Table of Contents Author Guidelines Submit a Manuscript
Advances in Virology
Volume 2012, Article ID 359869, 10 pages
http://dx.doi.org/10.1155/2012/359869
Review Article

Human Herpesviridae Methods of Natural Killer Cell Evasion

1School of Medicine, University of Alabama at Birmingham, 1600 6th Avenue South, CHB 118C, Birmingham, AL 35233-1701, USA
2Division of Neurosurgery, Department of Surgery, University of Alabama at Birmingham, 1530 3rd Avenue South, FOT 1060, Birmingham, AL 35294-3410, USA
3Department of Cell, Developmental, and Integrative Biology, University of Alabama at Birmingham, 1530 3rd Avenue South, Birmingham, AL 35294-3410, USA
4Division of Infectious Disease, Department of Pediatrics, University of Alabama at Birmingham, 600 7th Avenue South, CHB 118, Birmingham, AL 35233-1701, USA

Received 4 March 2012; Accepted 24 April 2012

Academic Editor: John Frater

Copyright © 2012 Carl I. Odom et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T. Chan, N. G. Barra, A. J. Lee, and A. A. Ashkar, “Innate and adaptive immunity against herpes simplex virus type 2 in the genital mucosa,” Journal of Reproductive Immunology, vol. 88, no. 2, pp. 210–218, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. S. E. Jackson, G. M. Mason, and M. R. Wills, “Human cytomegalovirus immunity and immune evasion,” Virus Research, vol. 157, no. 2, pp. 151–160, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. L. Coscoy, “Immune evasion by Kaposi's sarcoma-associated herpesvirus,” Nature Reviews Immunology, vol. 7, no. 5, pp. 391–401, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. E. J. Wiertz, R. Devlin, H. L. Collins, and M. E. Ressing, “Herpesvirus interference with major histocompatibility complex class II-restricted T-cell activation,” Journal of Virology, vol. 81, no. 9, pp. 4389–4396, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Jonjić, M. Babić, B. Polić, and A. Krmpotić, “Immune evasion of natural killer cells by viruses,” Current Opinion in Immunology, vol. 20, no. 1, pp. 30–38, 2008. View at Publisher · View at Google Scholar
  6. L. L. Lanier, “Evolutionary struggles between NK cells and viruses,” Nature Reviews Immunology, vol. 8, no. 4, pp. 259–268, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Groth, S. Klöss, E. Pogge Von Strandmann, U. Koehl, and J. Koch, “Mechanisms of tumor and viral immune escape from natural killer cell-mediated surveillance,” Journal of Innate Immunity, vol. 3, no. 4, pp. 344–354, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. V. J. Lisnić, A. Krmpotić, and S. Jonjić, “Modulation of natural killer cell activity by viruses,” Current Opinion in Microbiology, vol. 13, no. 4, pp. 530–539, 2010. View at Publisher · View at Google Scholar
  9. C. A. Biron, K. S. Byron, and J. L. Sullivan, “Severe herpesvirus infections in an adolescent without natural killer cells,” The New England Journal of Medicine, vol. 320, no. 26, pp. 1731–1735, 1989. View at Google Scholar · View at Scopus
  10. P. A. Fitzgerald, M. Mendelsohn, and C. Lopez, “Human natural killer cells limit replication of herpes simplex virus type 1 in vitro,” Journal of Immunology, vol. 134, no. 4, pp. 2666–2672, 1985. View at Google Scholar · View at Scopus
  11. C. V. Paya, R. A. Schoon, and P. J. Leibson, “Alternative mechanisms of natural killer cell activation during herpes simplex virus infection,” Journal of Immunology, vol. 144, no. 11, pp. 4370–4375, 1990. View at Google Scholar · View at Scopus
  12. P. Fitzgerald-Bocarsly, D. M. Howell, L. Pettera, S. Tehrani, and C. Lopez, “Immediate-early gene expression is sufficient for induction of natural killer cell-mediated lysis of herpes simplex virus type 1-infected fibroblasts,” Journal of Virology, vol. 65, no. 6, pp. 3151–3160, 1991. View at Google Scholar · View at Scopus
