1932

Abstract

Vertebrate immune systems suppress viral infection using both innate restriction factors and adaptive immunity. Viruses mutate to escape these defenses, driving hosts to counterevolve to regain fitness. This cycle recurs repeatedly, resulting in an evolutionary arms race whose outcome depends on the pace and likelihood of adaptation by host and viral genes. Although viruses evolve faster than their vertebrate hosts, their proteins are subject to numerous functional constraints that impact the probability of adaptation. These constraints are globally defined by evolutionary landscapes, which describe the fitness and adaptive potential of all possible mutations. We review deep mutational scanning experiments mapping the evolutionary landscapes of both host and viral proteins engaged in arms races. For restriction factors and some broadly neutralizing antibodies, landscapes favor the host, which may help to level the evolutionary playing field against rapidly evolving viruses. We discuss the biophysical underpinnings of these landscapes and their therapeutic implications.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-immunol-072621-084422
2022-04-26
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/immunol/40/1/annurev-immunol-072621-084422.html?itemId=/content/journals/10.1146/annurev-immunol-072621-084422&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Nakamichi K, Shen JZ, Lee CS, Lee A, Roberts EA et al. 2021. Hospitalization and mortality associated with SARS-CoV-2 viral clades in COVID-19. Sci. Rep. 11:14802
    [Google Scholar]
  2. 2. 
    Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N et al. 2003. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289:2179–86
    [Google Scholar]
  3. 3. 
    Schneider DS, Ayres JS. 2008. Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat. Rev. Immunol. 8:11889–95
    [Google Scholar]
  4. 4. 
    Duggal NK, Emerman M. 2012. Evolutionary conflicts between viruses and restriction factors shape immunity. Nat. Rev. Immunol. 12:10687–95
    [Google Scholar]
  5. 5. 
    Goila-Gaur R, Strebel K 2008. HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology 5:151
    [Google Scholar]
  6. 6. 
    Petersen JL, Morris CR, Solheim JC. 2003. Virus evasion of MHC class I molecule presentation. J. Immunol. 171:94473–78
    [Google Scholar]
  7. 7. 
    McCarthy KR, Rennick LJ, Nambulli S, Robinson-McCarthy LR, Bain WG et al. 2021. Recurrent deletions in the SARS-CoV-2 spike glycoprotein drive antibody escape. Science 371:65341139–42
    [Google Scholar]
  8. 8. 
    Doud MB, Hensley SE, Bloom JD. 2017. Complete mapping of viral escape from neutralizing antibodies. PLOS Pathog 13:3e1006271–20
    [Google Scholar]
  9. 9. 
    Fuchs J, Oschwald A, Graf L, Kochs G. 2020. Tick-transmitted thogotovirus gains high virulence by a single MxA escape mutation in the viral nucleoprotein. PLOS Pathog 16:11e1009038–25
    [Google Scholar]
  10. 10. 
    Van Valen L 1973. A new evolutionary law. Evol. Theory 1:1–30
    [Google Scholar]
  11. 11. 
    Victora GD, Nussenzweig MC. 2012. Germinal centers. Immunology 30:1429–57
    [Google Scholar]
  12. 12. 
    Liao H-X, Lynch R, Zhou T, Gao F, Alam SM et al. 2013. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496:7446469–76
    [Google Scholar]
  13. 13. 
    Gaebler C, Wang Z, Lorenzi JCC, Muecksch F, Finkin S et al. 2021. Evolution of antibody immunity to SARS-CoV-2. Nature 591:7851639–44
    [Google Scholar]
  14. 14. 
    Albert J, Abrahamsson B, Nagy K, Aurelius E, Gaines H et al. 1990. Rapid development of isolate-specific neutralizing antibodies after primary HIV-1 infection and consequent emergence of virus variants which resist neutralization by autologous sera. AIDS 4:2107–12
    [Google Scholar]
  15. 15. 
    Wei X, Decker JM, Wang S, Hui H, Kappes JC et al. 2003. Antibody neutralization and escape by HIV-1. Nature 422:6929307–12
    [Google Scholar]
  16. 16. 
    Richman DD, Wrin T, Little SJ, Petropoulos CJ. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. PNAS 100:74144–49
    [Google Scholar]
  17. 17. 
    Eguia RT, Crawford KHD, Stevens-Ayers T, Kelnhofer-Millevolte L, Greninger AL et al. 2021. A human coronavirus evolves antigenically to escape antibody immunity. PLOS Pathog 17:4e1009453
    [Google Scholar]
  18. 18. 
    McCarthy KR, Raymond DD, Do KT, Schmidt AG, Harrison SC. 2019. Affinity maturation in a human humoral response to influenza hemagglutinin. PNAS 116:5226745–51
    [Google Scholar]
  19. 19. 
    Chintalapati M, Moorjani P. 2020. Evolution of the mutation rate across primates. Curr. Opin. Genet. Dev. 62:58–64
    [Google Scholar]
  20. 20. 
