Skip to main content

Advertisement

SpringerLink
Log in

Herpesviral capture of immunomodulatory host genes

  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

Herpesviruses have acquired numerous genes from their hosts. Although these homologs are not essential for viral replication, they often have important immunomodulatory functions that ensure viral persistence in the host. Some of these viral molecules are called virokines as they mimic cellular cytokines of their host such as interleukin-10 (cIL-10). In recent years, many viral homologs of IL-10 (vIL-10s) have been discovered in the genome of members of the order Herpesvirales. For some, gene and protein structure as well as biological activity and potential use in the clinical context have been explored. Besides virokines, herpesviruses have also captured genes encoding membrane-bound host immunomodulatory proteins such as major histocompatibility complex (MHC) molecules. These viral MHC mimics also retain many of the functions of the cellular genes, in particular directly or indirectly modulating the activity of natural killer cells. The mechanisms underlying capture of cellular genes by large DNA viruses are still enigmatic. In this review, we provide an update of the advances in the field of herpesviral gene piracy and discuss possible scenarios that could explain how the gene transfer from host to viral genome was achieved.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. N.C. Elde, H.S. Malik, Nat. Rev. Microbiol. 7, 787–797 (2009)

    Article  CAS  PubMed  Google Scholar 

  2. M. Raftery, A. Muller, G. Schonrich, Virus Genes 21, 65–75 (2000)

    Article  CAS  PubMed  Google Scholar 

  3. R. Holzerlandt, C. Orengo, P. Kellam, M.M. Alba, Genome Res. 12, 1739–1748 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. L.A. Shackelton, E.C. Holmes, Trends Microbiol. 12, 458–465 (2004)

    Article  CAS  PubMed  Google Scholar 

  5. D.J. McGeoch, F.J. Rixon, A.J. Davison, Virus Res. 117, 90–104 (2006)

    Article  CAS  PubMed  Google Scholar 

  6. P.E. Pellett, B. Roizman, in Fields virology, ed. by D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman (Lippincott Williams & Wilkins, Philadelphia, 2013), pp. 1802–1822

    Google Scholar 

  7. D.J. McGeoch, S. Cook, A. Dolan, F.E. Jamieson, E.A. Telford, J. Mol. Biol. 247, 443–458 (1995)

    Article  CAS  PubMed  Google Scholar 

  8. P.E. Pellett, J. Virol. 88, 13520–13522 (2014)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. S.A. Connolly, J.O. Jackson, T.S. Jardetzky, R. Longnecker, Nat. Rev. Microbiol. 9, 369–381 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. A.V. Nicola, Traffic 17, 965–975 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. M.P. Taylor, O.O. Koyuncu, L.W. Enquist, Nat. Rev. Microbiol. 9, 427–439 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. T.C. Mettenleiter, J. Mol. Biol. 428, 1949–1961 (2016)

    Article  CAS  PubMed  Google Scholar 

  13. A.J. Davison, A. Dolan, P. Akter, C. Addison, D.J. Dargan, D.J. Alcendor, D.J. McGeoch, G.S. Hayward, J. Gen. Virol. 84, 17–28 (2003)

    Article  CAS  PubMed  Google Scholar 

  14. A.J. Davison, T. Kurobe, D. Gatherer, C. Cunningham, I. Korf, H. Fukuda, R.P. Hedrick, T.B. Waltzek, J. Virol. 87, 2908–2922 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. G. Dominguez, T.R. Dambaugh, F.R. Stamey, S. Dewhurst, N. Inoue, P.E. Pellett, J. Virol. 73, 8040–8052 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  16. E. Van Damme, K. Thys, M. Tuefferd, C. Van Hove, J. Aerssens, M. Van Loock, PLoS ONE 11, e0164843 (2016)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. A. Alcami, Nat. Rev. Immunol. 3, 36–50 (2003)

