The evolutionary dynamics of receptor binding avidity in influenza A: A mathematical model for a new antigenic drift hypothesis

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1614, 2013, Pages

  Yuan, Hsiang Yu ^a   Koelle, Katia ^a,b  

^a DUKE UNIVERSITY   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Antigenic drift; Binding avidity changes; Disease dynamics; Influenza evolution

Indexed keywords

AMINO ACID; ANTIGEN; EPIDEMIOLOGY; GENETIC ANALYSIS; IMMUNE RESPONSE; INFLUENZA; NUMERICAL MODEL; PHENOTYPE;

EPITOPE; INFLUENZA VACCINE; VIRUS ANTIGEN; VIRUS HEMAGGLUTININ;

ARTICLE; BIOLOGICAL MODEL; GENETIC VARIABILITY; GENETICS; HUMAN; INFLUENZA VIRUS A; METABOLISM; MOLECULAR EVOLUTION;

ANTIGENS, VIRAL; EPITOPES, B-LYMPHOCYTE; EVOLUTION, MOLECULAR; GENETIC VARIATION; HEMAGGLUTININS, VIRAL; HUMANS; INFLUENZA A VIRUS; INFLUENZA VACCINES; MODELS, GENETIC;

MLCS; MLOWN;

EID: 84880469551     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0204     Document Type: Article

References (41)