    Campbell TB, Schneider K, Wrin T, Petropoulos CJ, Connick E. 2003. Relationship between in vitro human immunodeficiency virus type 1 replication rate and virus load in plasma. J. Virol. 77:2212105–12
    [Google Scholar]
  21. 21. 
    Chen HY, Mascio MD, Perelson AS, Ho DD, Zhang L. 2007. Determination of virus burst size in vivo using a single-cycle SIV in rhesus macaques. PNAS 104:4819079–84
    [Google Scholar]
  22. 22. 
    Sender R, Bar-On YM, Gleizer S, Bernsthein B, Flamholz A et al. 2021. The total number and mass of SARS-CoV-2 virions. medRxiv 2020 11.16.20232009. https://doi.org/10.1101/2020.11.16.20232009
    [Crossref] [Google Scholar]
  23. 23. 
    Roach JC, Glusman G, Smit AFA, Huff CD, Hubley R et al. 2010. Analysis of genetic inheritance in a family quartet by whole-genome sequencing. Science 328:5978636–39
    [Google Scholar]
  24. 24. 
    Hanada K, Suzuki Y, Gojobori T. 2004. A large variation in the rates of synonymous substitution for RNA viruses and its relationship to a diversity of viral infection and transmission modes. Mol. Biol. Evol. 21:61074–80
    [Google Scholar]
  25. 25. 
    Sanjuán R, Domingo-Calap P. 2016. Mechanisms of viral mutation. Cell Mol. Life Sci. 73:234433–48
    [Google Scholar]
  26. 26. 
    McCrone JT, Lauring AS. 2018. Genetic bottlenecks in intraspecies virus transmission. Curr. Opin. Virol. 28:20–25
    [Google Scholar]
  27. 27. 
    Parrish NF, Gao F, Li H, Giorgi EE, Barbian HJ et al. 2013. Phenotypic properties of transmitted founder HIV-1. PNAS 110:176626–33
    [Google Scholar]
  28. 28. 
    McCarthy KR, Kirmaier A, Autissier P, Johnson WE 2015. Evolutionary and functional analysis of old world primate TRIM5 reveals the ancient emergence of primate lentiviruses and convergent evolution targeting a conserved capsid interface. PLOS Pathog 11:8e1005085
    [Google Scholar]
  29. 29. 
    Compton AA, Emerman M. 2013. Convergence and divergence in the evolution of the APOBEC3G-Vif interaction reveal ancient origins of simian immunodeficiency viruses. PLOS Pathog 9:1e1003135
    [Google Scholar]
  30. 30. 
    Etienne L, Bibollet-Ruche F, Sudmant PH, Wu LI, Hahn BH, Emerman M. 2015. The role of the antiviral APOBEC3 gene family in protecting chimpanzees against lentiviruses from monkeys. PLOS Pathog 11:9e1005149
    [Google Scholar]
  31. 31. 
    Ito J, Gifford RJ, Sato K 2020. Retroviruses drive the rapid evolution of mammalian APOBEC3 genes. PNAS 117:1610–18
    [Google Scholar]
  32. 32. 
    Kirmaier A, Wu F, Newman RM, Hall LR, Morgan JS et al. 2010. TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species. PLOS Biol 8:8e1000462–12Demonstration that a single restriction factor can suppress cross species transmission in vivo.
    [Google Scholar]
  33. 33. 
    Krupp A, McCarthy KR, Ooms M, Letko M, Morgan JS et al. 2013. APOBEC3G polymorphism as a selective barrier to cross-species transmission and emergence of pathogenic SIV and AIDS in a primate host. PLOS Pathog 9:10e1003641
    [Google Scholar]
  34. 34. 
    Mänz B, Dornfeld D, Götz V, Zell R, Zimmermann P et al. 2013. Pandemic influenza A viruses escape from restriction by human MxA through adaptive mutations in the nucleoprotein. PLOS Pathog 9:3e1003279–16
    [Google Scholar]
  35. 35. 
    Everitt AR, Clare S, Pertel T, John SP, Wash RS et al. 2012. IFITM3 restricts the morbidity and mortality associated with influenza. Nature 484:7395519–23
    [Google Scholar]
  36. 36. 
    Deeg CM, Hassan E, Mutz P, Rheinemann L, Götz V et al. 2017. In vivo evasion of MxA by avian influenza viruses requires human signature in the viral nucleoprotein. J. Exp. Med. 214:51239–48
    [Google Scholar]
  37. 37. 
    Kratovac Z, Virgen CA, Bibollet-Ruche F, Hahn BH, Bieniasz PD, Hatziioannou T. 2008. Primate lentivirus capsid sensitivity to TRIM5 proteins. J. Virol. 82:136772–77
    [Google Scholar]
  38. 38. 
    Compton AA, Hirsch VM, Emerman M 2012. The host restriction factor APOBEC3G and retroviral Vif protein coevolve due to ongoing genetic conflict. Cell Host Microbe 11:191–98Heterozygous alleles of the APOBEC3G restriction factor act codominantly and suppress viral counteradaptation.
    [Google Scholar]
  39. 39. 
