Co-evolution of Immunity and Seasonal Influenza Viruses

Overview

Journal Nat Rev Microbiol

Specialties Infectious Diseases
Microbiology

Date 2023 Aug 2

PMID 37532870

Authors

Alvin X Han

Simon P J de Jong

Colin A Russell

Affiliations

Soon will be listed here.

Abstract

Seasonal influenza viruses cause recurring global epidemics by continually evolving to escape host immunity. The viral constraints and host immune responses that limit and drive the evolution of these viruses are increasingly well understood. However, it remains unclear how most of these advances improve the capacity to reduce the impact of seasonal influenza viruses on human health. In this Review, we synthesize recent progress made in understanding the interplay between the evolution of immunity induced by previous infections or vaccination and the evolution of seasonal influenza viruses driven by the heterogeneous accumulation of antibody-mediated immunity in humans. We discuss the functional constraints that limit the evolution of the viruses, the within-host evolutionary processes that drive the emergence of new virus variants, as well as current and prospective options for influenza virus control, including the viral and immunological barriers that must be overcome to improve the effectiveness of vaccines and antiviral drugs.

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References

Iuliano A, Roguski K, Chang H, Muscatello D, Palekar R, Tempia S . Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet. 2017; 391(10127):1285-1300. PMC: 5935243. DOI: 10.1016/S0140-6736(17)33293-2. View

Chambers B, Parkhouse K, Ross T, Alby K, Hensley S . Identification of Hemagglutinin Residues Responsible for H3N2 Antigenic Drift during the 2014-2015 Influenza Season. Cell Rep. 2015; 12(1):1-6. PMC: 4487778. DOI: 10.1016/j.celrep.2015.06.005. View

Tenforde M, Garten Kondor R, Chung J, Zimmerman R, Nowalk M, Jackson M . Effect of Antigenic Drift on Influenza Vaccine Effectiveness in the United States-2019-2020. Clin Infect Dis. 2020; 73(11):e4244-e4250. PMC: 8664438. DOI: 10.1093/cid/ciaa1884. View

Petrova V, Russell C . The evolution of seasonal influenza viruses. Nat Rev Microbiol. 2017; 16(1):47-60. DOI: 10.1038/nrmicro.2017.118. View

Neumann G, Kawaoka Y . Transmission of influenza A viruses. Virology. 2015; 479-480:234-46. PMC: 4424116. DOI: 10.1016/j.virol.2015.03.009. View

Koutsakos M, Nguyen T, Barclay W, Kedzierska K . Knowns and unknowns of influenza B viruses. Future Microbiol. 2015; 11(1):119-35. DOI: 10.2217/fmb.15.120. View

van de Sandt C, Bodewes R, Rimmelzwaan G, de Vries R . Influenza B viruses: not to be discounted. Future Microbiol. 2015; 10(9):1447-65. DOI: 10.2217/fmb.15.65. View

FRANCIS Jr T . A NEW TYPE OF VIRUS FROM EPIDEMIC INFLUENZA. Science. 1940; 92(2392):405-8. DOI: 10.1126/science.92.2392.405. View

Rota P, Wallis T, Harmon M, Rota J, Kendal A, Nerome K . Cocirculation of two distinct evolutionary lineages of influenza type B virus since 1983. Virology. 1990; 175(1):59-68. DOI: 10.1016/0042-6822(90)90186-u. View

10.

Zamarin D, Garcia-Sastre A, Xiao X, Wang R, Palese P . Influenza virus PB1-F2 protein induces cell death through mitochondrial ANT3 and VDAC1. PLoS Pathog. 2005; 1(1):e4. PMC: 1238739. DOI: 10.1371/journal.ppat.0010004. View

11.

Jagger B, Wise H, Kash J, Walters K, Wills N, Xiao Y . An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science. 2012; 337(6091):199-204. PMC: 3552242. DOI: 10.1126/science.1222213. View

12.

Fernandez-Sesma A, Marukian S, Ebersole B, Kaminski D, Park M, Yuen T . Influenza virus evades innate and adaptive immunity via the NS1 protein. J Virol. 2006; 80(13):6295-304. PMC: 1488970. DOI: 10.1128/JVI.02381-05. View

13.

Krammer F . The human antibody response to influenza A virus infection and vaccination. Nat Rev Immunol. 2019; 19(6):383-397. DOI: 10.1038/s41577-019-0143-6. View

14.

Nelson M, Holmes E . The evolution of epidemic influenza. Nat Rev Genet. 2007; 8(3):196-205. DOI: 10.1038/nrg2053. View

15.

Garten R, Davis C, Russell C, Shu B, Lindstrom S, Balish A . Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science. 2009; 325(5937):197-201. PMC: 3250984. DOI: 10.1126/science.1176225. View

16.

Koel B, Burke D, Bestebroer T, van der Vliet S, Zondag G, Vervaet G . Substitutions near the receptor binding site determine major antigenic change during influenza virus evolution. Science. 2013; 342(6161):976-9. DOI: 10.1126/science.1244730. View

17.

Doud M, Bloom J . Accurate Measurement of the Effects of All Amino-Acid Mutations on Influenza Hemagglutinin. Viruses. 2016; 8(6). PMC: 4926175. DOI: 10.3390/v8060155. View

18.

Smith D, Lapedes A, de Jong J, Bestebroer T, Rimmelzwaan G, Osterhaus A . Mapping the antigenic and genetic evolution of influenza virus. Science. 2004; 305(5682):371-6. DOI: 10.1126/science.1097211. View

19.

Sandbulte M, Westgeest K, Gao J, Xu X, Klimov A, Russell C . Discordant antigenic drift of neuraminidase and hemagglutinin in H1N1 and H3N2 influenza viruses. Proc Natl Acad Sci U S A. 2011; 108(51):20748-53. PMC: 3251064. DOI: 10.1073/pnas.1113801108. View

20.

Bedford T, Riley S, Barr I, Broor S, Chadha M, Cox N . Global circulation patterns of seasonal influenza viruses vary with antigenic drift. Nature. 2015; 523(7559):217-20. PMC: 4499780. DOI: 10.1038/nature14460. View