  13. C. Lopez, D. Kirkpatrick, and P. A. Fitzgerald, “Studies of the cell lineage of the effector cells that spontaneously lyse HSV-1 infected fibroblasts (NK(HSV-1)),” Journal of Immunology, vol. 129, no. 2, pp. 824–828, 1982. View at Google Scholar · View at Scopus
  14. F. Marras, F. Bozzano, and A. De Maria, “Involvement of activating NK cell receptors and their modulation in pathogen immunity,” Journal of Biomedicine and Biotechnology, vol. 2011, Article ID 152430, 11 pages, 2011. View at Publisher · View at Google Scholar
  15. S. H. Lee and C. A. Biron, “Here today—not gone tomorrow: roles for activating receptors in sustaining NK cells during viral infections,” European Journal of Immunology, vol. 40, no. 4, pp. 923–932, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. S. S. Farag and M. A. Caligiuri, “Human natural killer cell development and biology,” Blood Reviews, vol. 20, no. 3, pp. 123–137, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. L. L. Lanier, “NK cell recognition,” Annual Review of Immunology, vol. 23, pp. 225–274, 2005. View at Publisher · View at Google Scholar
  18. Y. T. Bryceson, S. C. C. Chiang, S. Darmanin et al., “Molecular mechanisms of natural killer cell activation,” Journal of Innate Immunity, vol. 3, no. 3, pp. 216–226, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. M. G. Joyce and P. D. Sun, “The structural basis of ligand recognition by natural killer cell receptors,” Journal of Biomedicine and Biotechnology, vol. 2011, Article ID 203628, 15 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. B. Zafirova, F. M. Wensveen, M. Gulin, and B. Polić, “Regulation of immune cell function and differentiation by the NKG2D receptor,” Cellular and Molecular Life Sciences, vol. 68, no. 21, pp. 3519–3529, 2011. View at Publisher · View at Google Scholar
  21. A. K. Purdy and K. S. Campbell, “Natural killer cells and cancer: regulation by the killer cell ig-like receptors (KIR),” Cancer Biology and Therapy, vol. 8, no. 23, pp. 2211–2220, 2009. View at Google Scholar · View at Scopus
  22. D. H. Raulet, “Roles of the NKG2D immunoreceptor and its ligands,” Nature Reviews Immunology, vol. 3, no. 10, pp. 781–790, 2003. View at Google Scholar · View at Scopus
  23. R. A. Eagle and J. Trowsdale, “Promiscuity and the single receptor: NKG2D,” Nature Reviews Immunology, vol. 7, no. 9, pp. 737–744, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Li, S. T. Willie, S. Bauer, D. L. Morris, T. Spies, and R. K. Strong, “Crystal structure of the MHC class I homolog MIC-A, a γδ T cell ligand,” Immunity, vol. 10, no. 5, pp. 577–584, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Li, D. L. Morris, B. E. Willcox, A. Steinle, T. Spies, and R. K. Strong, “Complex structure of the activating immunoreceptor NKG2D and its MHC class I-like ligand MICA,” Nature Immunology, vol. 2, no. 5, pp. 443–451, 2001. View at Google Scholar · View at Scopus
  26. M. A. Holmes, P. Li, E. W. Petersdorf, and R. K. Strong, “Structural studies of allelic diversity of the MHC class I homolog MIC-B, a stress-inducible ligand for the activating immunoreceptor NKG2D,” Journal of Immunology, vol. 169, no. 3, pp. 1395–1400, 2002. View at Google Scholar · View at Scopus