    Article  CAS  PubMed  Google Scholar 

  18. W. Ouyang, S. Rutz, N.K. Crellin, P.A. Valdez, S.G. Hymowitz, Annu. Rev. Immunol. 29, 71–109 (2011)

    Article  CAS  PubMed  Google Scholar 

  19. E.B. Wilson, D.G. Brooks, Curr. Top. Microbiol. Immunol. 350, 39–65 (2011)

    CAS  PubMed  PubMed Central  Google Scholar 

  20. K.W. Moore, P. Vieira, D.F. Fiorentino, M.L. Trounstine, T.A. Khan, T.R. Mosmann, Science 248, 1230–1234 (1990)

    Article  CAS  PubMed  Google Scholar 

  21. S.V. Kotenko, S. Saccani, L.S. Izotova, O.V. Mirochnitchenko, S. Pestka, Proc Natl Acad Sci USA 97, 1695–1700 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. K.M. Lockridge, S.S. Zhou, R.H. Kravitz, J.L. Johnson, E.T. Sawai, E.L. Blewett, P.A. Barry, Virology 268, 272–280 (2000)

    Article  CAS  PubMed  Google Scholar 

  23. W.L. Chang, N. Baumgarth, D. Yu, P.A. Barry, J. Virol. 78, 8720–8731 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. J.V. Spencer, K.M. Lockridge, P.A. Barry, G. Lin, M. Tsang, M.E. Penfold, T.J. Schall, J. Virol. 76, 1285–1292 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. C. Jenkins, A. Abendroth, B. Slobedman, J. Virol. 78, 1440–1447 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. C. Jenkins, W. Garcia, A. Abendroth, B. Slobedman, Virology 370, 285–294 (2008)

    Article  CAS  PubMed  Google Scholar 

  27. C. Cunningham, D. Gatherer, B. Hilfrich, K. Baluchova, D.J. Dargan, M. Thomson, P.D. Griffiths, G.W. Wilkinson, T.F. Schulz, A.J. Davison, J. Gen. Virol. 91, 605–615 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. I. Garrigue, M.F. Corte, N. Magnin, L. Couzi, S. Capdepont, C. Rio, P. Merville, J. Dechanet-Merville, H. Fleury, M.E. Lafon, J. Clin. Virol. 40, 120–128 (2007)

    Article  CAS  PubMed  Google Scholar 

  29. P. Ouyang, K. Rakus, S.J. van Beurden, A.H. Westphal, A.J. Davison, D. Gatherer, A.F. Vanderplasschen, J. Gen. Virol. 95, 245–262 (2014)

    Article  CAS  PubMed  Google Scholar 

  30. B. Michel, G. Fournier, F. Lieffrig, B. Costes, A. Vanderplasschen, Emerg. Infect. Dis. 16, 1835–1843 (2010)

    Article  PubMed  PubMed Central  Google Scholar 

  31. P. Ouyang, K. Rakus, M. Boutier, A. Reschner, B. Leroy, M. Ronsmans, G. Fournier, S. Scohy, B. Costes, R. Wattiez, A. Vanderplasschen, Vet. Res. 44, 53 (2013)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. M.C. Piazzon, A.S. Wentzel, E.J. Tijhaar, K.L. Rakus, A. Vanderplasschen, G.F. Wiegertjes, M. Forlenza, J Immunol 195, 3694–3704 (2015)

    Article  CAS  PubMed  Google Scholar 

  33. F. Gandar, G.S. Wilkie, D. Gatherer, K. Kerr, D. Marlier, M. Diez, R.E. Marschang, J. Mast, B.G. Dewals, A.J. Davison, A.F. Vanderplasschen, J. Virol. 89, 11438–11456 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. B. Ehlers, K. Spiess, F. Leendertz, M. Peeters, C. Boesch, D. Gatherer, D.J. McGeoch, J. Gen. Virol. 91, 630–642 (2010)