    Goujon C, Moncorgé O, Bauby H, Doyle T, Ward CC et al. 2013. Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 502:7472559–62
    [Google Scholar]
  40. 40. 
    Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J 2004. The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427:6977848–53
    [Google Scholar]
  41. 41. 
    Schoggins JW. 2019. Interferon-stimulated genes: What do they all do?. Annu. Rev. Virol. 6:567–84
    [Google Scholar]
  42. 42. 
    OhAinle M, Helms L, Vermeire J, Roesch F, Humes D et al. 2018. A virus-packageable CRISPR screen identifies host factors mediating interferon inhibition of HIV. eLife 7:783
    [Google Scholar]
  43. 43. 
    Tareen SU, Sawyer SL, Malik HS, Emerman M 2009. An expanded clade of rodent Trim5 genes. Virology 385:2473–83
    [Google Scholar]
  44. 44. 
    Sawyer SL, Emerman M, Malik HS 2007. Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals. PLOS Pathog 3:12e197
    [Google Scholar]
  45. 45. 
    Yang L, Emerman M, Malik HS, McLaughlin RN 2020. Retrocopying expands the functional repertoire of APOBEC3 antiviral proteins in primates. eLife 9:e58436
    [Google Scholar]
  46. 46. 
    Russell RA, Pathak VK 2007. Identification of two distinct human immunodeficiency virus type 1 Vif determinants critical for interactions with human APOBEC3G and APOBEC3F. J. Virol 81:158201–10Duplicated APOBEC3 restriction factors impose distinct constraints on viruses, including functional trade-offs.
    [Google Scholar]
  47. 47. 
    Wilson SJ, Webb BLJ, Maplanka C, Newman RM, Verschoor EJ et al. 2008. Rhesus macaque TRIM5 alleles have divergent antiretroviral specificities. J. Virol. 82:147243–47
    [Google Scholar]
  48. 48. 
    Newman RM, Hall L, Connole M, Chen G-L, Sato S et al. 2006. Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5α. PNAS 103:5019134–39
    [Google Scholar]
  49. 49. 
    Simon-Loriere E, Holmes EC 2013. Gene duplication is infrequent in the recent evolutionary history of RNA viruses. Mol. Biol. Evol. 30:61263–69
    [Google Scholar]
  50. 50. 
    Elde NC, Child SJ, Eickbush MT, Kitzman JO, Rogers KS et al. 2012. Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses. Cell 150:4831–41
    [Google Scholar]
  51. 51. 
    Luria SE, Delbrück M. 1943. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28:6491–511
    [Google Scholar]
  52. 52. 
    Christensen DE, Ganser-Pornillos BK, Johnson JS, Pornillos O, Sundquist WI 2020. Reconstitution and visualization of HIV-1 capsid-dependent replication and integration in vitro. Science 370:6513eabc8420–13
    [Google Scholar]
  53. 53. 
    von Schwedler UK, Stray KM, Garrus JE, Sundquist WI. 2003. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77:95439–50
    [Google Scholar]
  54. 54. 
    Lindenmann J. 1964. Inheritance of resistance to influenza virus in mice. Proc. Soc. Exp. Biol. Med 116:2506–9
    [Google Scholar]
  55. 55. 
    McEwan WA, Schaller T, Ylinen LM, Hosie MJ, Towers GJ, Willett BJ. 2009. Truncation of TRIM5 in the Feliformia explains the absence of retroviral restriction in cells of the domestic cat. J. Virol. 83:168270–75
    [Google Scholar]
  56. 56. 
    Wright S. 1932. The roles of mutation, inbreeding, crossbreeding, and selection in evolution. Proc. Sixth Int. Congr. Genet. 1:356–66
    [Google Scholar]
  57. 57. 
    Smith JM. 1970. Natural selection and the concept of a protein space. Nature 225:5232563–64
    [Google Scholar]
  58. 58. 
    Jardine JG, Kulp DW, Havenar-Daughton C, Sarkar A, Briney B et al. 2016. HIV-1 broadly neutralizing antibody precursor B cells revealed by germline-targeting immunogen. Science 351:62801458–63
    [Google Scholar]
  59. 59. 
    Conti S, Kaczorowski KJ, Song G, Porter K, Andrabi R et al. 2021. Design of immunogens to elicit broadly neutralizing antibodies against HIV targeting the CD4 binding site. PNAS 118:9e2018338118
    [Google Scholar]
  60. 60. 
    Soh YS, Moncla LH, Eguia R, Bedford T, Bloom JD 2019. Comprehensive mapping of adaptation of the avian influenza polymerase protein PB2 to humans. eLife 8:12241
    [Google Scholar]
  61. 61. 
    Daugherty MD, Malik HS. 2012. Rules of engagement: molecular insights from host-virus arms races. Annu. Rev. Genet. 46:677–700
    [Google Scholar]
  62. 62. 
    Sorouri M, Chang T, Jesudhasan P, Pinkham C, Elde NC, Hancks DC. 2020. Signatures of host-pathogen evolutionary conflict reveal MISTR—a conserved MItochondrial STress Response network. PLOS Biol 18:12e3001045
    [Google Scholar]
  63. 63. 
