev.mi.37.100183.002525.
5. Das SR, Hensley SE, Ince WL, Brooke CB, Subba A, Delboy MG, Russ G, Gibbs JS, Bennink JR, Yewdell JW. 2013. Defining influenza A virus hemagglutinin antigenic drift by sequential monoclonal antibody selection. Cell Host & Microbe 13:314-323. doi: 10.1016/j.chom.2013.02.008.
6. Davies DR, Cohen GH. 1996. Interactions of protein antigens with antibodies. Proceedings of the National Academy of Sciences of USA 93:7-12. doi: 10.1073/pnas.93.1.7.
7. Deng L, Luo M, Velikovsky A, Mariuzza RA. 2013. Structural insights into the evolution of the adaptive immune system. Annual Review of Biophysics 42:191-215. doi: 10.1146/annurev-biophys-083012-130422.
8. Dolan BP, Knowlton JJ, David A, Bennink JR, Yewdell JW. 2010. RNA polymerase II inhibitors dissociate antigenic peptide generation from normal viral protein synthesis: a role for nuclear translation in defective ribosomal product synthesis? Journal of Immunology 185:6728-6733. doi: 10.4049/jimmunol.1002543.
9. Finstad J, Good RA. 1964. The evolution of the immune response. 3. Immunologic responses in the lamprey. The Journal of Experimental Medicine 120:1151-1168. doi: 10.1084/jem.120.6.1151.
10. Georgiou G, Ippolito GC, Beausang J, Busse CE, Wardemann H, Quake SR. 2014. The promise and challenge of high-throughput sequencing of the antibody repertoire. Nature Biotechnology 32:158-168. doi: 10.1038/nbt.2782.
11. Gerhard W, Yewdell J, Frankel ME, Webster R. 1981. Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies. Nature 290:713-717. doi: 10.1038/290713a0.
12. Han BW, Herrin BR, Cooper MD, Wilson IA. 2008. Antigen recognition by variable lymphocyte receptors. Science 321:1834-1837. doi: 10.1126/science.1162484.
13. Herrin BR, Alder MN, Roux KH, Sina C, Ehrhardt GR, Boydston JA, Turnbough CL Jr, Cooper MD. 2008. Structure and specificity of lamprey monoclonal antibodies. Proceedings of the National Academy of Sciences of USA 105: 2040-2045. doi: 10.1073/pnas.0711619105.
14. Hutchinson EC, Charles PD, Hester SS, Thomas B, Trudgian D, Martínez-Alonso M, Fodor E. 2014. Conserved and host-specific features of influenza virion architecture. Nature Communications 5:4816. doi: 10.1038/ ncomms5816.
15. Kim HM, Oh SC, Lim KJ, Kasamatsu J, Heo JY, Park BS, Lee H, Yoo OJ, Kasahara M, Lee JO. 2007. Structural diversity of the hagfish variable lymphocyte receptors. The Journal of Biological Chemistry 282:6726-6732. doi: 10.1074/jbc.M608471200.
16. Kirchdoerfer RN, Herrin BR, Han BW, Turnbough CL, Cooper MD, Wilson IA. 2012. Variable lymphocyte receptor recognition of the immunodominant glycoprotein of Bacillus anthracis spores. Structure 20:479-486.
17. Laursen NS, Wilson IA. 2013. Broadly neutralizing antibodies against influenza viruses. Antiviral Research 98: 476-483. doi: 10.1016/j.antiviral.2013.03.021.
18. Lubeck M, Gerhard W. 1982. Conformational changes at topologically distinct antigenic sites on the influenza A/PR/8/34 virus HA molecule are induced by the binding of monoclonal antibodies. Virology 118:1-7. doi: 10. 1016/0042-6822(82)90313-0.
19. Luo M, Velikovsky CA, Yang X, Siddiqui MA, Hong X, Barchi JJ Jr, Gildersleeve JC, Pancer Z, Mariuzza RA. 2013. Recognition of the Thomsen-Friedenreich pancarcinoma carbohydrate antigen by a lamprey variable lymphocyte receptor. The Journal of Biological Chemistry 288:23597-23606. doi: 10.1074/jbc.M113.480467.
20. Magadan JG, Khurana S, Das SR, Frank GM, Stevens J, Golding H, Bennink JR, Yewdell JW. 2013. Influenza a virus hemagglutinin trimerization completes monomer folding and antigenicity. Journal of Virology 87:9742-9753. doi: 10.1128/JVI.00471-13.
21. Mian IS, Bradwell AR, Olson AJ. 1991. Structure, function and properties of antibody binding sites. Journal of Molecular Biology 217:133-151. doi: 10.1016/0022-2836(91)90617-F.
22. Nagawa F, Kishishita N, Shimizu K, Hirose S, Miyoshi M, Nezu J, Nishimura T, Nishizumi H, Takahashi Y, Hashimoto S, Takeuchi M, Miyajima A, Takemori T, Otsuka AJ, Sakano H. 2007. Antigen-receptor genes of the agnathan lamprey are assembled by a process involving copy choice. Nature Immunology 8:206-213. doi: 10.1038/ni1419.
23. Oxford JS, Schild GC. 1976. Immunological and physicochemical studies of influenza matrix (M) polypeptides. Virology 74:394-402. doi: 10.1016/0042-6822(76)90345-7.
24. Pancer Z, Amemiya CT, Ehrhardt GR, Ceitlin J, Gartland GL, Cooper MD. 2004. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430:174-180. doi: 10.1038/nature02740.
25. Ramaraj T, Angel T, Dratz EA, Jesaitis AJ, Mumey B. 2012. Antigen-antibody interface properties: composition, residue interactions, and features of 53 non-redundant structures. Biochimica et Biophysica Acta 1824:520-532. doi: 10.1016/j.bbapap.2011.12.007.
26. Robin G, Sato Y, Desplancq D, Rochel N, Weiss E, Martineau P. 2014. Restricted diversity of antigen binding residues of antibodies revealed by computational alanine scanning of 227 antibody-antigen complexes. Journal of Molecular Biology 426:3729-3743. doi: 10.1016/j.jmb.2014.08.013.
27. Rogozin IB, Iyer LM, Liang L, Glazko GV, Liston VG, Pavlov YI, Aravind L, Pancer Z. 2007. Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase. Nature Immunology 8:647-656. doi: 10.1038/ni1463.
28. Velikovsky CA, Deng L, Tasumi S, Iyer LM, Kerzic MC, Aravind L, Pancer Z, Mariuzza RA. 2009. Structure of a lamprey variable lymphocyte receptor in complex with a protein antigen. Nature Structural & Molecular Biology 16:725-730. doi: 10.1038/nsmb.1619.
29. Xu Z, Parra D, Gomez D, Salinas I, Zhang YA, von Gersdorff Jorgensen L, Heinecke RD, Buchmann K, LaPatra S, Sunyer JO. 2013. Teleost skin, an ancient mucosal surface that elicits gut-like immune responses. Proceedings of the National Academy of Sciences of USA 110:13097-13102. doi: 10.1073/pnas.1304319110.
30. Ye Q, Guu TS, Mata DA, Kuo RL, Smith B, Krug RM, Tao YJ. 2013. Biochemical and structural evidence in support of a coherent model for the formation of the double-helical influenza A virus ribonucleoprotein. mBio 4: e00467-12. doi: 10.1128/mBio.00467-12.
31. Yewdell JW, Frank E, Gerhard W. 1981. Expression of influenza A virus internal antigens on the surface of infected P815 cells. Journal of Immunology 126:1814-1819.