  27. L. Moretta, C. Bottino, D. Pende, R. Castriconi, M. C. Mingari, and A. Moretta, “Surface NK receptors and their ligands on tumor cells,” Seminars in Immunology, vol. 18, no. 3, pp. 151–158, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. N. Stern-Ginossar and O. Mandelboim, “An integrated view of the regulation of NKG2D ligands,” Immunology, vol. 128, no. 1, pp. 1–6, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Gasser, S. Orsulic, E. J. Brown, and D. H. Raulet, “The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor,” Nature, vol. 436, no. 7054, pp. 1186–1190, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Yamamoto, Y. Fujiyama, A. Andoh, T. Bamba, and H. Okabe, “Oxidative stress increases MICA and MICB gene expression in the human colon carcinoma cell line (CaCo-2),” Biochimica et Biophysica Acta, vol. 1526, no. 1, pp. 10–12, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Frigoul and M.-P. Lefranc, “MICA: standardized IMGT allele nomenclature, polymorphisms and diseases,” in Recent Research Developments in Human Genetics, S. G. Pandalai, Ed., vol. 3, pp. 95–145, 2005. View at Google Scholar
  32. E. W. Petersdorf, K. B. Shuler, G. M. Longton, T. Spies, and J. A. Hansen, “Population study of allelic diversity in the human MHC class I-related MIC-A gene,” Immunogenetics, vol. 49, no. 7-8, pp. 605–612, 1999. View at Publisher · View at Google Scholar · View at Scopus
  33. F. Zhu, H. Zhao, Y. He et al., “Distribution of MICA diversity in the Chinese Han population by polymerase chain reaction sequence-based typing for exons 2-6,” Tissue Antigens, vol. 73, no. 4, pp. 358–363, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. M. L. C. Marin, C. R. Savioli, J. H. Yamamoto, J. Kalil, and A. C. Goldberg, “MICA polymorphism in a sample of the São Paulo population, Brazil,” European Journal of Immunogenetics, vol. 31, no. 2, pp. 63–71, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. X. Gao, R. M. Single, P. Karacki, D. Marti, S. J. O'Brien, and M. Carrington, “Diversity of MICA and linkage disequilibrium with HLA-B in two North American populations,” Human Immunology, vol. 67, no. 3, pp. 152–158, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. D. Lucas, J. A. Campillo, R. López-Hernández et al., “Allelic diversity of MICA gene and MICA/HLA-B haplotypic variation in a population of the Murcia region in southeastern Spain,” Human Immunology, vol. 69, no. 10, pp. 655–660, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. W. Tian, D. A. Boggs, G. Uko et al., “MICA, HLA-B haplotypic variation in five population groups of sub-Saharan African ancestry,” Genes and Immunity, vol. 4, no. 7, pp. 500–505, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Cambra, I. Muñoz-Saá, C. Crespí et al., “MICA-HLA-B haplotype diversity and linkage disequilibrium in a population of Jewish descent from Majorca (the Balearic Islands),” Human Immunology, vol. 70, no. 7, pp. 513–517, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. V. Ďurmanová, J. Tirpakova, M. Stuchlikova et al., “Characterization of MICA gene polymorphism of HLA complex in the Slovak population,” Annals of Human Biology, vol. 38, no. 5, pp. 570–576, 2011. View at Publisher · View at Google Scholar
  40. D. Cosman, J. Müllberg, C. L. Sutherland et al., “ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor,” Immunity, vol. 14, no. 2, pp. 123–133, 2001. View at Google Scholar · View at Scopus
  41. C. Bottino, R. Biassoni, R. Millo, L. Moretta, and A. Moretta, “The human natural cytotoxicity receptors (NCR) that induce HLA class I-independent NK cell triggering,” Human Immunology, vol. 61, no. 1, pp. 1–6, 2000. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Vitale et al., “Identification of NKp80, a novel triggering molecule expressed by human NK cells,” European Journal of Immunology, vol. 31, no. 1, pp. 233–242, 2001. View at Google Scholar