    Article  CAS  PubMed  Google Scholar 

  35. J. Hart, M. Ackermann, G. Jayawardane, G. Russell, D.M. Haig, H. Reid, J.P. Stewart, J. Gen. Virol. 88, 28–39 (2007)

    Article  CAS  PubMed  Google Scholar 

  36. G. Jayawardane, G.C. Russell, J. Thomson, D. Deane, H. Cox, D. Gatherer, M. Ackermann, D.M. Haig, J.P. Stewart, J. Gen. Virol. 89, 2447–2455 (2008)

    Article  CAS  PubMed  Google Scholar 

  37. B.C. Jones, N.J. Logsdon, K. Josephson, J. Cook, P.A. Barry, M.R. Walter, Proc Natl Acad Sci USA 99, 9404–9409 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. L. Hertel, V.G. Lacaille, H. Strobl, E.D. Mellins, E.S. Mocarski, J. Virol. 77, 7563–7574 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. M. Moutaftsi, A.M. Mehl, L.K. Borysiewicz, Z. Tabi, Blood 99, 2913–2921 (2002)

    Article  CAS  PubMed  Google Scholar 

  40. M.J. Raftery, M. Schwab, S.M. Eibert, Y. Samstag, H. Walczak, G. Schonrich, Immunity 15, 997–1009 (2001)

    Article  CAS  PubMed  Google Scholar 

  41. S. Riegler, H. Hebart, H. Einsele, P. Brossart, G. Jahn, C. Sinzger, J. Gen. Virol. 81, 393–399 (2000)

    Article  CAS  PubMed  Google Scholar 

  42. S. Avdic, B.P. McSharry, B. Slobedman, Front. Microbiol. 5, 337 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  43. S. Avdic, J.Z. Cao, B.P. McSharry, L.E. Clancy, R. Brown, M. Steain, D.J. Gottlieb, A. Abendroth, B. Slobedman, J. Virol. 87, 10273–10282 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. A.K. Cheung, D.J. Gottlieb, B. Plachter, S. Pepperl-Klindworth, S. Avdic, A.L. Cunningham, A. Abendroth, B. Slobedman, Blood 114, 4128–4137 (2009)

    Article  CAS  PubMed  Google Scholar 

  45. A. Jaworowski, W.J. Cheng, C.L. Westhorpe, A. Abendroth, S.M. Crowe, B. Slobedman, Virology 391, 20–24 (2009)

    Article  CAS  PubMed  Google Scholar 

  46. C. Jenkins, W. Garcia, M.J. Godwin, J.V. Spencer, J.L. Stern, A. Abendroth, B. Slobedman, J. Virol. 82, 3736–3750 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. M.J. Raftery, M. Hitzler, F. Winau, T. Giese, B. Plachter, S.H. Kaufmann, G. Schonrich, J. Virol. 82, 4308–4319 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. M.J. Raftery, D. Wieland, S. Gronewald, A.A. Kraus, T. Giese, G. Schonrich, J Immunol. 173, 3383–3391 (2004)

    Article  CAS  PubMed  Google Scholar 

  49. S. Avdic, J.Z. Cao, A.K. Cheung, A. Abendroth, B. Slobedman, J. Virol. 85, 7465–7471 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. N.J. Logsdon, M.K. Eberhardt, C.E. Allen, P.A. Barry, M.R. Walter, PLoS ONE 6, e28127 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. E.D. Carosella, N. Rouas-Freiss, Roux D. Tronik-Le, P. Moreau, J. LeMaoult, Adv. Immunol. 127, 33–144 (2015)

    Article  PubMed  Google Scholar 

  52. W.L. Chang, N. Baumgarth, M.K. Eberhardt, C.Y. Lee, C.A. Baron, J.P. Gregg, P.A. Barry, J. Immunol. 178, 7794–7804 (2007)

