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Annual Review of Immunology

Volume 42, 2024

Poxvirus Immune Evasion

Abstract

Poxviruses have evolved a wide array of mechanisms to evade the immune response, and we provide an overview of the different immunomodulatory strategies. Poxviruses prevent the recognition of viral DNA that triggers the immune responses and inhibit signaling pathways within the infected cell. A unique feature of poxviruses is the production of secreted proteins that mimic cytokines and cytokine receptors, acting as decoy receptors to neutralize the activity of cytokines and chemokines. The capacity of these proteins to evade cellular immune responses by inhibiting cytokine activation is complemented by poxviruses’ strategies to block natural killer cells and cytotoxic T cells, often through interfering with antigen presentation pathways. Mechanisms that target complement activation are also encoded by poxviruses. Virus-encoded proteins that target immune molecules and pathways play a major role in immune modulation, and their contribution to viral pathogenesis, facilitating virus replication or preventing immunopathology, is discussed.

Keyword(s): cell-mediated immunity, cytokine, decoy receptor, immune pathway, poxvirus, viral pathogenesis
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/content/journals/10.1146/annurev-immunol-090222-110227
2024-06-28
2024-06-30
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Literature Cited

  1. 1.
    Smith GL, McFadden G. 2002.. Smallpox: anything to declare?. Nat. Rev. Immunol. 2:(7):521–27
     [Crossref] [Google Scholar]
  2. 2.
    Moss B, Shisler JL, Xiang Y, Senkevich TG. 2000.. Immune-defense molecules of molluscum contagiosum virus, a human poxvirus. . Trends Microbiol. 8:(10):473–77
     [Crossref] [Google Scholar]
  3. 3.
    Reynolds MG, Damon IK. 2012.. Outbreaks of human monkeypox after cessation of smallpox vaccination. . Trends Microbiol. 20:(2):80–87
     [Crossref] [Google Scholar]
  4. 4.
    Lum F-M, Torres-Ruesta A, Tay MZ, Lin RTP, Lye DC, et al. 2022.. Monkeypox: disease epidemiology, host immunity and clinical interventions. . Nat. Rev. Immunol. 22:(10):597–613
     [Crossref] [Google Scholar]
  5. 5.
    Alcamí A. 2023.. Pathogenesis of the circulating mpox virus and its adaptation to humans. . PNAS 120:(13):e2301662120
     [Crossref] [Google Scholar]
  6. 6.
    Seet BT, Johnston JB, Brunetti CR, Barrett JW, Everett H, et al. 2003.. Poxviruses and immune evasion. . Annu. Rev. Immunol. 21::377–423
     [Crossref] [Google Scholar]
  7. 7.
    Smith GL, Benfield CT, Maluquer de Motes C, Mazzon M, Ember SW, et al. 2013.. Vaccinia virus immune evasion: mechanisms, virulence and immunogenicity. . J. Gen. Virol. 94:(Part 11):2367–92
     [Crossref] [Google Scholar]
  8. 8.
    Hendrickson RC, Wang C, Hatcher EL, Lefkowitz EJ. 2010.. Orthopoxvirus genome evolution: the role of gene loss. . Viruses 2:(9):1933–67
     [Crossref] [Google Scholar]
  9. 9.
    Franklin E, Khan AR. 2013.. Poxvirus antagonism of innate immunity by Bcl-2 fold proteins. . J. Struct. Biol. 181:(1):1–10
     [Crossref] [Google Scholar]
  10. 10.
    Alcami A. 2003.. Viral mimicry of cytokines, chemokines and their receptors. . Nat. Rev. Immunol. 3:(1):36–50
     [Crossref] [Google Scholar]
  11. 11.
    Felix J, Savvides SN. 2017.. Mechanisms of immunomodulation by mammalian and viral decoy receptors: insights from structures. . Nat. Rev. Immunol. 17:(2):112–29
     [Crossref] [Google Scholar]
  12. 12.
    Yu H, Bruneau RC, Brennan G, Rothenburg S. 2021.. Battle royale: innate recognition of poxviruses and viral immune evasion. . Biomedicines 9:(7):765
     [Crossref] [Google Scholar]
  13. 13.
    Veyer DL, Carrara G, Maluquer de Motes C, Smith GL. 2017.. Vaccinia virus evasion of regulated cell death. . Immunol. Lett. 186::68–80
     [Crossref] [Google Scholar]
  14. 14.
    Reus JB, Rex EA, Gammon DB. 2022.. How to inhibit nuclear factor-kappa B signaling: lessons from poxviruses. . Pathogens 11:(9):1061
     [Crossref] [Google Scholar]
  15. 15.
    Perdiguero B, Esteban M. 2009.. The interferon system and vaccinia virus evasion mechanisms. . J. Interferon Cytokine Res. 29:(9):581–98
     [Crossref] [Google Scholar]
  16. 16.
    Smith GL, Talbot-Cooper C, Lu Y. 2018.. How does vaccinia virus interfere with interferon?. Adv. Virus Res. 100::355–78
     [Crossref] [Google Scholar]
  17. 17.
    Hopfner K-P, Hornung V. 2020.. Molecular mechanisms and cellular functions of cGAS-STING signalling. . Nat. Rev. Mol. Cell Biol. 21:(9):501–21
     [Crossref] [Google Scholar]
  18. 18.
    Rathinam VAK, Jiang Z, Waggoner SN, Sharma S, Cole LE, et al. 2010.. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. . Nat. Immunol. 11:(5):395–402
     [Crossref] [Google Scholar]
  19. 19.
    Rivera-Calzada A, Arribas-Bosacoma R, Ruiz-Ramos A, Escudero-Bravo P, Boskovic J, et al. 2022.. Structural basis for the inactivation of cytosolic DNA sensing by the vaccinia virus. . Nat. Commun. 13:(1):7062
     [Crossref] [Google Scholar]
  20. 20.
    Scutts SR, Ember SW, Ren H, Ye C, Lovejoy CA, et al. 2018.. DNA-PK is targeted by multiple vaccinia virus proteins to inhibit DNA sensing. . Cell Rep. 25:(7):1953–65.e4
     [Crossref] [Google Scholar]
  21. 21.
    Peters NE, Ferguson BJ, Mazzon M, Fahy AS, Krysztofinska E, et al. 2013.. A mechanism for the inhibition of DNA-PK-mediated DNA sensing by a virus. . PLOS Pathog. 9:(10):e1003649
     [Crossref] [Google Scholar]
  22. 22.
    Mazzon M, Castro C, Roberts LD, Griffin JL, Smith GL. 2015.. A role for vaccinia virus protein C16 in reprogramming cellular energy metabolism. . J. Gen. Virol. 96:(2):395–407
     [Crossref] [Google Scholar]
  23. 23.
    Mazzon M, Peters NE, Loenarz C, Krysztofinska EM, Ember SWJ, et al. 2013.. A mechanism for induction of a hypoxic response by vaccinia virus. . PNAS 110:(30):12444–49
     [Crossref] [Google Scholar]
  24. 24.
    Eaglesham JB, Pan Y, Kupper TS, Kranzusch PJ. 2019.. Viral and metazoan poxins are cGAMP-specific nucleases that restrict cGAS-STING signalling. . Nature 566:(7743):259–63
     [Crossref] [Google Scholar]
  25. 25.
    Hernáez B, Alonso G, Georgana I, El-Jesr M, Martín R, et al. 2020.. Viral cGAMP nuclease reveals the essential role of DNA sensing in protection against acute lethal virus infection. . Sci. Adv. 6:(38):eabb4565
     [Crossref] [Google Scholar]
  26. 26.
    De La Casa-Esperón E. 2011.. From mammals to viruses: the Schlafen genes in developmental, proliferative and immune processes. . BioMol. Concepts 2:(3):159–69
     [Crossref] [Google Scholar]
  27. 27.