    Sawyer SL, Wu LI, Emerman M, Malik HS 2005. Positive selection of primate TRIM5α identifies a critical species-specific retroviral restriction domain. PNAS 102:82832–37
    [Google Scholar]
  64. 64. 
    Lim ES, Malik HS, Emerman M 2010. Ancient adaptive evolution of Tetherin shaped the functions of Vpu and Nef in human immunodeficiency virus and primate lentiviruses. J. Virol. 84:147124–34
    [Google Scholar]
  65. 65. 
    Biris N, Yang Y, Taylor AB, Tomashevski A, Guo M et al. 2012. Structure of the rhesus monkey TRIM5α PRYSPRY domain, the HIV capsid recognition module. PNAS 109:3313278–83
    [Google Scholar]
  66. 66. 
    McNatt MW, Zang T, Bieniasz PD 2013. Vpu binds directly to Tetherin and displaces it from nascent virions. PLOS Pathog 9:4e1003299
    [Google Scholar]
  67. 67. 
    Clackson T, Wells J 1995. A hot spot of binding energy in a hormone-receptor interface. Science 267:5196383–86
    [Google Scholar]
  68. 68. 
    Li Y, Li X, Stremlau M, Lee M, Sodroski J 2006. Removal of arginine 332 allows human TRIM5α to bind human immunodeficiency virus capsids and to restrict infection. J. Virol. 80:146738–44
    [Google Scholar]
  69. 69. 
    Mitchell PS, Patzina C, Emerman M, Haller O, Malik HS, Kochs G 2012. Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA. Cell Host Microbe 12:4598–604
    [Google Scholar]
  70. 70. 
    Lenormand T, Roze D, Rousset F 2009. Stochasticity in evolution. Trends Ecol. Evol. 24:3157–65
    [Google Scholar]
  71. 71. 
    Sharp PM, Hahn BH. 2011. Origins of HIV and the AIDS pandemic. Cold Spring Harb. Perspect. Med. 1:1a006841
    [Google Scholar]
  72. 72. 
    Bell SM, Bedford T. 2017. Modern-day SIV viral diversity generated by extensive recombination and cross-species transmission. PLOS Pathog 13:7e1006466
    [Google Scholar]
  73. 73. 
    Tenthorey JL, Young C, Sodeinde A, Emerman M, Malik HS 2020. Mutational resilience of antiviral restriction favors primate TRIM5α in host-virus evolutionary arms races. eLife 9:e59988Most comprehensive map of a restriction factor evolutionary landscape to date.
    [Google Scholar]
  74. 74. 
    Dingens AS, Arenz D, Weight H, Overbaugh J, Bloom JD 2019. An antigenic atlas of HIV-1 escape from broadly neutralizing antibodies distinguishes functional and structural epitopes. Immunity 50:2520–32.e3
    [Google Scholar]
  75. 75. 
    Sourisseau M, Lawrence DJP, Schwarz MC, Storrs CH, Veit EC et al. 2019. Deep mutational scanning comprehensively maps how Zika envelope protein mutations affect viral growth and antibody escape. J. Virol. 93:23e01291–19
    [Google Scholar]
  76. 76. 
    Ashenberg O, Padmakumar J, Doud MB, Bloom JD 2017. Deep mutational scanning identifies sites in influenza nucleoprotein that affect viral inhibition by MxA. PLOS Pathog 13:3e1006288–23First deep mutational scan for viral escape from a restriction factor.
    [Google Scholar]
  77. 77. 
    Fowler DM, Araya CL, Fleishman SJ, Kellogg EH, Stephany JJ et al. 2010. High-resolution mapping of protein sequence-function relationships. Nat. Methods 7:9741–46Authors pioneered the deep mutational scanning approach to map evolutionary landscapes.
    [Google Scholar]
  78. 78. 
    Fowler DM, Fields S. 2014. Deep mutational scanning: a new style of protein science. Nat. Methods 11:8801–7
    [Google Scholar]
  79. 79. 
    Narayanan KK, Procko E. 2021. Deep mutational scanning of viral glycoproteins and their host receptors. Front. Mol. Biosci. 8:636660
    [Google Scholar]
  80. 80. 
    Cunningham B, Wells J. 1989. High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science 244:49081081–85
    [Google Scholar]
  81. 81. 
    Pacheco B, Finzi A, Stremlau M, Sodroski J. 2010. Adaptation of HIV-1 to cells expressing rhesus monkey TRIM5α. Virology 408:2204–12
    [Google Scholar]
  82. 82. 
    Greaney AJ, Starr TN, Gilchuk P, Zost SJ, Binshtein E et al. 2020. Complete mapping of mutations to the SARS-CoV-2 spike receptor-binding domain that escape antibody recognition. Cell Host Microbe 29:144–57.e9
    [Google Scholar]
  83. 83. 