    Article  CAS  PubMed  Google Scholar 

  53. W.L. Chang, P.A. Barry, Proc Natl Acad Sci USA 107, 22647–22652 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. J. McKenzie, F. Lopez-Giraldez, H.J. Delecluse, A. Walsh, A. El-Guindy, PLoS Pathog. 12, e1006008 (2016)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. N.F. Go, B.E. Castle, R. Barrett, R. Kastelein, W. Dang, T.R. Mosmann, K.W. Moore, M. Howard, J. Exp. Med. 172, 1625–1631 (1990)

    Article  CAS  PubMed  Google Scholar 

  56. I.A. MacNeil, T. Suda, K.W. Moore, T.R. Mosmann, A. Zlotnik, J. Immunol. 145, 4167–4173 (1990)

    CAS  PubMed  Google Scholar 

  57. P. Vieira, R. de Waal-Malefyt, M.N. Dang, K.E. Johnson, R. Kastelein, D.F. Fiorentino, J.E. deVries, M.G. Roncarolo, T.R. Mosmann, K.W. Moore, Proc Natl Acad Sci USA 88, 1172–1176 (1991)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. G.J. Lindquester, K.A. Greer, J.P. Stewart, J.T. Sample, Herpesviridae 5, 1 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  59. S. Jochum, A. Moosmann, S. Lang, W. Hammerschmidt, R. Zeidler, PLoS Pathog. 8, e1002704 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. S. Redpath, A. Angulo, N.R. Gascoigne, P. Ghazal, J. Immunol. 162, 6701–6707 (1999)

    CAS  PubMed  Google Scholar 

  61. J. McCaskill, P. Praihirunkit, P.M. Sharp, A.H. Buck, RNA Biol. 12, 579–585 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  62. V. Libri, A. Helwak, P. Miesen, D. Santhakumar, J.G. Borger, G. Kudla, F. Grey, D. Tollervey, A.H. Buck, Proc Natl Acad Sci USA 109, 279–284 (2012)

    Article  CAS  PubMed  Google Scholar 

  63. L. Marcinowski, M. Tanguy, A. Krmpotic, B. Radle, V.J. Lisnic, L. Tuddenham, B. Chane-Woon-Ming, Z. Ruzsics, F. Erhard, C. Benkartek, M. Babic, R. Zimmer, J. Trgovcich, U.H. Koszinowski, S. Jonjic, S. Pfeffer, L. Dolken, PLoS Pathog. 8, e1002510 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Y.E. Guo, K.J. Riley, A. Iwasaki, J.A. Steitz, Mol. Cell 54, 67–79 (2014)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. S. Avdic, B.P. McSharry, M. Steain, E. Poole, J. Sinclair, A. Abendroth, B. Slobedman, J. Virol. 90, 3819–3827 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. S.L. Lambert, O.M. Martinez, J Immunol 179, 8225–8234 (2007)

    Article  CAS  PubMed  Google Scholar 

  67. M.K. Eberhardt, A. Deshpande, J. Fike, R. Short, K.A. Schmidt, S.A. Blozis, M.R. Walter, P.A. Barry, J. Virol. 90, 9920–9930 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. F. Apparailly, C. Verwaerde, C. Jacquet, C. Auriault, J. Sany, C. Jorgensen, J. Immunol. 160, 5213–5220 (1998)

    CAS  PubMed  Google Scholar 

  69. K.N. Kim, S. Watanabe, Y. Ma, S. Thornton, E.H. Giannini, R. Hirsch, J. Immunol. 164, 1576–1581 (2000)

    Article  CAS  PubMed  Google Scholar 

  70. E.R. Lechman, D. Jaffurs, S.C. Ghivizzani, A. Gambotto, I. Kovesdi, Z. Mi, C.H. Evans, P.D. Robbins, J. Immunol. 163, 2202–2208 (1999)

    CAS  PubMed  Google Scholar 

  71. Y. Ma, S. Thornton, L.E. Duwel, G.P. Boivin, E.H. Giannini, J.M. Leiden, J.A. Bluestone, R. Hirsch, J. Immunol. 161, 1516–1524 (1998)