    Mavrommatis E, Fish EN, Platanias LC. 2013.. The Schlafen family of proteins and their regulation by interferons. . J. Interferon Cytokine Res. 33:(4):206–10
     [Crossref] [Google Scholar]
  28. 28.
    Maluquer De Motes C. 2021.. Poxvirus cGAMP nucleases: clues and mysteries from a stolen gene. . PLOS Pathog. 17:(3):e1009372
     [Crossref] [Google Scholar]
  29. 29.
    Mühlemann B, Vinner L, Margaryan A, Wilhelmson H, De La Fuente Castro C, et al. 2020.. Diverse variola virus (smallpox) strains were widespread in northern Europe in the Viking Age. . Science 369:(6502):eaaw8977
     [Crossref] [Google Scholar]
  30. 30.
    Alcamí A. 2020.. Was smallpox a widespread mild disease?. Science 369:(6502):376–77
     [Crossref] [Google Scholar]
  31. 31.
    Yang N, Wang Y, Dai P, Li T, Zierhut C, et al. 2023.. Vaccinia E5 is a major inhibitor of the DNA sensor cGAS. . Nat. Commun. 14:(1):2898
     [Crossref] [Google Scholar]
  32. 32.
    Meade N, King M, Munger J, Walsh D. 2019.. mTOR dysregulation by vaccinia virus F17 controls multiple processes with varying roles in infection. . J. Virol. 93:(15):e00784-19
     [Crossref] [Google Scholar]
  33. 33.
    Najarro P, Traktman P, Lewis JA. 2001.. Vaccinia virus blocks gamma interferon signal transduction: viral VH1 phosphatase reverses Stat1 activation. . J. Virol. 75:(7):3185–96
     [Crossref] [Google Scholar]
  34. 34.
    Mann BA, Huang JH, Li P, Chang H-C, Slee RB, et al. 2008.. Vaccinia virus blocks Stat1-dependent and Stat1-independent gene expression induced by type I and type II interferons. . J. Interferon Cytokine Res. 28:(6):367–80
     [Crossref] [Google Scholar]
  35. 35.
    Liu K, Lemon B, Traktman P. 1995.. The dual-specificity phosphatase encoded by vaccinia virus, VH1, is essential for viral transcription in vivo and in vitro. . J. Virol. 69:(12):7823–34
     [Crossref] [Google Scholar]
  36. 36.
    Schmidt FI, Bleck CKE, Reh L, Novy K, Wollscheid B, et al. 2013.. Vaccinia virus entry is followed by core activation and proteasome-mediated release of the immunomodulatory effector VH1 from lateral bodies. . Cell Rep. 4:(3):464–76
     [Crossref] [Google Scholar]
  37. 37.
    Unterholzner L, Sumner RP, Baran M, Ren H, Mansur DS, et al. 2011.. Vaccinia virus protein C6 is a virulence factor that binds TBK-1 adaptor proteins and inhibits activation of IRF3 and IRF7. . PLOS Pathog. 7:(9):e1002247
     [Crossref] [Google Scholar]
  38. 38.
    Stuart JH, Sumner RP, Lu Y, Snowden JS, Smith GL. 2016.. Vaccinia virus protein C6 inhibits type I IFN signalling in the nucleus and binds to the transactivation domain of STAT2. . PLOS Pathog. 12:(12):e1005955
     [Crossref] [Google Scholar]
  39. 39.
    Smith GL. 2018.. Vaccinia virus protein C6: a multifunctional interferon antagonist. . Adv. Exp. Med. Biol. 1052::1–7
     [Crossref] [Google Scholar]
  40. 40.
    Lu Y, Stuart JH, Talbot-Cooper C, Agrawal-Singh S, Huntly B, et al. 2019.. Histone deacetylase 4 promotes type I interferon signaling, restricts DNA viruses, and is degraded via vaccinia virus protein C6. . PNAS 116:(24):11997–96
     [Crossref] [Google Scholar]
  41. 41.
    Chang HW, Watson JC, Jacobs BL. 1992.. The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein kinase. . PNAS 89:(11):4825–29
     [Crossref] [Google Scholar]
  42. 42.
    Romano PR, Zhang F, Tan S-L, Garcia-Barrio MT, Katze MG, et al. 1998.. Inhibition of double-stranded RNA-dependent protein kinase PKR by vaccinia virus E3: role of complex formation and the E3 N-terminal domain. . Mol. Cell. Biol. 18:(12):7304–16
     [Crossref] [Google Scholar]
  43. 43.
    Davies MV, Elroy-Stein O, Jagus R, Moss B, Kaufman RJ. 1992.. The vaccinia virus K3L gene product potentiates translation by inhibiting double-stranded-RNA-activated protein kinase and phosphorylation of the alpha subunit of eukaryotic initiation factor 2. . J. Virol. 66:(4):1943–50
     [Crossref] [Google Scholar]
  44. 44.
    Nájera JL, Gómez CE, Domingo-Gil E, Gherardi MM, Esteban M. 2006.. Cellular and biochemical differences between two attenuated poxvirus vaccine candidates (MVA and NYVAC) and role of the C7L gene. . J. Virol. 80:(12):6033–47
     [Crossref] [Google Scholar]
  45. 45.
    Langland JO, Jacobs BL. 2002.. The role of the PKR-inhibitory genes, E3L and K3L, in determining vaccinia virus host range. . Virology 299:(1):133–41
     [Crossref] [Google Scholar]
  46. 46.
    Brandt TA, Jacobs BL. 2001.. Both carboxy- and amino-terminal domains of the vaccinia virus interferon resistance gene, E3L, are required for pathogenesis in a mouse model. . J. Virol. 75:(2):850–56
     [Crossref] [Google Scholar]
  47. 47.
    Vijaysri S, Jentarra G, Heck MC, Mercer AA, McInnes CJ, Jacobs BL. 2008.. Vaccinia viruses with mutations in the E3L gene as potential replication-competent, attenuated vaccines: intra-nasal vaccination. . Vaccine 26:(5):664–76
     [Crossref] [Google Scholar]
  48. 48.
    Park C, Peng C, Rahman MJ, Haller SL, Tazi L, et al. 2021.. Orthopoxvirus K3 orthologs show virus- and host-specific inhibition of the antiviral protein kinase PKR. . PLOS Pathog. 17:(1):e1009183
     [Crossref] [Google Scholar]
  49. 49.
    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:(4):831–41
     [Crossref] [Google Scholar]
  50. 50.
    Elde NC, Child SJ, Geballe AP, Malik HS. 2009.. Protein kinase R reveals an evolutionary model for defeating viral mimicry. . Nature 457:(7228):485–89
     [Crossref] [Google Scholar]
  51. 51.
    Guerra S, Cáceres A, Knobeloch K-P, Horak I, Esteban M. 2008.. Vaccinia virus E3 protein prevents the antiviral action of ISG15. . PLOS Pathog. 4:(7):e1000096
     [Crossref] [Google Scholar]
  52. 52.
    Liu R, Moss B. 2018.. Vaccinia virus C9 ankyrin repeat/F-box protein is a newly identified antagonist of the type I interferon-induced antiviral state. . J. Virol. 92:(9):e00053-18
     [Crossref] [Google Scholar]
  53. 53.
    Napetschnig J, Wu H. 2013.. Molecular basis of NF-κB signaling. . Annu. Rev. Biophys. 42::443–68
     [Crossref] [Google Scholar]
  54. 54.
    Stack J, Haga IR, Schröder M, Bartlett NW, Maloney G, et al. 2005.. Vaccinia virus protein A46R targets multiple Toll-like-interleukin-1 receptor adaptors and contributes to virulence. . J. Exp. Med. 201:(6):1007–18
     [Crossref] [Google Scholar]
  55. 55.