1. Nelson MI, Holmes EC. 2007 The evolution of epidemic influenza. Nat. Rev. Genet. 8, 196-205. (doi:10.1038/nrg2053)
2. Pease CM. 1987 An evolutionary epidemiological mechanism, with applications to type A influenza. Theor. Popul. Biol. 31, 422-452. (doi:10.1016/ 0040-5809(87)90014-1)
3. Dushoff J, Plotkin JB, Levin SA, Earn DJD. 2004 Dynamical resonance can account for seasonality of influenza epidemics. Proc. Natl Acad. Sci. USA 101, 16 915-16 916. (doi:10.1073/pnas.0407293101)
4. Shaman J, Pitzer VE, Viboud C, Grenfell BT, Lipsitch M. 2010 Absolute humidity and the seasonal onset of influenza in the continental US. PLoS Biol. 8, e1000316. (doi:10.1371/journal.pbio.1000316)
5. Casagrandi R, Bolzoni L, Levin SA, Andreasen V. 2006 The SIRC model and influenza A. Math. Biosci. 200, 152-169. (doi:10.1016/j.mbs.2005.12.029)
6. Andreasen V, Lin J, Levin SA. 1997 The dynamics of co-circulating influenza strains conferring partial cross-immunity. J. Math. Biol. 35, 825-842. (doi:10.1007/s002850050079)
7. Gog JR, Grenfell BT. 2002 Dynamics and selection of many-strain pathogens. Proc. Natl Acad. Sci. USA 99, 17 209-17 214. (doi:10.1073/pnas.252512799)
8. Ferguson NM, Galvani AP, Bush RM. 2003 Ecological and immunological determinants of influenza evolution. Nature 422, 428-433. (doi:10.1038/ nature01509)
9. Andreasen V, Sasaki A. 2006 Shaping the phylogenetic tree of influenza by cross-immunity. Theor. Popul. Biol. 70, 164-173. (doi:10.1016/j.tpb.2006.04.004)
10. Koelle K, Cobey S, Grenfell B, Pascual M. 2006 Epochal evolution shapes the phylodynamics of influenza A (H3N2) in humans. Science 314, 1898-1903. (doi:10.1126/science.1132745)
11. Gog JR. 2008 The impact of evolutionary constraints on influenza dynamics. Vaccine 26, C15-C24. (doi:10.1016/j.vaccine.2008.04.008)
12. Koelle K, Khatri P, Kamradt M, Kepler TB. 2010 A two-tiered model for simulating the ecological and evolutionary dynamics of rapidly evolving viruses, with an application to influenza. J. R. Soc. Interface 7, 1257-1274. (doi:10.1098/rsif.2010.0007)
13. Bedford T, Rambaut A, Pascual M. 2012 Canalization of the evolutionary trajectory of the human influenza virus. BMC Biol. 10, 2-12. (doi:10.1186/ 1741-7007-10-2)
14. Earn DJD, Dushoff J, Levin SA. 2002 Ecology and evolution of the flu. Trends Ecol. Evol. 17, 334-340. (doi:10.1016/S0169-5347(02)02502-8)
15. Yewdell JW, Webster RG, Gerhard WU. 1979 Antigenic variation in three distinct determinants of an influenza type A haemagglutinin molecule. Nature 279 246-248. (doi:10.1038/279246a0)
16. Yewdell JW, Caton AJ, Gerhard WU. 1986 Selection of Influenza A virus adsorptive mutants by growth in the presence of a mixture of monoclonal antihemagglutinin antibodies. J. Virol. 57, 623-628.
17. Wang M-L, Skehel JJ, Wiley DC. 1986 Comparative analyses of the specificities of anti-influenza hemagglutinin antibodies in human sera. J. Virol. 57, 124-128.
18. Hensley SE et al. 2009 Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 326, 734-736. (doi:10.1126/science.1178258)
19. Lande R. 1976 Natural selection and random genetic drift in phenotypic evolution. Evolution 30, 314-334. (doi:10.2307/2407703)
20. Abrams P. 2001 Modelling the adaptive dynamics of traits involved in inter-and intraspecific interactions: an assessment of three methods. Ecol. Lett. 4, 166-175. (doi:10.1046/j.1461-0248.2001.00199.x)
21. Metz JAJ, Nisbet RM, Geritz SAH. 1992 How should we define 'fitness' for general ecological scenarios? Trends Ecol. Evol. 7, 198-202. (doi:10.1016/0169-5347(92)90073-K)
22. de Jong JC et al. 2007 Antigenic and genetic evolution of swine influenza A (H3N2) viruses in Europe. J. Virol. 81, 4315-4322. (doi:10.1128/JVI. 02458-06)
23. Aledort JE, Lurie N, Wasserman J, Bozzette S. 2007 Non-pharmaceutical public health interventions for pandemic influenza: an evaluation of the evidence base. BMC Public Health 7, 1-9. (doi:10.1186/ 1471-2458-7-208)
24. Bootsma MCJ, Ferguson NM. 2007 The effect of public health measures on the 1918 influenza pandemic in US cities. Proc. Natl Acad. Sci. USA 104, 7588-7593. (doi:10.1073/pnas.0611071104)
25. Smith NM, Bresee JS, Shay DK, Uyeki TM, Cox NJ, Strikas RA. 2006 Prevention and control of influenza with vaccines: recommendations of the advisory committee on immunization practices (ACIP). MMWR Recomm. Rep. 55, 1-42.
26. Fiore AE et al. 2010 Prevention and control of influenza with vaccines: recommendations of the advisory committee on immunization practices (ACIP). MMWR Recomm. Rep. 59, 1-62.
27. Boni MF. 2008 Vaccination and antigenic drift in influenza. Vaccine 26, C8-C14. (doi:10.1016/j. vaccine.2008.04.011)
28. Rudneva IA, Sklyanskaya EI, Barulina OS, Yamnikova SS, Kovaleva VP, Tsvetkova IV, Kaverin NV. 1996 Phenotypic expression of HA-NA combinations in human-avian influenza A virus reassortants. Arch. Virol. 141, 1091-1099. (doi:10.1007/BF01718612)
29. Hensley SE, Das SR, Gibbs JS, Bailey AL, Schmidt LM, Bennink JR, Yewdell JW, de la Torre JC. 2011 Influenza A virus hemagglutinin antibody escape promotes neuraminidase antigenic variation and drug resistance. PLoS ONE 6, e15190. (doi:10.1371/ journal.pone.0015190)
30. Kaverin NV et al. 1998 Postreassortment changes in influenza A virus hemagglutinin restoring HA-NA functional match. Virology 244, 315-321. (doi:10.1006/viro.1998.9119)
31. Wagner R, Matrosovich M, Klenk H. 2002 Functional balance between hemagglutinin and neuraminadase in influenza virus infections. Rev. Med. Virol. 12, 159-166. (doi:10.1002/rmv.352)
32. Fazekas de St. Groth S, Webster RG. 1996 Disquisitions on original antigenic sin. I. Evidence in man. J. Exp. Med. 124, 331-345. (doi:10.1084/jem.124.3.331)
33. Lessler J, Riley S, Read JM, Wang S, Zhu H, Smith GJD, Guan Y, Jiang CQ, Cummings DAT. 2012 Evidence for antigenic seniority in influenza A (H3N2) antibody responses in Southern China. PLoS Pathog. 8, e1002802. (doi:10.1371/journal.ppat.1002802)
34. Liu Q, Hoi SC, Su CT, Li Z, Kwoh CK, Wong L, Li J. 2011 Structural analysis of the hot spots in the binding between H1N1 HA and the 2D1 antibody: do mutations of H1N1 from 1918 to 2009 affect much on this binding? Bioinformatics 27, 2529-2536.
35. Tusche C, Steinbrück L, McHardy AC. 2008 Detecting patches of protein sites of influenza A viruses under positive selection. Mol. Biol. Evol. 24, 1-9.
36. Arinaminpathy N, Grenfell B. 2010 Dynamics of glycoprotein charge in the evolutionary history of human influenza. PLoS ONE 5, e15674. (doi:10.1371/journal.pone.0015674)
37. Das SR, Hensley SE, David A, Schmidt L, Gibbs JS, Puigbo P, Ince WL, Bennink JR, Yewdell JW. 2011 Fitness costs limit influenza A virus hemagglutinin glycosylation as an immune evasion strategy. Proc. Natl Acad. Sci. USA 108, E1417-E1422. (doi:10.1073/pnas.1108754108)
38. Kobayashi Y, Suzuki Y. 2012 Compensatory evolution of net-charge in influenza A virus hemagglutinin. PLoS ONE 7, e40422. (doi:10.1371/journal.pone.0040422)
39. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, Tatusova T, Ostell J, Lipman D. 2008 The influenza virus resource at the National Center for Biotechnology Information. J. Virol. 82, 596-601. (doi:10.1128/JVI.02005-07)
40. Fitch WM, Bush WM, Bender CA, Cox NJ. 1997 Long term trends in the evolution of H(3) HA1 human influenza type A. Proc. Natl Acad. Sci. USA 94, 7712-7718. (doi:10.1073/pnas.94.15.7712)
41. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, Osterhaus ADME, Fouchier RAM. 2004 Mapping the antigenic and genetic evolution of influenza virus. Science 305, 371-376. (doi:10.1126/science.1097211)