    CAS  PubMed  Google Scholar 

  72. J.D. Whalen, E.L. Lechman, C.A. Carlos, K. Weiss, I. Kovesdi, J.C. Glorioso, P.D. Robbins, C.H. Evans, J. Immunol. 162, 3625–3632 (1999)

    CAS  PubMed  Google Scholar 

  73. C. Hughes, A. Sette, M. Seed, F. D’Acquisto, A. Manzo, T.L. Vincent, N.H. Lim, A. Nissim, Arthritis Res. Ther. 16, R151 (2014)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. C.C. Nast, A. Moudgil, X.J. Zuo, M. Toyoda, S.C. Jordan, Transplantation 64, 1578–1582 (1997)

    Article  CAS  PubMed  Google Scholar 

  75. L. Qin, K.D. Chavin, Y. Ding, H. Tahara, J.P. Favaro, J.E. Woodward, T. Suzuki, P.D. Robbins, M.T. Lotze, J.S. Bromberg, J. Immunol. 156, 2316–2323 (1996)

    CAS  PubMed  Google Scholar 

  76. J.D. Carter, J.D. Ellett, M. Chen, K.M. Smith, L.B. Fialkow, M.J. McDuffie, K.S. Tung, J.L. Nadler, Z. Yang, Mol. Ther. 12, 360–368 (2005)

    Article  CAS  PubMed  Google Scholar 

  77. S.J. Kim, D.J. Doudet, A.R. Studenov, C. Nian, T.J. Ruth, S.S. Gambhir, C.H. McIntosh, Nat. Med. 12, 1423–1428 (2006)

    Article  CAS  PubMed  Google Scholar 

  78. Z. Yang, M. Chen, R. Wu, L.B. Fialkow, J.S. Bromberg, M. McDuffie, A. Naji, J.L. Nadler, J. Immunol. 168, 6479–6485 (2002)

    Article  CAS  PubMed  Google Scholar 

  79. C. de Lemos Rieper, P. Galle, B.K. Pedersen, M.B. Hansen, J. Gen. Virol. 92, 1508–1518 (2011)

    Article  PubMed  CAS  Google Scholar 

  80. M.K. Eberhardt, W.L. Chang, N.J. Logsdon, Y. Yue, M.R. Walter, P.A. Barry, PLoS ONE 7, e37931 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. M.K. Eberhardt, A. Deshpande, W.L. Chang, S.W. Barthold, M.R. Walter, P.A. Barry, J. Virol. 87, 11323–11331 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. E. Flano, B. Kayhan, D.L. Woodland, M.A. Blackman, J. Immunol. 175, 3225–3234 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. S. Beck, B.G. Barrell, Nature 331, 269–272 (1988)

    Article  CAS  PubMed  Google Scholar 

  84. H. Browne, G. Smith, S. Beck, T. Minson, Nature 347, 770–772 (1990)

    Article  CAS  PubMed  Google Scholar 

  85. M.L. Fahnestock, J.L. Johnson, R.M. Feldman, J.M. Neveu, W.S. Lane, P.J. Bjorkman, Immunity 3, 583–590 (1995)

    Article  CAS  PubMed  Google Scholar 

  86. T.L. Chapman, A.P. Heikeman, P.J. Bjorkman, Immunity 11, 603–613 (1999)

    Article  CAS  PubMed  Google Scholar 

  87. B. Park, H. Oh, S. Lee, Y. Song, J. Shin, Y.C. Sung, S.Y. Hwang, K. Ahn, J. Immunol. 168, 3464–3469 (2002)

    Article  CAS  PubMed  Google Scholar 

  88. Z. Yang, P.J. Bjorkman, Proc Natl Acad Sci USA 105, 10095–10100 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. H.G. Ljunggren, K. Karre, Immunol. Today 11, 237–244 (1990)