  43. C. Fauriat, S. Just-Landi, F. Mallet et al., “Deficient expression of NCR in NK cells from acute myeloid leukemia: Evolution during leukemia treatment and impact of leukemia cells in NCR dull phenotype induction,” Blood, vol. 109, no. 1, pp. 323–330, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. R. T. Costello, B. Knoblauch, C. Sanchez, D. Mercier, T. Le Treut, and G. Sébahoun, “Expression of natural killer cell activating receptors in patients with chronic lymphocytic leukaemia,” Immunology, vol. 135, no. 2, pp. 151–157, 2012. View at Publisher · View at Google Scholar
  45. A. Glasner, H. Ghadially, C. Gur et al., “Recognition and prevention of tumor metastasis by the NK receptor NKp46/NCR1,” Journal of Immunology, vol. 188, no. 6, pp. 2509–2515, 2012. View at Publisher · View at Google Scholar
  46. S. Morgado, B. Sanchez-Correa, J. G. Casado et al., “NK cell recognition and killing of melanoma cells is controlled by multiple activating receptor-ligand interactions,” Journal of Innate Immunity, vol. 3, no. 4, pp. 365–373, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Li, Q. Wang, and R. A. Mariuzza, “Structure of the human activating natural cytotoxicity receptor NKp30 bound to its tumor cell ligand B7-H6,” Journal of Experimental Medicine, vol. 208, no. 4, pp. 703–714, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. T. Kaifu, B. Escalière, L. N. Gastinel, E. Vivier, and M. Baratin, “B7-H6/NKp30 interaction: a mechanism of alerting NK cells against tumors,” Cellular and Molecular Life Sciences, vol. 68, no. 21, pp. 3531–3539, 2011. View at Publisher · View at Google Scholar
  49. E. Pogge von Strandmann, V. R. Simhadri, B. von Tresckow et al., “Human leukocyte antigen-B-associated transcript 3 is released from tumor vells and engages the NKp30 receptor on natural killer cells,” Immunity, vol. 27, no. 6, pp. 965–974, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. M. L. Hecht, B. Rosental, T. Horlacher et al., “Natural cytotoxicity receptors NKp30, NKp44 and NKp46 bind to different heparan sulfate/heparin sequences,” Journal of Proteome Research, vol. 8, no. 2, pp. 712–720, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Jarahian, C. Watzl, P. Fournier et al., “Activation of natural killer cells by Newcastle disease virus hemagglutinin-neuraminidase,” Journal of Virology, vol. 83, no. 16, pp. 8108–8121, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Carlsten, N. K. Björkström, H. Norell et al., “DNAX accessory molecule-1 mediated recognition of freshly isolated ovarian carcinoma by resting natural killer cells,” Cancer Research, vol. 67, no. 3, pp. 1317–1325, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Castriconi, A. Dondero, M. V. Corrias et al., “Natural killer cell-mediated killing of freshly isolated neuroblastoma cells: Critical role of DNAX accessory molecule-1-poliovirus receptor interaction,” Cancer Research, vol. 64, no. 24, pp. 9180–9184, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. C. J. Chan, D. M. Andrews, N. M. McLaughlin et al., “DNAM-1/CD155 interactions promote cytokine and NK cell-mediated suppression of poorly immunogenic melanoma metastases,” Journal of Immunology, vol. 184, no. 2, pp. 902–911, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Lakshmikanth, S. Burke, T. H. Ali et al., “NCRs and DNAM-1 mediate NK cell recognition and lysis of human and mouse melanoma cell lines in vitro and in vivo,” Journal of Clinical Investigation, vol. 119, no. 5, pp. 1251–1263, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. Z. Zhang, T. Su, L. He et al., “Identification and functional analysis of ligands for natural killer cell activating receptors in colon carcinoma,” The Tohoku journal of experimental medicine, vol. 226, no. 1, pp. 59–68, 2012. View at Google Scholar