    Soll SJ, Wilson SJ, Kutluay SB, Hatziioannou T, Bieniasz PD. 2013. Assisted evolution enables HIV-1 to overcome a high TRIM5α-imposed genetic barrier to rhesus macaque tropism. PLOS Pathog 9:9e1003667
    [Google Scholar]
  84. 84. 
    Checkley MA, Luttge BG, Freed EO. 2011. HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation. J. Mol. Biol. 410:4582–608
    [Google Scholar]
  85. 85. 
    Duan L, Zheng Q, Zhang H, Niu Y, Lou Y, Wang H 2020. The SARS-CoV-2 spike glycoprotein biosynthesis, structure, function, and antigenicity: implications for the design of spike-based vaccine immunogens. Front. Immunol. 11:576622
    [Google Scholar]
  86. 86. 
    Haddox HK, Dingens AS, Hilton SK, Overbaugh J, Bloom JD 2018. Mapping mutational effects along the evolutionary landscape of HIV envelope. eLife 7:e34420
    [Google Scholar]
  87. 87. 
    Starr TN, Greaney AJ, Hilton SK, Ellis D, Crawford KHD et al. 2020. Deep mutational scanning of SARS-CoV-2 receptor binding domain reveals constraints on folding and ACE2 binding. Cell 182:51295–310.e20
    [Google Scholar]
  88. 88. 
    Doud M, Bloom J. 2016. Accurate measurement of the effects of all amino-acid mutations on influenza hemagglutinin. Viruses 8:6155
    [Google Scholar]
  89. 89. 
    Starr TN, Greaney AJ, Addetia A, Hannon WW, Choudhary MC et al. 2021. Prospective mapping of viral mutations that escape antibodies used to treat COVID-19. Science 371:6531850–54
    [Google Scholar]
  90. 90. 
    Stoddard CI, Galloway J, Chu HY, Shipley MM, Sung K et al. 2021. Epitope profiling reveals binding signatures of SARS-CoV-2 immune response in natural infection and cross-reactivity with endemic human CoVs. Cell Rep 35:8109164
    [Google Scholar]
  91. 91. 
    Eshleman SH, Laeyendecker O, Kammers K, Chen A, Sivay MV et al. 2019. Comprehensive profiling of HIV antibody evolution. Cell Rep 27:51422–33.e4
    [Google Scholar]
  92. 92. 
    Dingens AS, Pratap P, Malone KD, Hilton SK, Ketas T et al. 2021. High-resolution mapping of the neutralizing and binding specificities of polyclonal sera post HIV Env trimer vaccination. eLife 10:e64281
    [Google Scholar]
  93. 93. 
    Weisblum Y, Schmidt F, Zhang F, DaSilva J, Poston D et al. 2020. Escape from neutralizing antibodies by SARS-CoV-2 spike protein variants. eLife 9:e61312
    [Google Scholar]
  94. 94. 
    Lee JM, Eguia R, Zost SJ, Choudhary S, Wilson PC et al. 2019. Mapping person-to-person variation in viral mutations that escape polyclonal serum targeting influenza hemagglutinin. eLife 8:e49324Polyclonal antibody responses are highly focused and allow viral escape via single mutations.
    [Google Scholar]
  95. 95. 
    Doud MB, Lee JM, Bloom JD 2018. How single mutations affect viral escape from broad and narrow antibodies to H1 influenza hemagglutinin. Nat. Commun 9:11386Extreme mutational constraint is required to prevent viral escape from even broadly neutralizing antibodies.
    [Google Scholar]
  96. 96. 
    Dingens AS, Haddox HK, Overbaugh J, Bloom JD 2017. Comprehensive mapping of HIV-1 escape from a broadly neutralizing antibody. Cell Host Microbe 21:6777–87.e4
    [Google Scholar]
  97. 97. 
    Dingens AS, Acharya P, Haddox HK, Rawi R, Xu K et al. 2018. Complete functional mapping of infection- and vaccine-elicited antibodies against the fusion peptide of HIV. PLOS Pathog 14:7e1007159
    [Google Scholar]
  98. 98. 
    Thyagarajan B, Bloom JD 2014. The inherent mutational tolerance and antigenic evolvability of influenza hemagglutinin. eLife 3:R119–26
    [Google Scholar]
  99. 99. 
    Greaney AJ, Loes AN, Crawford KHD, Starr TN, Malone KD et al. 2021. Comprehensive mapping of mutations in the SARS-CoV-2 receptor-binding domain that affect recognition by polyclonal human plasma antibodies. Cell Host Microbe 29:3463–76.e6
    [Google Scholar]
  100. 100. 
    Muñoz-Alía , Nace RA, Zhang L, Russell SJ. 2021. Serotypic evolution of measles virus is constrained by multiple co-dominant B cell epitopes on its surface glycoproteins. Cell Rep. Med. 2:4100225
    [Google Scholar]
  101. 101. 
    Xue KS, Moncla LH, Bedford T, Bloom JD. 2018. Within-host evolution of human influenza virus. Trends Microbiol 26:9781–93
    [Google Scholar]
  102. 102. 