    Article  CAS  PubMed  Google Scholar 

  90. C.C. Leong, T.L. Chapman, P.J. Bjorkman, D. Formankova, E.S. Mocarski, J.H. Phillips, L.L. Lanier, J. Exp. Med. 187, 1681–1687 (1998)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. V. Prod’homme, C. Griffin, R.J. Aicheler, E.C. Wang, B.P. McSharry, C.R. Rickards, R.J. Stanton, L.K. Borysiewicz, M. Lopez-Botet, G.W. Wilkinson, P. Tomasec, J. Immunol. 178, 4473–4481 (2007)

    Article  PubMed  PubMed Central  Google Scholar 

  92. K.C. Chen, R.J. Stanton, J.J. Banat, M.R. Wills, J. Virol. 90, 3123–3137 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. M.R. Wills, O. Ashiru, M.B. Reeves, G. Okecha, J. Trowsdale, P. Tomasec, G.W. Wilkinson, J. Sinclair, J.G. Sissons, J. Immunol. 175, 7457–7465 (2005)

    Article  CAS  PubMed  Google Scholar 

  94. N.J. Chalupny, A. Rein-Weston, S. Dosch, D. Cosman, Biochem. Biophys. Res. Commun. 346, 175–181 (2006)

    Article  CAS  PubMed  Google Scholar 

  95. N.J. Bennett, O. Ashiru, F.J. Morgan, Y. Pang, G. Okecha, R.A. Eagle, J. Trowsdale, J.G. Sissons, M.R. Wills, J. Immunol. 185, 1093–1102 (2010)

    Article  CAS  PubMed  Google Scholar 

  96. E.J. Adams, A.M. Luoma, Annu. Rev. Immunol. 31, 529–561 (2013)

    Article  CAS  PubMed  Google Scholar 

  97. W.D. Rawlinson, H.E. Farrell, B.G. Barrell, J. Virol. 70, 8833–8849 (1996)

    CAS  PubMed  PubMed Central  Google Scholar 

  98. K. Natarajan, A. Hicks, J. Mans, H. Robinson, R. Guan, R.A. Mariuzza, D.H. Margulies, J. Mol. Biol. 358, 157–171 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. H.E. Farrell, H. Vally, D.M. Lynch, P. Fleming, G.R. Shellam, A.A. Scalzo, N.J. Davis-Poynter, Nature 386, 510–514 (1997)

    Article  CAS  PubMed  Google Scholar 

  100. E. Cretney, M.A. Degli-Esposti, E.H. Densley, H.E. Farrell, N.J. Davis-Poynter, M.J. Smyth, J. Exp. Med. 190, 435–444 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. P.S. Beisser, J.S. Kloover, G.E. Grauls, M.J. Blok, C.A. Bruggeman, C. Vink, J. Virol. 74, 1045–1050 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. H. Geyer, J. Ettinger, L. Moller, E. Schmolz, A. Nitsche, W. Brune, S. Heaggans, G.R. Sandford, G.S. Hayward, S. Voigt, J. Genl. Virol. 96, 1873–1879 (2015)

    Article  CAS  Google Scholar 

  103. C. Vink, E. Beuken, C.A. Bruggeman, J. Virol. 74, 7656–7665 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. M.R. Schleiss, A. McGregor, K.Y. Choi, S.V. Date, X. Cui, M.A. McVoy, Virol. J. 5, 139 (2008)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. M.M. Crumpler, K.Y. Choi, M.A. McVoy, M.R. Schleiss, Vaccine 27, 4209–4218 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. J. Loh, G. Zhao, C.A. Nelson, P. Coder, L. Droit, S.A. Handley, L.S. Johnson, P. Vachharajani, H. Guzman, R.B. Tesh, D. Wang, D.H. Fremont, H.W. Virgin, J. Virol. 85, 2642–2656 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. H. Zhang, S. Todd, M. Tachedjian, J.A. Barr, M. Luo, M. Yu, G.A. Marsh, G. Crameri, L.F. Wang, J. Virol. 86, 8014–8030 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. J.W. Wynne, A.P. Woon, N.L. Dudek, N.P. Croft, J.H. Ng, M.L. Baker, L.F. Wang, A.W. Purcell, J. Immunol. 196, 4468–4476 (2016)