    Bowie A, Kiss-Toth E, Symons JA, Smith GL, Dower SK, O'Neill LAJ. 2000.. A46R and A52R from vaccinia virus are antagonists of host IL-1 and Toll-like receptor signaling. . PNAS 97:(18):10162–67
     [Crossref] [Google Scholar]
  56. 56.
    Harte MT, Haga IR, Maloney G, Gray P, Reading PC, et al. 2003.. The poxvirus protein A52R targets Toll-like receptor signaling complexes to suppress host defense. . J. Exp. Med. 197:(3):343–51
     [Crossref] [Google Scholar]
  57. 57.
    Schröder M, Baran M, Bowie AG. 2008.. Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKε-mediated IRF activation. . EMBO J. 27:(15):2147–57
     [Crossref] [Google Scholar]
  58. 58.
    DiPerna G, Stack J, Bowie AG, Boyd A, Kotwal G, et al. 2004.. Poxvirus protein N1L targets the I-κB kinase complex, inhibits signaling to NF-κB by the tumor necrosis factor superfamily of receptors, and inhibits NF-κB and IRF3 signaling by Toll-like receptors. . J. Biol. Chem. 279:(35):36570–78
     [Crossref] [Google Scholar]
  59. 59.
    Maluquer De Motes C, Cooray S, Ren H, Almeida GMF, McGourty K, et al. 2011.. Inhibition of apoptosis and NF-κB activation by vaccinia protein N1 occur via distinct binding surfaces and make different contributions to virulence. . PLOS Pathog. 7:(12):e1002430
     [Crossref] [Google Scholar]
  60. 60.
    Tang Q, Chakraborty S, Xu G. 2018.. Mechanism of vaccinia viral protein B14-mediated inhibition of IκB kinase β activation. . J. Biol. Chem. 293:(26):10344–52
     [Crossref] [Google Scholar]
  61. 61.
    Chen RA-J, Ryzhakov G, Cooray S, Randow F, Smith GL. 2008.. Inhibition of IκB kinase by vaccinia virus virulence factor B14. . PLOS Pathog. 4:(2):e22
     [Crossref] [Google Scholar]
  62. 62.
    Neidel S, Ren H, Torres AA, Smith GL. 2019.. NF-κB activation is a turn on for vaccinia virus phosphoprotein A49 to turn off NF-κB activation. . PNAS 116:(12):5699–704
     [Crossref] [Google Scholar]
  63. 63.
    Shisler JL, Jin X-L. 2004.. The vaccinia virus K1L gene product inhibits host NF-κB activation by preventing IκBα degradation. . J. Virol. 78:(7):3553–60
     [Crossref] [Google Scholar]
  64. 64.
    Mansur DS, Maluquer De Motes C, Unterholzner L, Sumner RP, Ferguson BJ, et al. 2013.. Poxvirus targeting of E3 ligase β-TrCP by molecular mimicry: a mechanism to inhibit NF-κB activation and promote immune evasion and virulence. . PLOS Pathog. 9:(2):e1003183
     [Crossref] [Google Scholar]
  65. 65.
    Herbert M, Squire C, Mercer A. 2015.. Poxviral ankyrin proteins. . Viruses 7:(2):709–38
     [Crossref] [Google Scholar]
  66. 66.
    Burles K, Van Buuren N, Barry M. 2014.. Ectromelia virus encodes a family of ankyrin/F-box proteins that regulate NFκB. . Virology 468–470::351–62
     [Crossref] [Google Scholar]
  67. 67.
    Odon V, Georgana I, Holley J, Morata J, Maluquer De Motes C. 2018.. Novel class of viral ankyrin proteins targeting the host E3 ubiquitin ligase cullin-2. . J. Virol. 92:(23):e01374-18
     [Crossref] [Google Scholar]
  68. 68.
    Chang S-J, Hsiao J-C, Sonnberg S, Chiang C-T, Yang M-H, et al. 2009.. Poxvirus host range protein CP77 contains an F-box-like domain that is necessary to suppress NF-κB activation by tumor necrosis factor alpha but is independent of its host range function. . J. Virol. 83:(9):4140–52
     [Crossref] [Google Scholar]
  69. 69.
    Pallett MA, Ren H, Zhang R-Y, Scutts SR, Gonzalez L, et al. 2019.. Vaccinia virus BBK E3 ligase adaptor A55 targets importin-dependent NF-κB activation and inhibits CD8+ T-cell memory. . J. Virol. 93:(10):e00051-19
     [Crossref] [Google Scholar]
  70. 70.
    Ember SWJ, Ren H, Ferguson BJ, Smith GL. 2012.. Vaccinia virus protein C4 inhibits NF-κB activation and promotes virus virulence. . J. Gen. Virol. 93:(10):2098–108
     [Crossref] [Google Scholar]
  71. 71.
    Bravo Cruz AG, Han A, Roy EJ, Guzmán AB, Miller RJ, et al. 2017.. Deletion of the K1L gene results in a vaccinia virus that is less pathogenic due to muted innate immune responses, yet still elicits protective immunity. . J. Virol. 91:(15):e00542-17
     [Crossref] [Google Scholar]
  72. 72.
    Huang B, Yang X-D, Zhou M-M, Ozato K, Chen L-F. 2009.. Brd4 coactivates transcriptional activation of NF-κB via specific binding to acetylated RelA. . Mol. Cell. Biol. 29:(5):1375–87
     [Crossref] [Google Scholar]
  73. 73.
    Mohamed MR, Rahman MM, Rice A, Moyer RW, Werden SJ, McFadden G. 2009.. Cowpox virus expresses a novel ankyrin repeat NF-κB inhibitor that controls inflammatory cell influx into virus-infected tissues and is critical for virus pathogenesis. . J. Virol. 83:(18):9223–36
     [Crossref] [Google Scholar]
  74. 74.
    Reading PC, Smith GL. 2003.. Vaccinia virus interleukin-18-binding protein promotes virulence by reducing gamma interferon production and natural killer and T-cell activity. . J. Virol. 77:(18):9960–68
     [Crossref] [Google Scholar]
  75. 75.
    Benfield CTO, Ren H, Lucas SJ, Bahsoun B, Smith GL. 2013.. Vaccinia virus protein K7 is a virulence factor that alters the acute immune response to infection. . J. Gen. Virol. 94:(7):1647–57
     [Crossref] [Google Scholar]
  76. 76.
    Tscharke DC, Reading PC, Smith GL. 2002.. Dermal infection with vaccinia virus reveals roles for virus proteins not seen using other inoculation routes. . J. Gen. Virol. 83:(8):1977–86
     [Crossref] [Google Scholar]
  77. 77.
    Albarnaz JD, Ren H, Torres AA, Shmeleva EV, Melo CA, et al. 2021.. Molecular mimicry of NF-κB by vaccinia virus protein enables selective inhibition of antiviral responses. . Nat. Microbiol. 7:(1):154–68
     [Crossref] [Google Scholar]
  78. 78.
    Hernáez B, Alonso-Lobo JM, Montanuy I, Fischer C, Sauer S, et al. 2018.. A virus-encoded type I interferon decoy receptor enables evasion of host immunity through cell-surface binding. . Nat. Commun. 9:(1):5440
     [Crossref] [Google Scholar]
  79. 79.
    Xu R-H, Cohen M, Tang Y, Lazear E, Whitbeck JC, et al. 2008.. The orthopoxvirus type I IFN binding protein is essential for virulence and an effective target for vaccination. . J. Exp. Med. 205:(4):981–92
     [Crossref] [Google Scholar]
  80. 80.
    Van Buuren N, Burles K, Schriewer J, Mehta N, Parker S, et al. 2014.. EVM005: an ectromelia-encoded protein with dual roles in NF-κB inhibition and virulence. . PLOS Pathog. 10:(8):e1004326
     [Crossref] [Google Scholar]
  81. 81.