    Harvey WT, Carabelli AM, Jackson B, Gupta RK, Thomson EC et al. 2021. SARS-CoV-2 variants, spike mutations and immune escape. Nat. Rev. Microbiol. 19:7409–24
    [Google Scholar]
  103. 103. 
    Gao S, von der Malsburg A, Paeschke S, Behlke J, Haller O et al. 2010. Structural basis of oligomerization in the stalk region of dynamin-like MxA. Nature 465:7297502–6
    [Google Scholar]
  104. 104. 
    Colón-Thillet R, Hsieh E, Graf L, McLaughlin RN, Young JM et al. 2019. Combinatorial mutagenesis of rapidly evolving residues yields super-restrictor antiviral proteins. PLOS Biol 17:10e3000181
    [Google Scholar]
  105. 105. 
    Draghi JA, Parsons TL, Wagner GP, Plotkin JB. 2010. Mutational robustness can facilitate adaptation. Nature 463:7279353–55
    [Google Scholar]
  106. 106. 
    Hayden EJ, Ferrada E, Wagner A 2011. Cryptic genetic variation promotes rapid evolutionary adaptation in an RNA enzyme. Nature 474:734992–95
    [Google Scholar]
  107. 107. 
    Fulton BO, Sachs D, Beaty SM, Won ST, Lee B et al. 2015. Mutational analysis of measles virus suggests constraints on antigenic variation of the glycoproteins. Cell Rep 11:91331–38
    [Google Scholar]
  108. 108. 
    Doud MB, Ashenberg O, Bloom JD 2015. Site-specific amino acid preferences are mostly conserved in two closely related protein homologs. Mol. Biol. Evol. 32:112944–60
    [Google Scholar]
  109. 109. 
    Rihn SJ, Wilson SJ, Loman NJ, Alim M, Bakker SE et al. 2013. Extreme genetic fragility of the HIV-1 capsid. PLOS Pathog 9:6e1003461
    [Google Scholar]
  110. 110. 
    Shen Q, Xu C, Jang S, Xiong Q, Devarkar SC et al. 2020. A DNA-origami nuclear pore mimic reveals nuclear entry mechanisms of HIV-1 capsid. bioRxiv 2020.08.10.245522. https://doi.org/10.1101/2020.08.10.245522
    [Crossref]
  111. 111. 
    Zila V, Margiotta E, Turoňová B, Müller TG, Zimmerli CE et al. 2021. Cone-shaped HIV-1 capsids are transported through intact nuclear pores. Cell 184:41032–46.e18
    [Google Scholar]
  112. 112. 
    Campbell EM, Hope TJ. 2015. HIV-1 capsid: the multifaceted key player in HIV-1 infection. Nat. Rev. Microbiol. 13:8471–83
    [Google Scholar]
  113. 113. 
    Portela A, Digard P. 2002. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J. Gen. Virol. 83:4723–34
    [Google Scholar]
  114. 114. 
    Phillips AM, Ponomarenko AI, Chen K, Ashenberg O, Miao J et al. 2018. Destabilized adaptive influenza variants critical for innate immune system escape are potentiated by host chaperones. PLOS Biol 16:9e3000008–23A mutation that allows escape from the MxA restriction factor is biophysically deleterious.
    [Google Scholar]
  115. 115. 
    Götz V, Magar L, Dornfeld D, Giese S, Pohlmann A et al. 2016. Influenza A viruses escape from MxA restriction at the expense of efficient nuclear vRNP import. Sci. Rep. 6:123138
    [Google Scholar]
  116. 116. 
    Ooms M, Letko M, Simon V. 2017. The structural interface between HIV-1 Vif and human APOBEC3H. J. Virol. 91:5e02289–16
    [Google Scholar]
  117. 117. 
    Nakashima M, Ode H, Kawamura T, Kitamura S, Naganawa Y et al. 2016. Structural insights into HIV-1 Vif-APOBEC3F interaction. J. Virol. 90:21034–47
    [Google Scholar]
  118. 118. 
    Huthoff H, Malim MH. 2007. Identification of amino acid residues in APOBEC3G required for regulation by human immunodeficiency virus type 1 Vif and virion encapsidation. J. Virol. 81:83807–15
    [Google Scholar]
  119. 119. 
    Binning JM, Chesarino NM, Emerman M, Gross JD 2019. Structural basis for a species-specific determinant of an SIV Vif protein toward hominid APOBEC3G antagonism. Cell Host Microbe 26:6739–47.e4
    [Google Scholar]
  120. 120. 
    Salamango DJ, Harris RS. 2021. Dual functionality of HIV-1 Vif in APOBEC3 counteraction and cell cycle arrest. Front. Microbiol 11:622012
    [Google Scholar]
  121. 121. 
    DePristo MA, Weinreich DM, Hartl DL. 2005. Missense meanderings in sequence space: a biophysical view of protein evolution. Nat. Rev. Genet. 6:9678–87
    [Google Scholar]
  122. 122. 
    Tokuriki N, Tawfik DS. 2009. Stability effects of mutations and protein evolvability. Curr. Opin. Struc. Biol. 19:5596–604
    [Google Scholar]
  123. 123. 