  57. Z. Huang, B. Fu, S. G. Zheng et al., “Involvement of CD226+ NK cells in immunopathogenesis of systemic lupus erythematosus,” Journal of Immunology, vol. 186, no. 6, pp. 3421–3431, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. A. K. Maiti, X. Kim-Howard, P. Viswanathan et al., “Non-synonymous variant (Gly307Ser) in CD226 is associated with susceptibility to multiple autoimmune diseases,” Rheumatology, vol. 49, no. 7, Article ID kep470, pp. 1239–1244, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. J. M. L. Tjon, Y. M. C. Kooy-Winkelaar, G. J. Tack et al., “DNAM-1 mediates epithelial cell-specific cytotoxicity of aberrant intraepithelial lymphocyte lines from refractory celiac disease type II patients,” Journal of Immunology, vol. 186, no. 11, pp. 6304–6312, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. N. Wagtmann, S. Rajagopalan, C. C. Winter, M. Peruzzi, and E. O. Long, “Killer cell inhibitory receptors specific for HLA-C and HLA-B identified by direct binding and by functional transfer,” Immunity, vol. 3, no. 6, pp. 801–809, 1995. View at Publisher · View at Google Scholar · View at Scopus
  61. V. M. Braud, D. S. J. Allan, C. A. O'Callaghan et al., “HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C,” Nature, vol. 391, no. 6669, pp. 795–799, 1998. View at Publisher · View at Google Scholar · View at Scopus
  62. F. Borrego, M. Ulbrecht, E. H. Weiss, J. E. Coligan, and A. G. Brooks, “Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis,” Journal of Experimental Medicine, vol. 187, no. 5, pp. 813–818, 1998. View at Publisher · View at Google Scholar · View at Scopus
  63. B. Huard and K. Früh, “A role for MHC class I down-regulation in NK cell lysis of herpes virus-infected cells,” European Journal of Immunology, vol. 30, no. 2, pp. 509–515, 2000. View at Publisher · View at Google Scholar
  64. K. Karre, H. G. Ljunggren, G. Piontek, and R. Kiessling, “Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy,” Nature, vol. 319, no. 6055, pp. 675–678, 1986. View at Google Scholar · View at Scopus
  65. J. Yu, G. Heller, J. Chewning, S. Kim, W. M. Yokoyama, and K. C. Hsu, “Hierarchy of the human natural killer cell response is determined by class and quantity of inhibitory receptors for self-HLA-B and HLA-C ligands,” Journal of Immunology, vol. 179, no. 9, pp. 5977–5989, 2007. View at Google Scholar · View at Scopus
  66. J. Van Bergen, A. Thompson, C. Retière, J. Trowsdale, and F. Koning, “Cutting edge: killer Ig-like receptors mediate “missing self” recognition in vivo,” Journal of Immunology, vol. 182, no. 5, pp. 2569–2572, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Lin, H. Xu, and W. Yan, “Modulation of HLA expression in human cytomegalovirus immune evasion,” Cellular & Molecular Immunology, vol. 4, no. 2, pp. 91–98, 2007. View at Google Scholar · View at Scopus
  68. N. J. Chalupny, A. Rein-Weston, S. Dosch, and D. Cosman, “Down-regulation of the NKG2D ligand MICA by the human cytomegalovirus glycoprotein UL142,” Biochemical and Biophysical Research Communications, vol. 346, no. 1, pp. 175–181, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. O. Ashiru, N. J. Bennett, L. H. Boyle, M. Thomas, J. Trowsdale, and M. R. Wills, “NKG2D ligand MICA is retained in the cis-Golgi apparatus by human cytomegalovirus protein UL142,” Journal of Virology, vol. 83, no. 23, pp. 12345–12354, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Thomas, M. Wills, and P. J. Lehner, “Natural killer cell evasion by an E3 ubiquitin ligase from Kaposi's sarcoma-associated herpesvirus,” Biochemical Society Transactions, vol. 36, no. 3, pp. 459–463, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. M. Thomas, J. M. Boname, S. Field et al., “Down-regulation of NKG2D and NKp80 ligands by Kaposi's sarcoma-associated herpesvirus K5 protects against NK cell cytotoxicity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 5, pp. 