    Article  CAS  PubMed  Google Scholar 

  109. A.J. Davison, C. Cunningham, W. Sauerbier, R.G. McKinnell, J. Gen. Virol. 87, 3509–3514 (2006)

    Article  CAS  PubMed  Google Scholar 

  110. E.A. Gorshkova, E.S. Shilov, Biochemistry (Mosc) 81, 1350–1357 (2016)

    Article  CAS  Google Scholar 

  111. G. Morissette, L. Flamand, J. Virol. 84, 12100–12109 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. A. Aswad, A. Katzourakis, PLoS Genet. 10, e1004332 (2014)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  113. D.M. Knipe, P.M. Lieberman, J.U. Jung, A.A. McBride, K.V. Morris, M. Ott, D. Margolis, A. Nieto, M. Nevels, R.J. Parks, T.M. Kristie, Virology 435, 141–156 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. A. Prasad, J. Remick, S.L. Zeichner, J. Virol. 87, 10641–10650 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. B.D. Larsen, C.S. Sørensen, FEBS J. 284, 1160–1170 (2017). doi:10.1111/febs.13970

    Article  CAS  PubMed  Google Scholar 

  116. K. Crasta, N.J. Ganem, R. Dagher, A.B. Lantermann, E.V. Ivanova, Y. Pan, L. Nezi, A. Protopopov, D. Chowdhury, D. Pellman, Nature 482, 53–58 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. B. Berkhout, M. Jebbink, J. Zsiros, J. Virol. 73, 2365–2375 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  118. M. Bukrinsky, Mol. Med. 10, 1–5 (2004)

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Hamid F. Bin, J. Kim, C.G. Shin, Can. J. Microbiol. 62, 1–15 (2016)

    Article  CAS  Google Scholar 

  120. S. Bedoui, M. Greyer, Front. Microbiol. 5, 533 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  121. G. Schonrich, M.J. Raftery, Front. Microbiol. 6, 417 (2015)

    PubMed  PubMed Central  Google Scholar 

  122. P. Brunovskis, H.J. Kung, Virus Genes 11, 259–270 (1995)

    Article  CAS  PubMed  Google Scholar 

  123. D. Jones, R. Isfort, R. Witter, R. Kost, H.J. Kung, Proc Natl Acad Sci USA 90, 3855–3859 (1993)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. R. Isfort, D. Jones, R. Kost, R. Witter, H.J. Kung, Proc Natl Acad Sci USA 89, 991–995 (1992)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. A. Aswad, A. Katzourakis, Nat. Commun. 6, 8299 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. S. Kumar, G. Stecher, K. Tamura, Mol. Biol. Evol. 33, 1870–1874 (2016)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgement

This work was supported by Deutsche Forschungsgemeinschaft (Support code SCHO 592/9-1).

Author contributions

GS and MJR contributed to the conception, writing, and editing of this review; MOA contributed to the editing of this review.

Author information

Authors and Affiliations

  1. Institute of Medical Virology, Helmut-Ruska-Haus, Charité−Universitätsmedizin Berlin, Charitéplatz 1, 10117, Berlin, Germany

    Günther Schönrich, Mohammed O. Abdelaziz & Martin J. Raftery

Authors
  1. Günther Schönrich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohammed O. Abdelaziz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin J. Raftery
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Günther Schönrich.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Edited by Detlev H. Kruger.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schönrich, G., Abdelaziz, M.O. & Raftery, M.J. Herpesviral capture of immunomodulatory host genes. Virus Genes 53, 762–773 (2017). https://doi.org/10.1007/s11262-017-1460-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-017-1460-0

Keywords

Search

Navigation