    Rubio D, Xu R-H, Remakus S, Krouse TE, Truckenmiller ME, et al. 2013.. Crosstalk between the type 1 interferon and nuclear factor kappa B pathways confers resistance to a lethal virus infection. . Cell Host Microbe 13:(6):701–10
     [Crossref] [Google Scholar]
  82. 82.
    Taylor JM, Barry M. 2006.. Near death experiences: poxvirus regulation of apoptotic death. . Virology 344:(1):139–50
     [Crossref] [Google Scholar]
  83. 83.
    Kotwal GJ, Moss B. 1989.. Vaccinia virus encodes two proteins that are structurally related to members of the plasma serine protease inhibitor superfamily. . J. Virol. 63:(2):600–6
     [Crossref] [Google Scholar]
  84. 84.
    Smith GL, Howard ST, Chan YS. 1989.. Vaccinia virus encodes a family of genes with homology to serine proteinase inhibitors. . J. Gen. Virol. 70:(9):2333–43
     [Crossref] [Google Scholar]
  85. 85.
    Garcia-Calvo M, Peterson EP, Leiting B, Ruel R, Nicholson DW, Thornberry NA. 1998.. Inhibition of human caspases by peptide-based and macromolecular inhibitors. . J. Biol. Chem. 273:(49):32608–13
     [Crossref] [Google Scholar]
  86. 86.
    Zhou Q, Snipas S, Orth K, Muzio M, Dixit VM, Salvesen GS. 1997.. Target protease specificity of the viral serpin CrmA. . J. Biol. Chem. 272:(12):7797–800
     [Crossref] [Google Scholar]
  87. 87.
    Stewart TL, Wasilenko ST, Barry M. 2005.. Vaccinia virus F1L protein is a tail-anchored protein that functions at the mitochondria to inhibit apoptosis. . J. Virol. 79:(2):1084–98
     [Crossref] [Google Scholar]
  88. 88.
    Postigo A, Cross JR, Downward J, Way M. 2006.. Interaction of F1L with the BH3 domain of Bak is responsible for inhibiting vaccinia-induced apoptosis. . Cell Death Differ. 13:(10):1651–62
     [Crossref] [Google Scholar]
  89. 89.
    Wasilenko ST, Banadyga L, Bond D, Barry M. 2005.. The vaccinia virus F1L protein interacts with the proapoptotic protein Bak and inhibits Bak activation. . J. Virol. 79:(22):14031–43
     [Crossref] [Google Scholar]
  90. 90.
    Gerlic M, Faustin B, Postigo A, Yu EC-W, Proell M, et al. 2013.. Vaccinia virus F1L protein promotes virulence by inhibiting inflammasome activation. . PNAS 110:(19):7808–13
     [Crossref] [Google Scholar]
  91. 91.
    Cooray S, Bahar MW, Abrescia NGA, McVey CE, Bartlett NW, et al. 2007.. Functional and structural studies of the vaccinia virus virulence factor N1 reveal a Bcl-2-like anti-apoptotic protein. . J. Gen. Virol. 88:(6):1656–66
     [Crossref] [Google Scholar]
  92. 92.
    Ryerson MR, Richards MM, Kvansakul M, Hawkins CJ, Shisler JL. 2017.. Vaccinia virus encodes a novel inhibitor of apoptosis that associates with the apoptosome. . J. Virol. 91:(23):e01385-17
     [Crossref] [Google Scholar]
  93. 93.
    Gubser C, Bergamaschi D, Hollinshead M, Lu X, Van Kuppeveld FJM, Smith GL. 2007.. A new inhibitor of apoptosis from vaccinia virus and eukaryotes. . PLOS Pathog. 3:(2):e17
     [Crossref] [Google Scholar]
  94. 94.
    Saraiva N, Prole DL, Carrara G, De Motes CM, Johnson BF, et al. 2013.. Human and viral Golgi anti-apoptotic proteins (GAAPs) oligomerize via different mechanisms and monomeric GAAP inhibits apoptosis and modulates calcium. . J. Biol. Chem. 288:(18):13057–67
     [Crossref] [Google Scholar]
  95. 95.
    Kettle S, Khanna A, Alcamí A, Jassoy C, Ehret R, Smith GL. 1997.. Vaccinia virus serpin B13R (SPI-2) inhibits interleukin-1beta-converting enzyme and protects virus-infected cells from TNF- and Fas-mediated apoptosis, but does not prevent IL-1beta-induced fever. . J. Gen. Virol. 78:(3):677–85
     [Crossref] [Google Scholar]
  96. 96.
    Buller RM, Chakrabarti S, Cooper JA, Twardzik DR, Moss B. 1988.. Deletion of the vaccinia virus growth factor gene reduces virus virulence. . J. Virol. 62:(3):866–74
     [Crossref] [Google Scholar]
  97. 97.
    Pant A, Dsouza L, Cao S, Peng C, Yang Z. 2021.. Viral growth factor- and STAT3 signaling-dependent elevation of the TCA cycle intermediate levels during vaccinia virus infection. . PLOS Pathog. 17:(2):e1009303
     [Crossref] [Google Scholar]
  98. 98.
    Postigo A, Martin MC, Dodding MP, Way M. 2009.. Vaccinia-induced epidermal growth factor receptor-MEK signalling and the anti-apoptotic protein F1L synergize to suppress cell death during infection. . Cell Microbiol. 11:(8):1208–18
     [Crossref] [Google Scholar]
  99. 99.
    Beerli C, Yakimovich A, Kilcher S, Reynoso GV, Fläschner G, et al. 2019.. Vaccinia virus hijacks EGFR signalling to enhance virus spread through rapid and directed infected cell motility. . Nat. Microbiol. 4:(2):216–25
     [Crossref] [Google Scholar]
  100. 100.
    Bennett JR, Lateef Z, Fleming SB, Mercer AA, Wise LM. 2016.. Orf virus IL-10 reduces monocyte, dendritic cell and mast cell recruitment to inflamed skin. . Virus Res. 213::230–37
     [Crossref] [Google Scholar]
  101. 101.
    Fleming SB, Anderson IE, Thomson J, Deane DL, McInnes CJ, et al. 2007.. Infection with recombinant orf viruses demonstrates that the viral interleukin-10 is a virulence factor. . J. Gen. Virol. 88:(Part 7):1922–27
     [Crossref] [Google Scholar]
  102. 102.
    Fleming SB, Wise LM, Mercer AA. 2015.. Molecular genetic analysis of orf virus: a poxvirus that has adapted to skin. . Viruses 7:(3):1505–39
     [Crossref] [Google Scholar]
  103. 103.
    Bartlett NW, Dumoutier L, Renauld J-C, Kotenko SV, McVey CE, et al. 2004.. A new member of the interleukin 10-related cytokine family encoded by a poxvirus. . J. Gen. Virol. 85:(Part 6):1401–12
     [Crossref] [Google Scholar]
  104. 104.
    Savory LJ, Stacker SA, Fleming SB, Niven BE, Mercer AA. 2000.. Viral vascular endothelial growth factor plays a critical role in orf virus infection. . J. Virol. 74:(22):10699–706
     [Crossref] [Google Scholar]
  105. 105.
    Wise LM, Inder MK, Real NC, Stuart GS, Fleming SB, Mercer AA. 2012.. The vascular endothelial growth factor (VEGF)-E encoded by orf virus regulates keratinocyte proliferation and migration and promotes epidermal regeneration. . Cell Microbiol. 14:(9):1376–90
     [Crossref] [Google Scholar]
  106. 106.