1656–1661, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. D. Schepis, M. D'Amato, M. Studahl, T. Bergström, K. Kärre, and L. Berg, “Herpes simplex virus infection downmodulates NKG2D ligand expression,” Scandinavian Journal of Immunology, vol. 69, no. 5, pp. 429–436, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. S. E. Chisholm, K. Howard, M. V. Gómez, and H. T. Reyburn, “Expression of ICP0 is sufficient to trigger natural killer cell recognition of herpes simplex virus-infected cells by natural cytotoxicity receptors,” Journal of Infectious Diseases, vol. 195, no. 8, pp. 1160–1168, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. C. L. Schneider and A. W. Hudson, “The human herpesvirus-7 (HHV-7) U21 immunoevasin subverts NK-mediated cytoxicity through modulation of MICA and MICB,” PLoS Pathogens, vol. 7, no. 11, Article ID e1002362, 2011. View at Publisher · View at Google Scholar
  75. S. A. Welte, C. Sinzger, S. Z. Lutz et al., “Selective intracellular retention of virally induced NKG2D ligands by the human cytomegalovirus UL16 glycoprotein,” European Journal of Immunology, vol. 33, no. 1, pp. 194–203, 2003. View at Publisher · View at Google Scholar · View at Scopus
  76. J. Wu, N. J. Chalupny, T. J. Manley, S. R. Riddell, D. Cosman, and T. Spies, “Intracellular retention of the MHC class I-related chain B ligand of NKG2D by the human cytomegalovirus UL16 glycoprotein,” Journal of Immunology, vol. 170, no. 8, pp. 4196–4200, 2003. View at Google Scholar · View at Scopus
  77. C. Dunn, N. J. Chalupny, C. L. Sutherland et al., “Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity,” Journal of Experimental Medicine, vol. 197, no. 11, pp. 1427–1439, 2003. View at Publisher · View at Google Scholar · View at Scopus
  78. N. Stern-Ginossar, N. Elefant, A. Zimmermann et al., “Host immune system gene targeting by a viral miRNA,” Science, vol. 317, no. 5836, pp. 376–381, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. D. Nachmani, N. Stern-Ginossar, R. Sarid, and O. Mandelboim, “Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells,” Cell Host and Microbe, vol. 5, no. 4, pp. 376–385, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. H. T. Reyburn, O. Mandelboim, M. Valés-Gómez, D. M. Davis, L. Pazmany, and J. L. Strominger, “The class I MHC homologue of human cytomegalovirus inhibits attack by natural killer cells,” Nature, vol. 386, no. 6624, pp. 514–517, 1997. View at Publisher · View at Google Scholar · View at Scopus
  81. Z. Yang and P. J. Bjorkman, “Structure of UL18, a peptide-binding viral MHC mimic, bound to a host inhibitory receptor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 29, pp. 10095–10100, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. P. Tomasec, “Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40,” Science, vol. 287, no. 5455, pp. 1031–1033, 2000. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Ulbrecht, S. Martinozzi, M. Grzeschik et al., “Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis,” Journal of Immunology, vol. 164, no. 10, pp. 5019–5022, 2000. View at Google Scholar · View at Scopus
  84. E. C. Y. Wang, B. McSharry, C. Retiere et al., “UL40-mediated NK evasion during productive infection with human cytomegalovirus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 11, pp. 7570–7575, 2002. View at Publisher · View at Google Scholar · View at Scopus
  85. S. Ishido, C. Wang, B. S. Lee, G. B. Cohen, and J. U. Jung, “Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins,” Journal of Virology, vol. 74, no. 11, pp. 5300–5309, 2000. View at Publisher · View at Google Scholar · View at Scopus