    Wylie CS, Shakhnovich EI. 2011. A biophysical protein folding model accounts for most mutational fitness effects in viruses. PNAS 108:249916–21
    [Google Scholar]
  124. 124. 
    Weinreich DM, Delaney NF, DePristo MA, Hartl DL. 2006. Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312:5770111–14
    [Google Scholar]
  125. 125. 
    Harms MJ, Thornton JW. 2014. Historical contingency and its biophysical basis in glucocorticoid receptor evolution. Nature 512:7513203–7
    [Google Scholar]
  126. 126. 
    Phillips AM, Gonzalez LO, Nekongo EE, Ponomarenko AI, McHugh SM et al. 2017. Host proteostasis modulates influenza evolution. eLife 6:e28652
    [Google Scholar]
  127. 127. 
    Bloom JD, Labthavikul ST, Otey CR, Arnold FH. 2006. Protein stability promotes evolvability. PNAS 103:155869–74
    [Google Scholar]
  128. 128. 
    Bloom JD, Lu Z, Chen D, Raval A, Venturelli OS, Arnold FH. 2007. Evolution favors protein mutational robustness in sufficiently large populations. BMC Biol 5:129
    [Google Scholar]
  129. 129. 
    Guo HH, Choe J, Loeb LA. 2004. Protein tolerance to random amino acid change. PNAS 101:259205–10
    [Google Scholar]
  130. 130. 
    McLaughlin RN, Poelwijk FJ, Raman A, Gosal WS, Ranganathan R. 2012. The spatial architecture of protein function and adaptation. Nature 491:7422138–42
    [Google Scholar]
  131. 131. 
    Suckow J, Markiewicz P, Kleina LG, Miller J, Kisters-Woike B, Müller-Hill B. 1996. Genetic studies of the Lac repressor. XV: 4000 single amino acid substitutions and analysis of the resulting phenotypes on the basis of the protein structure. J. Mol. Biol. 261:4509–23
    [Google Scholar]
  132. 132. 
    Fribourgh JL, Nguyen HC, Matreyek KA, Alvarez FJD, Summers BJ et al. 2014. Structural insight into HIV-1 restriction by MxB. Cell Host Microbe 16:5627–38
    [Google Scholar]
  133. 133. 
    Daugherty PS, Chen G, Iverson BL, Georgiou G. 2000. Quantitative analysis of the effect of the mutation frequency on the affinity maturation of single chain Fv antibodies. PNAS 97:52029–34
    [Google Scholar]
  134. 134. 
    Sheng Z, Schramm CA, Kong R, Program NCS, Mullikin JC et al. 2017. Gene-specific substitution profiles describe the types and frequencies of amino acid changes during antibody somatic hypermutation. Front. Immunol. 8:537
    [Google Scholar]
  135. 135. 
    Mishra AK, Mariuzza RA. 2018. Insights into the structural basis of antibody affinity maturation from next-generation sequencing. Front. Immunol. 9:117
    [Google Scholar]
  136. 136. 
    Nigg PE, Pavlovic J. 2015. Oligomerization and GTP-binding requirements of MxA for viral target recognition and antiviral activity against influenza A virus. J. Biol. Chem. 290:5029893–906
    [Google Scholar]
  137. 137. 
    Wagner JM, Roganowicz MD, Skorupka K, Alam SL, Christensen D et al. 2016. Mechanism of B-box 2 domain-mediated higher-order assembly of the retroviral restriction factor TRIM5α. eLife 5:213
    [Google Scholar]
  138. 138. 
    Schroeder HW, Cavacini L. 2010. Structure and function of immunoglobulins. J. Allergy Clin. Immun. 125:2S41–52
    [Google Scholar]
  139. 139. 
    Tanner EJ, Liu H, Oberste MS, Pallansch M, Collett MS, Kirkegaard K 2014. Dominant drug targets suppress the emergence of antiviral resistance. eLife 3:e03830Viral escape proteins arise from and coexpress with nonescape variants, and hetero-oligomerization suppresses escape evolution.
    [Google Scholar]
  140. 140. 
    Rowe WP, Hartley JW 1972. Studies of genetic transmission of murine leukemia virus by AKR mice: II. Crosses with Fv-1b strains of mice. J. Exp. Med. 136:51286–301
    [Google Scholar]
  141. 141. 
    Goldstein S, Brown CR, Ourmanov I, Pandrea I, Buckler-White A et al. 2006. Comparison of simian immunodeficiency virus SIVagmVer replication and CD4+ T-cell dynamics in vervet and sabaeus African green monkeys. J. Virol. 80:104868–77
    [Google Scholar]
  142. 142. 
    Shi J, Friedman DB, Aiken C. 2013. Retrovirus restriction by TRIM5 proteins requires recognition of only a small fraction of viral capsid subunits. J. Virol. 87:169271–78
    [Google Scholar]
  143. 143. 
    Venkat A, Hahn MW, Thornton JW. 2018. Multinucleotide mutations cause false inferences of lineage-specific positive selection. Nat. Ecol. Evol. 2:81280–88
    [Google Scholar]
  144. 144. 