    Lüttichau HR, Stine J, Boesen TP, Johnsen AH, Chantry D, et al. 2000.. A highly selective CC chemokine receptor (CCR)8 antagonist encoded by the poxvirus molluscum contagiosum. . J. Exp. Med. 191:(1):171–80
     [Crossref] [Google Scholar]
  107. 107.
    Comeau MR, Johnson R, DuBose RF, Petersen M, Gearing P, et al. 1998.. A poxvirus-encoded semaphorin induces cytokine production from monocytes and binds to a novel cellular semaphorin receptor, VESPR. . Immunity 8:(4):473–82
     [Crossref] [Google Scholar]
  108. 108.
    Liu H, Juo ZS, Shim AH-R, Focia PJ, Chen X, et al. 2010.. Structural basis of semaphorin-plexin recognition and viral mimicry from Sema7A and A39R complexes with PlexinC1. . Cell 142:(5):749–61
     [Crossref] [Google Scholar]
  109. 109.
    Walzer T, Galibert L, De Smedt T. 2005.. Poxvirus semaphorin A39R inhibits phagocytosis by dendritic cells and neutrophils. . Eur. J. Immunol. 35:(2):391–98
     [Crossref] [Google Scholar]
  110. 110.
    Walzer T, Galibert L, Comeau MR, De Smedt T. 2005.. Plexin C1 engagement on mouse dendritic cells by viral semaphorin A39R induces actin cytoskeleton rearrangement and inhibits integrin-mediated adhesion and chemokine-induced migration. . J. Immunol. 174:(1):51–59
     [Crossref] [Google Scholar]
  111. 111.
    Gardner JD, Tscharke DC, Reading PC, Smith GL. 2001.. Vaccinia virus semaphorin A39R is a 50–55 kDa secreted glycoprotein that affects the outcome of infection in a murine intradermal model. . J. Gen. Virol. 82:(Part 9):2083–93
     [Crossref] [Google Scholar]
  112. 112.
    Hernaez B, Alcamí A. 2020.. Virus-encoded cytokine and chemokine decoy receptors. . Curr. Opin. Immunol. 66::50–56
     [Crossref] [Google Scholar]
  113. 113.
    Alcamí A, Smith GL. 1992.. A soluble receptor for interleukin-1β encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. . Cell 71:(1):153–67
     [Crossref] [Google Scholar]
  114. 114.
    Spriggs MK, Hruby DE, Maliszewski CR, Pickup DJ, Sims JE, et al. 1992.. Vaccinia and cowpox viruses encode a novel secreted interleukin-1-binding protein. . Cell 71:(1):145–52
     [Crossref] [Google Scholar]
  115. 115.
    Alcamí A, Smith GL. 1996.. A mechanism for the inhibition of fever by a virus. . PNAS 93:(20):11029–34
     [Crossref] [Google Scholar]
  116. 116.
    Upton C, Mossman K, McFadden G. 1992.. Encoding of a homolog of the IFN-γ receptor by myxoma virus. . Science 258:(5086):1369–72
     [Crossref] [Google Scholar]
  117. 117.
    Alcamí A, Smith GL. 1995.. Vaccinia, cowpox, and camelpox viruses encode soluble gamma interferon receptors with novel broad species specificity. . J. Virol. 69:(8):4633–39
     [Crossref] [Google Scholar]
  118. 118.
    Nuara AA, Walter LJ, Logsdon NJ, Yoon SI, Jones BC, et al. 2008.. Structure and mechanism of IFN-γ antagonism by an orthopoxvirus IFN-γ-binding protein. . PNAS 105:(6):1861–66
     [Crossref] [Google Scholar]
  119. 119.
    Mossman K, Nation P, Macen J, Garbutt M, Lucas A, McFadden G. 1996.. Myxoma virus M-T7, a secreted homolog of the interferon-γ receptor, is a critical virulence factor for the development of myxomatosis in European rabbits. . Virology 215:(1):17–30
     [Crossref] [Google Scholar]
  120. 120.
    Krumm B, Meng X, Li Y, Xiang Y, Deng J. 2008.. Structural basis for antagonism of human interleukin 18 by poxvirus interleukin 18-binding protein. . PNAS 105:(52):20711–15
     [Crossref] [Google Scholar]
  121. 121.
    Xiang Y, Moss B. 1999.. IL-18 binding and inhibition of interferon γ induction by human poxvirus-encoded proteins. . PNAS 96:(20):11537–42
     [Crossref] [Google Scholar]
  122. 122.
    Smith VP, Bryant NA, Alcamí A. 2000.. Ectromelia, vaccinia and cowpox viruses encode secreted interleukin-18-binding proteins. . J. Gen. Virol. 81:(Part 5):1223–30
     [Google Scholar]
  123. 123.
    Born TL, Morrison LA, Esteban DJ, VandenBos T, Thebeau LG, et al. 2000.. A poxvirus protein that binds to and inactivates IL-18, and inhibits NK cell response. . J. Immunol. 164:(6):3246–54
     [Crossref] [Google Scholar]
  124. 124.
    Krumm B, Meng X, Wang Z, Xiang Y, Deng J. 2012.. A unique bivalent binding and inhibition mechanism by the yatapoxvirus interleukin 18 binding protein. . PLOS Pathog. 8:(8):e1002876
     [Crossref] [Google Scholar]
  125. 125.
    Xiang Y, Moss B. 2003.. Molluscum contagiosum virus interleukin-18 (IL-18) binding protein is secreted as a full-length form that binds cell surface glycosaminoglycans through the C-terminal tail and a furin-cleaved form with only the IL-18 binding domain. . J. Virol. 77:(4):2623–30
     [Crossref] [Google Scholar]
  126. 126.
    Esteban DJ, Nuara AA, Buller RML. 2004.. Interleukin-18 and glycosaminoglycan binding by a protein encoded by Variola virus. . J. Gen. Virol. 85:(Part 5):1291–99
     [Crossref] [Google Scholar]
  127. 127.
    Symons JA, Alcamí A, Smith GL. 1995.. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. . Cell 81:(4):551–60
     [Crossref] [Google Scholar]
  128. 128.
    Colamonici OR, Domanski P, Sweitzer SM, Larner A, Buller RM. 1995.. Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon α transmembrane signaling. . J. Biol. Chem. 270:(27):15974–78
     [Crossref] [Google Scholar]
  129. 129.
    del Mar Fernández de Marco M, Alejo A, Hudson P, Damon IK, Alcami A. 2010.. The highly virulent variola and monkeypox viruses express secreted inhibitors of type I interferon. . FASEB J. 24:(5):1479–88
     [Crossref] [Google Scholar]
  130. 130.
    Alcamí A, Symons JA, Smith GL. 2000.. The vaccinia virus soluble alpha/beta interferon (IFN) receptor binds to the cell surface and protects cells from the antiviral effects of IFN. . J. Virol. 74:(23):11230–39
     [Crossref] [Google Scholar]
  131. 131.
    Montanuy I, Alejo A, Alcami A. 2011.. Glycosaminoglycans mediate retention of the poxvirus type I interferon binding protein at the cell surface to locally block interferon antiviral responses. . FASEB J. 25:(6):1960–71
     [Crossref] [Google Scholar]
  132. 132.
    Deane D, McInnes CJ, Percival A, Wood A, Thomson J, et al. 2000.. Orf virus encodes a novel secreted protein inhibitor of granulocyte-macrophage colony-stimulating factor and interleukin-2. . J. Virol. 74:(3):1313–20
     [Crossref] [Google Scholar]
  133. 133.
    Nelson CA, Epperson ML, Singh S, Elliott JI, Fremont DH. 2015.. Structural conservation and functional diversity of the poxvirus immune evasion (PIE) domain superfamily. . Viruses 7:(9):4878–98
     [Crossref] [Google Scholar]
  134. 134.
    Felix J, Kandiah E, De Munck S, Bloch Y, van Zundert GCP, et al. 2016.. Structural basis of GM-CSF and IL-2 sequestration by the viral decoy receptor GIF. . Nat. Commun. 7::13228
     [Crossref] [Google Scholar]
  135. 135.
    Martins M, Rodrigues FS, Joshi LR, Jardim JC, Flores MM, et al. 2021.. Orf virus ORFV112, ORFV117 and ORFV127 contribute to ORFV IA82 virulence in sheep. . Vet. Microbiol. 257::109066
     [Crossref] [Google Scholar]
  136. 136.
    Alvarez-de Miranda FJ, Alonso-Sánchez I, Alcamí A, Hernaez B. 2021.. TNF decoy receptors encoded by poxviruses. . Pathogens 10:(8):1065
     [Crossref] [Google Scholar]
  137. 137.
    Smith CA, Davis T, Wignall JM, Din WS, Farrah T, et al. 1991.. T2 open reading frame from Shope fibroma virus encodes a soluble form of the TNF receptor. . Biochem. Biophys. Res. Commun. 176::335–42
     [Crossref] [Google Scholar]
  138. 138.
    Hu F, Smith CA, Pickup DJ. 1994.. Cowpox virus contains two copies of an early gene encoding a soluble secreted form of the type II TNF receptor. . Virology 204::343–56
     [Crossref] [Google Scholar]
  139. 139.
    Smith CA, Hu FQ, Smith TD, Richards CL, Smolak P, et al. 1996.. Cowpox virus genome encodes a second soluble homologue of cellular TNF receptors, distinct from CrmB, that binds TNF but not LTα. . Virology 223::132–47
     [Crossref] [Google Scholar]
  140. 140.
    Loparev VN, Parsons JM, Knight JC, Panus JF, Ray CA, et al. 1998.. A third distinct tumor necrosis factor receptor of orthopoxviruses. . PNAS 95:(7):3786–91
     [Crossref] [Google Scholar]
  141. 141.
    Saraiva M, Alcami A. 2001.. CrmE, a novel soluble tumor necrosis factor receptor encoded by poxviruses. . J. Virol. 75:(1):226–33
     [Crossref] [Google Scholar]
  142. 142.
    Pontejo SM, Alejo A, Alcami A. 2015.. Comparative biochemical and functional analysis of viral and human secreted tumor necrosis factor (TNF) decoy receptors. . J. Biol. Chem. 290:(26):15973–84
     [Crossref] [Google Scholar]
  143. 143.
    Pontejo SM, Sanchez C, Ruiz-Argüello B, Alcami A. 2019.. Insights into ligand binding by a viral tumor necrosis factor (TNF) decoy receptor yield a selective soluble human type 2 TNF receptor. . J. Biol. Chem. 294:(13):5214–27
     [Crossref] [Google Scholar]
  144. 144.
    Schreiber M, Rajarathnam K, McFadden G. 1996.. Myxoma virus T2 protein, a tumor necrosis factor (TNF) receptor homolog, is secreted as a monomer and dimer that each bind rabbit TNFα, but the dimer is a more potent TNF inhibitor. . J. Biol. Chem. 271:(23):13333–41
     [Crossref] [Google Scholar]
  145. 145.
    Alcamí A, Khanna A, Paul NL, Smith GL. 1999.. Vaccinia virus strains Lister, USSR and Evans express soluble and cell-surface tumour necrosis factor receptors. . J. Gen. Virol. 80:(Part 4):949–59
     [Crossref] [Google Scholar]
  146. 146.
    Reading PC, Khanna A, Smith GL. 2002.. Vaccinia virus CrmE encodes a soluble and cell surface tumor necrosis factor receptor that contributes to virus virulence. . Virology 292:(2):285–98
     [Crossref] [Google Scholar]
  147. 147.
    Pontejo SM, Alejo A, Alcami A. 2015.. Poxvirus-encoded TNF decoy receptors inhibit the biological activity of transmembrane TNF. . J. Gen. Virol. 96:(10):3118–23
     [Crossref] [Google Scholar]
  148. 148.
    Juhász K, Buzás K, Duda E. 2013.. Importance of reverse signaling of the TNF superfamily in immune regulation. . Expert Rev. Clin. Immunol. 9:(4):335–48
     [Crossref] [Google Scholar]
  149. 149.
    Al Rumaih Z, Tuazon Kels MJ, Ng E, Pandey P, Pontejo SM, et al. 2020.. Poxvirus-encoded TNF receptor homolog dampens inflammation and protects from uncontrolled lung pathology during respiratory infection. . PNAS 117:(43):26885–94
     [Crossref] [Google Scholar]
  150. 150.
    Schreiber M, Sedger L, McFadden G. 1997.. Distinct domains of M-T2, the myxoma virus tumor necrosis factor (TNF) receptor homolog, mediate extracellular TNF binding and intracellular apoptosis inhibition. . J. Virol. 71:(3):2171–81
     [Crossref] [Google Scholar]
  151. 151.
    Alejo A, Ruiz-Argüello MB, Ho Y, Smith VP, Saraiva M, Alcami A. 2006.. A chemokine-binding domain in the tumor necrosis factor receptor from variola (smallpox) virus. . PNAS 103:(15):5995–6000
     [Crossref] [Google Scholar]
  152. 152.
    Alejo A, Ruiz-Argüello MB, Pontejo SM, del Mar Fernandez de Marco M, Saraiva M, et al. 2018.. Chemokines cooperate with TNF to provide protective anti-viral immunity and to enhance inflammation. . Nat. Commun. 9:(1):1790
     [Crossref] [Google Scholar]
  153. 153.
    Brunetti CR, Paulose-Murphy M, Singh R, Qin J, Barrett JW, et al. 2003.. A secreted high-affinity inhibitor of human TNF from Tanapox virus. . PNAS 100:(8):4831–36
     [Crossref] [Google Scholar]
  154. 154.
    Rahman MM, Barrett JW, Brouckaert P, McFadden G. 2006.. Variation in ligand binding specificities of a novel class of poxvirus-encoded tumor necrosis factor-binding protein. . J. Biol. Chem. 281:(32):22517–26
     [Crossref] [Google Scholar]
  155. 155.
    Yang Z, West AP, Bjorkman PJ. 2009.. Crystal structure of TNFα complexed with a poxvirus MHC-related TNF binding protein. . Nat. Struct. Mol. Biol. 16:(11):1189–91
     [Crossref] [Google Scholar]
  156. 156.
    Rahman MM, Jeng D, Singh R, Coughlin J, Essani K, McFadden G. 2009.. Interaction of human TNF and β2-microglobulin with Tanapox virus-encoded TNF inhibitor, TPV-2L. . Virology 386:(2):462–68
     [Crossref] [Google Scholar]
  157. 157.
    Saraiva M, Smith P, Fallon PG, Alcami A. 2002.. Inhibition of type 1 cytokine-mediated inflammation by a soluble CD30 homologue encoded by ectromelia (mousepox) virus. . J. Exp. Med. 196::829–39
     [Crossref] [Google Scholar]
  158. 158.
    Panus JF, Smith CA, Ray CA, Smith TD, Patel DD, Pickup DJ. 2002.. Cowpox virus encodes a fifth member of the tumor necrosis factor receptor family: a soluble, secreted CD30 homologue. . PNAS 99:(12):8348–53
     [Crossref] [Google Scholar]
  159. 159.
    Alejo A, Saraiva M, Ruiz-Argüello MB, Viejo-Borbolla A, de Marco MF, et al. 2009.. A method for the generation of ectromelia virus (ECTV) recombinants: in vivo analysis of ECTV vCD30 deletion mutants. . PLOS ONE 4:(4):e5175
     [Crossref] [Google Scholar]
  160. 160.