    Ogden PJ, Kelsic ED, Sinai S, Church GM 2019. Comprehensive AAV capsid fitness landscape reveals a viral gene and enables machine-guided design. Science 366:64691139–43
    [Google Scholar]
  145. 145. 
    Starr TN, Czudnochowski N, Liu Z, Zatta F, Park Y-J et al. 2021. SARS-CoV-2 RBD antibodies that maximize breadth and resistance to escape. Nature 597:787497–102
    [Google Scholar]
  146. 146. 
    Kemp SA, Collier DA, Datir RP, Ferreira IATM, Gayed S et al. 2021. SARS-CoV-2 evolution during treatment of chronic infection. Nature 592:7853277–82
    [Google Scholar]
  147. 147. 
    Pham QT, Bouchard A, Grütter MG, Berthoux L. 2010. Generation of human TRIM5α mutants with high HIV-1 restriction activity. Gene Ther 17:7859–71
    [Google Scholar]
  148. 148. 
    Veillette M, Bichel K, Pawlica P, Freund SMV, Plourde MB et al. 2013. The V86M mutation in HIV-1 capsid confers resistance to TRIM5α by abrogation of cyclophilin A-dependent restriction and enhancement of viral nuclear import. Retrovirology 10:25
    [Google Scholar]
  149. 149. 
    Voit RA, McMahon MA, Sawyer SL, Porteus MH. 2013. Generation of an HIV resistant T-cell line by targeted “stacking” of restriction factors. Mol. Ther. 21:4786–95
    [Google Scholar]
  150. 150. 
    Pallesen J, Wang N, Corbett KS, Wrapp D, Kirchdoerfer RN et al. 2017. Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen. PNAS 114:35E7348–57
    [Google Scholar]
  151. 151. 
    Lauring AS, Acevedo A, Cooper SB, Andino R. 2012. Codon usage determines the mutational robustness, evolutionary capacity, and virulence of an RNA virus. Cell Host Microbe 12:5623–32
    [Google Scholar]
  152. 152. 
    Moratorio G, Henningsson R, Barbezange C, Carrau L, Bordería AV et al. 2017. Attenuation of RNA viruses by redirecting their evolution in sequence space. Nat. Microbiol. 2:817088
    [Google Scholar]
  153. 153. 
    Buchmann K. 2014. Evolution of innate immunity: clues from invertebrates via fish to mammals. Front. Immunol. 5:459
    [Google Scholar]
  154. 154. 
    Baccam P, Beauchemin C, Macken CA, Hayden FG, Perelson AS 2006. Kinetics of influenza A virus infection in humans. J. Virol. 80:157590–99
    [Google Scholar]
  155. 155. 
    Holmes M, Zhang F, Bieniasz PD. 2015. Single-cell and single-cycle analysis of HIV-1 replication. PLOS Pathog 11:6e1004961
    [Google Scholar]
  156. 156. 
    Heldt FS, Kupke SY, Dorl S, Reichl U, Frensing T 2015. Single-cell analysis and stochastic modelling unveil large cell-to-cell variability in influenza A virus infection. Nat. Commun. 6:18938
    [Google Scholar]
  157. 157. 
    Bar-On YM, Flamholz A, Phillips R, Milo R 2020. SARS-CoV-2 (COVID-19) by the numbers. eLife 9:e57309
    [Google Scholar]
  158. 158. 
    Pauly MD, Procario MC, Lauring AS 2017. A novel twelve class fluctuation test reveals higher than expected mutation rates for influenza A viruses. eLife 6:e26437
    [Google Scholar]
  159. 159. 
    Huang KJ, Wooley DP. 2005. A new cell-based assay for measuring the forward mutation rate of HIV-1. J. Virol. Methods 124:1–295–104
    [Google Scholar]
  160. 160. 
    Borges V, Alves MJ, Amicone M, Isidro J, Zé-Zé L et al. 2021. Mutation rate of SARS-CoV-2 and emergence of mutators during experimental evolution. bioRxiv 2021.05.19.4447744
  161. 161. 
    Drake JW, Hwang CBC. 2005. On the mutation rate of herpes simplex virus type 1. Genetics 170:2969–70
    [Google Scholar]
  162. 162. 
    Laguette N, Benkirane M. 2015. Shaping of the host cell by viral accessory proteins. Front. Microbiol. 6:142
    [Google Scholar]
  163. 163. 
    Bahar MW, Graham SC, Chen RA-J, Cooray S, Smith GL et al. 2011. How vaccinia virus has evolved to subvert the host immune response. J. Struct. Biol. 175:2127–34
    [Google Scholar]
  164. 164. 
    Schroder HW. 2006. Similarity and divergence in the development and expression of the mouse and human antibody repertoires. Dev. Comp. Immunol. 30:119–35
    [Google Scholar]
/content/journals/10.1146/annurev-immunol-072621-084422
Loading
/content/journals/10.1146/annurev-immunol-072621-084422
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error