    Bonecchi R, Savino B, Borroni EM, Mantovani A, Locati M. 2010.. Chemokine decoy receptors: structure-function and biological properties. . Curr. Top. Microbiol. Immunol. 341::15–36
     [Google Scholar]
  161. 161.
    Heidarieh H, Hernáez B, Alcamí A. 2015.. Immune modulation by virus-encoded secreted chemokine binding proteins. . Virus Res. 209::67–75
     [Crossref] [Google Scholar]
  162. 162.
    Graham KA, Lalani AS, Macen JL, Ness TL, Barry M, et al. 1997.. The T1/35kDa family of poxvirus-secreted proteins bind chemokines and modulate leukocyte influx into virus-infected tissues. . Virology 229:(1):12–24
     [Crossref] [Google Scholar]
  163. 163.
    Smith CA, Smith TD, Smolak PJ, Friend D, Hagen H, et al. 1997.. Poxvirus genomes encode a secreted, soluble protein that preferentially inhibits β chemokine activity yet lacks sequence homology to known chemokine receptors. . Virology 236:(2):316–27
     [Crossref] [Google Scholar]
  164. 164.
    Alcamí A, Symons JA, Collins PD, Williams TJ, Smith GL. 1998.. Blockade of chemokine activity by a soluble chemokine binding protein from vaccinia virus. . J. Immunol. 160:(2):624–33
     [Crossref] [Google Scholar]
  165. 165.
    Martinez-Pomares L, Thompson JP, Moyer RW. 1995.. Mapping and investigation of the role in pathogenesis of the major unique secreted 35-kDa protein of rabbitpox virus. . Virology 206:(1):591–600
     [Crossref] [Google Scholar]
  166. 166.
    Reading PC, Symons JA, Smith GL. 2003.. A soluble chemokine-binding protein from vaccinia virus reduces virus virulence and the inflammatory response to infection. . J. Immunol. 170:(3):1435–42
     [Crossref] [Google Scholar]
  167. 167.
    Seet BT, Barrett J, Robichaud J, Shilton B, Singh R, McFadden G. 2001.. Glycosaminoglycan binding properties of the myxoma virus CC-chemokine inhibitor, M-T1. . J. Biol. Chem. 276:(32):30504–13
     [Crossref] [Google Scholar]
  168. 168.
    Couñago RM, Knapp KM, Nakatani Y, Fleming SB, Corbett M, et al. 2015.. Structures of Orf virus chemokine binding protein in complex with host chemokines reveal clues to broad binding specificity. . Structure 23:(7):1199–213
     [Crossref] [Google Scholar]
  169. 169.
    Sharif S, Ueda N, Nakatani Y, Wise LM, Clifton S, et al. 2019.. Chemokine-binding proteins encoded by parapoxvirus of red deer of New Zealand display evidence of gene duplication and divergence of ligand specificity. . Front. Microbiol. 10::1421
     [Crossref] [Google Scholar]
  170. 170.
    Ng A, Tscharke DC, Reading PC, Smith GL. 2001.. The vaccinia virus A41L protein is a soluble 30 kDa glycoprotein that affects virus virulence. . J. Gen. Virol. 82:(Part 9):2095–105
     [Crossref] [Google Scholar]
  171. 171.
    Bahar MW, Kenyon JC, Putz MM, Abrescia NG, Pease JE, et al. 2008.. Structure and function of A41, a vaccinia virus chemokine binding protein. . PLOS Pathog. 4:(1):e5
     [Crossref] [Google Scholar]
  172. 172.
    Ruiz-Argüello MB, Smith VP, Campanella GS, Baleux F, Arenzana-Seisdedos F, et al. 2008.. An ectromelia virus protein that interacts with chemokines through their glycosaminoglycan binding domain. . J. Virol. 82:(2):917–26
     [Crossref] [Google Scholar]
  173. 173.
    Handel TM, Johnson Z, Crown SE, Lau EK, Proudfoot AE. 2005.. Regulation of protein function by glycosaminoglycans—as exemplified by chemokines. . Annu. Rev. Biochem. 74::385–410
     [Crossref] [Google Scholar]
  174. 174.
    Heidarieh H, Alcamí A. 2018.. Mechanism of action of the viral chemokine binding protein E163 from ectromelia virus. . J. Biol. Chem. 293:(45):17418–29
     [Crossref] [Google Scholar]
  175. 175.
    Xue X, Lu Q, Wei H, Wang D, Chen D, et al. 2011.. Structural basis of chemokine sequestration by CrmD, a poxvirus-encoded tumor necrosis factor receptor. . PLOS Pathog. 7:(7):e1002162
     [Crossref] [Google Scholar]
  176. 176.
    Price N, Tscharke DC, Hollinshead M, Smith GL. 2000.. Vaccinia virus gene B7R encodes an 18-kDa protein that is resident in the endoplasmic reticulum and affects virus virulence. . Virology 267:(1):65–79
     [Crossref] [Google Scholar]
  177. 177.
    Iyer RF, Edwards DM, Kolb P, Raué H-P, Nelson CA, et al. 2022.. The secreted protein Cowpox Virus 14 contributes to viral virulence and immune evasion by engaging Fc-gamma-receptors. . PLOS Pathog. 18:(9):e1010783
     [Crossref] [Google Scholar]
  178. 178.
    Lalani AS, Graham K, Mossman K, Rajarathnam K, Clark-Lewis I, et al. 1997.. The purified myxoma virus gamma interferon receptor homolog M-T7 interacts with the heparin-binding domains of chemokines. . J. Virol. 71:(6):4356–63
     [Crossref] [Google Scholar]
  179. 179.
    Najarro P, Gubser C, Hollinshead M, Fox J, Pease J, Smith GL. 2006.. Yaba-like disease virus chemokine receptor 7L, a CCR8 orthologue. . J. Gen. Virol. 87:(Part 4):809–16
     [Crossref] [Google Scholar]
  180. 180.
    Sigal LJ. 2016.. The pathogenesis and immunobiology of mousepox. . Adv. Immunol. 129::251–76
     [Google Scholar]
  181. 181.
    Panchanathan V, Chaudhri G, Karupiah G. 2008.. Correlates of protective immunity in poxvirus infection: Where does antibody stand?. Immunol. Cell Biol. 86:(1):80–86
     [Crossref] [Google Scholar]
  182. 182.
    Alzhanova D, Edwards DM, Hammarlund E, Scholz IG, Horst D, et al. 2009.. Cowpox virus inhibits the transporter associated with antigen processing to evade T cell recognition. . Cell Host Microbe 6:(5):433–45
     [Crossref] [Google Scholar]
  183. 183.
    Byun M, Wang X, Pak M, Hansen TH, Yokoyama WM. 2007.. Cowpox virus exploits the endoplasmic reticulum retention pathway to inhibit MHC class I transport to the cell surface. . Cell Host Microbe 2:(5):306–15
     [Crossref] [Google Scholar]
  184. 184.
    Wang X, Piersma SJ, Elliott JI, Errico JM, Gainey MD, et al. 2019.. Cowpox virus encodes a protein that binds B7.1 and B7.2 and subverts T cell costimulation. . PNAS 116:(42):21113–19
     [Crossref] [Google Scholar]
  185. 185.
    Kleinpeter P, Remy-Ziller C, Winter E, Gantzer M, Nourtier V, et al. 2019.. By binding CD80 and CD86, the vaccinia virus M2 protein blocks their interactions with both CD28 and CTLA4 and potentiates CD80 binding to PD-L1. . J. Virol. 93:(11):e00207-19
     [Crossref] [Google Scholar]
  186. 186.
    Albarnaz JD, Torres AA, Smith GL. 2018.. Modulating vaccinia virus immunomodulators to improve immunological memory. . Viruses 10:(3):101
     [Crossref] [Google Scholar]
  187. 187.
    Gedey R, Jin X-L, Hinthong O, Shisler JL. 2006.. Poxviral regulation of the host NF-κB response: The vaccinia virus M2L protein inhibits induction of NF-κB activation via an ERK2 pathway in virus-infected human embryonic kidney cells. . J. Virol. 80:(17):8676–85
     [Crossref] [Google Scholar]
  188. 188.
    Guerin J-L, Gelfi J, Boullier S, Delverdier M, Bellanger F-A, et al. 2002.. Myxoma virus leukemia-associated protein is responsible for major histocompatibility complex class I and Fas-CD95 down-regulation and defines scrapins, a new group of surface cellular receptor abductor proteins. . J. Virol. 76:(6):2912–23
     [Crossref] [Google Scholar]
  189. 189.
    Mansouri M, Bartee E, Gouveia K, Hovey Nerenberg BT, Barrett J, et al. 2003.. The PHD/LAP-domain protein M153R of myxomavirus is a ubiquitin ligase that induces the rapid internalization and lysosomal destruction of CD4. . J. Virol. 77:(2):1427–40
     [Crossref] [Google Scholar]
  190. 190.
    Rehm KE, Connor RF, Jones GJB, Yimbu K, Roper RL. 2010.. Vaccinia virus A35R inhibits MHC class II antigen presentation. . Virology 397:(1):176–86
     [Crossref] [Google Scholar]
  191. 191.
    Alzhanova D, Hammarlund E, Reed J, Meermeier E, Rawlings S, et al. 2014.. T cell inactivation by poxviral B22 family proteins increases viral virulence. . PLOS Pathog. 10:(5):e1004123
     [Crossref] [Google Scholar]
  192. 192.
    Forsyth KS, Roy NH, Peauroi E, DeHaven BC, Wold ED, et al. 2020.. Ectromelia-encoded virulence factor C15 specifically inhibits antigen presentation to CD4+ T cells post peptide loading. . PLOS Pathog. 16:(8):e1008685
     [Crossref] [Google Scholar]
  193. 193.
    Peauroi EM, Carro SD, Pei L, Reynoso GV, Hickman HD, Eisenlohr LC. 2022.. The ectromelia virus virulence factor C15 facilitates early viral spread by inhibiting NK cell contact. . iScience 25:(12):105510
     [Crossref] [Google Scholar]
  194. 194.
    Reynolds SE, Earl PL, Minai M, Moore I, Moss B. 2017.. A homolog of the variola virus B22 membrane protein contributes to ectromelia virus pathogenicity in the mouse footpad model. . Virology 501::107–14
     [Crossref] [Google Scholar]
  195. 195.
    Harvey IB, Wang X, Fremont DH. 2019.. Molluscum contagiosum virus MC80 sabotages MHC-I antigen presentation by targeting tapasin for ER-associated degradation. . PLOS Pathog. 15:(4):e1007711
     [Crossref] [Google Scholar]
  196. 196.
    Elasifer H, Wang ECY, Prod'homme V, Davies J, Forbes S, et al. 2020.. Downregulation of HLA-I by the molluscum contagiosum virus mc080 impacts NK-cell recognition and promotes CD8+ T-cell evasion. . J. Gen. Virol. 101:(8):863–72
     [Crossref] [Google Scholar]
  197. 197.
    Jarahian M, Fiedler M, Cohnen A, Djandji D, Hämmerling GJ, et al. 2011.. Modulation of NKp30- and NKp46-mediated natural killer cell responses by poxviral hemagglutinin. . PLOS Pathog. 7:(8):e1002195
     [Crossref] [Google Scholar]
  198. 198.
    Campbell JA, Trossman DS, Yokoyama WM, Carayannopoulos LN. 2007.. Zoonotic orthopoxviruses encode a high-affinity antagonist of NKG2D. . J. Exp. Med. 204:(6):1311–17
     [Crossref] [Google Scholar]
  199. 199.
    Lazear E, Peterson LW, Nelson CA, Fremont DH. 2013.. Crystal structure of the cowpox virus-encoded NKG2D ligand OMCP. . J. Virol. 87:(2):840–50
     [Crossref] [Google Scholar]
  200. 200.
    Campbell JA, Davis RS, Lilly LM, Fremont DH, French AR, Carayannopoulos LN. 2010.. Cutting edge: FcR-like 5 on innate B cells is targeted by a poxvirus MHC class I-like immunoevasin. . J. Immunol. 185:(1):28–32
     [Crossref] [Google Scholar]
  201. 201.
    Weaver JR, Isaacs SN. 2008.. Monkeypox virus and insights into its immunomodulatory proteins. . Immunol. Rev. 225::96–113
     [Crossref] [Google Scholar]
  202. 202.
    Liszewski MK, Bertram P, Leung MK, Hauhart R, Zhang L, Atkinson JP. 2008.. Smallpox inhibitor of complement enzymes (SPICE): regulation of complement activation on cells and mechanism of its cellular attachment. . J. Immunol. 181:(6):4199–207
     [Crossref] [Google Scholar]
  203. 203.
    DeHaven BC, Gupta K, Isaacs SN. 2011.. The vaccinia virus A56 protein: a multifunctional transmembrane glycoprotein that anchors two secreted viral proteins. . J. Gen. Virol. 92:(Part 9):1971–80
     [Crossref] [Google Scholar]
  204. 204.
    Rosengard AM, Liu Y, Nie Z, Jimenez R. 2002.. Variola virus immune evasion design: expression of a highly efficient inhibitor of human complement. . PNAS 99:(13):8808–13
     [Crossref] [Google Scholar]
  205. 205.
    Hudson PN, Self J, Weiss S, Braden Z, Xiao Y, et al. 2012.. Elucidating the role of the complement control protein in monkeypox pathogenicity. . PLOS ONE 7:(4):e35086
     [Crossref] [Google Scholar]
  206. 206.
    Vanderplasschen A, Mathew E, Hollinshead M, Sim RB, Smith GL. 1998.. Extracellular enveloped vaccinia virus is resistant to complement because of incorporation of host complement control proteins into its envelope. . PNAS 95:(13):7544–49
     [Crossref] [Google Scholar]
  207. 207.
    Mutz P, Resch W, Faure G, Senkevich TG, Koonin EV, Moss B. 2023.. Exaptation of inactivated host enzymes for structural roles in orthopoxviruses and novel folds of virus proteins revealed by protein structure modeling. . mBio 14:(2):e0040823
     [Crossref] [Google Scholar]
  208. 208.
    Hernaez B, Alcami A. 2018.. New insights into the immunomodulatory properties of poxvirus cytokine decoy receptors at the cell surface. . F1000Research 7::719
     [Crossref] [Google Scholar]
  209. 209.
    Shchelkunov SN, Totmenin AV, Loparev VN, Safronov PF, Gutorov VV, et al. 2000.. Alastrim smallpox variola minor virus genome DNA sequences. . Virology 266:(2):361–86
     [Crossref] [Google Scholar]
  210. 210.
    Isidro J, Borges V, Pinto M, Sobral D, Santos JD, et al. 2022.. Phylogenomic characterization and signs of microevolution in the 2022 multi-country outbreak of monkeypox virus. . Nat. Med. 28:(8):1569–72
     [Crossref] [Google Scholar]
  211. 211.
    Yaron JR, Zhang L, Guo Q, Burgin M, Schutz LN, et al. 2020.. Deriving immune modulating drugs from viruses—a new class of biologics. . J. Clin. Med. 9:(4):972
     [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-immunol-090222-110227
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Poxvirus Immune Evasion
Annual Review of Immunology 42, 551 (2024); https://doi.org/10.1146/annurev-immunol-090222-110227
/content/journals/10.1146/annurev-immunol-090222-110227
/content/journals/10.1146/annurev-immunol-090222-110227
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  • Article Type: Review Article

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