  86. M. Haque, K. Ueda, K. Nakano et al., “Major histocompatibility complex class I molecules are down-regulated at the cell surface by the K5 protein encoded by Kaposi's sarcoma-associated herpesvirus/human herpesvirus-8,” Journal of General Virology, vol. 82, part 5, pp. 1175–1180, 2001. View at Google Scholar · View at Scopus
  87. E. Bartee, M. Mansouri, B. T. H. Nerenberg, K. Gouveia, and K. Früh, “Downregulation of major histocompatibility complex class I by human ubiquitin ligases related to viral Immune evasion proteins,” Journal of Virology, vol. 78, no. 3, pp. 1109–1120, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. A. B. Hill, B. C. Barnett, A. J. McMichael, and D. J. McGeoch, “HLA class I molecules are not transported to the cell surface in cells infected with herpes simplex virus types 1 and 2,” Journal of Immunology, vol. 152, no. 6, pp. 2736–2741, 1994. View at Google Scholar · View at Scopus
  89. A. Hill, P. Juovic, I. York et al., “Herpes simplex virus turns off the TAP to evade host immunity,” Nature, vol. 375, no. 6530, pp. 411–415, 1995. View at Google Scholar · View at Scopus
  90. I. A. York, C. Roop, D. W. Andrews, S. R. Riddell, F. L. Graham, and D. C. Johnson, “A cytosolic herpes simplex virus protein inhibits antigen presentation to CD8+ T lymphocytes,” Cell, vol. 77, no. 4, pp. 525–535, 1994. View at Publisher · View at Google Scholar · View at Scopus
  91. S.-H. Sin and D. P. Dittmer, “Cytokine homologs of human gammaherpesviruses,” Journal of Interferon and Cytokine Research, vol. 32, no. 2, pp. 53–59, 2012. View at Publisher · View at Google Scholar
  92. N. P. Croft, C. Shannon-Lowe, A. I. Bell et al., “Stage-specific inhibition of MHC class I presentation by the epstein-barr virus BNLF2a protein during virus lytic cycle,” PLoS Pathogens, vol. 5, no. 6, Article ID e1000490, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. D. Horst, V. Favaloro, F. Vilardi et al., “EBV protein BNLF2a exploits host tail-anchored protein integration machinery to inhibit TAP,” Journal of Immunology, vol. 186, no. 6, pp. 3594–3605, 2011. View at Publisher · View at Google Scholar · View at Scopus
  94. J. Zuo, L. L. Quinn, J. Tamblyn et al., “The Epstein-Barr virus-encoded BILF1 protein modulates immune recognition of endogenously processed antigen by targeting major histocompatibility complex class I molecules trafficking on both the exocytic and endocytic pathways,” Journal of Virology, vol. 85, no. 4, pp. 1604–1614, 2011. View at Publisher · View at Google Scholar · View at Scopus
  95. N. L. Glosson and A. W. Hudson, “Human herpesvirus-6A and -6B encode viral immunoevasins that downregulate class I MHC molecules,” Virology, vol. 365, no. 1, pp. 125–135, 2007. View at Publisher · View at Google Scholar · View at Scopus
  96. N. L. Glosson, P. Gonyo, N. A. May et al., “Insight into the mechanism of human herpesvirus 7 U21-mediated diversion of class I MHC molecules to lysosomes,” Journal of Biological Chemistry, vol. 285, no. 47, pp. 37016–37029, 2010. View at Publisher · View at Google Scholar · View at Scopus
  97. N. A. May, N. L. Glosson, and A. W. Hudson, “Human herpesvirus 7 U21 downregulates classical and nonclassical class I major histocompatibility complex molecules from the cell surface,” Journal of Virology, vol. 84, no. 8, pp. 3738–3751, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. A. W. Hudson, D. Blom, P. M. Howley, and H. L. Ploegh, “The ER-lumenal domain of the HHV-7 immunoevasin U21 directs class I MHC molecules to lysosomes,” Traffic, vol. 4, no. 12, pp. 824–837, 2003. View at Publisher · View at Google Scholar · View at Scopus
  99. A. Abendroth, I. Lin, B. Slobedman, H. Ploegh, and A. M. Arvin, “Varicella-zoster virus retains major histocompatibility complex class I proteins in the golgi compartment of infected cells,” Journal of Virology, vol. 75, no. 10, pp. 4878–4888, 2001. View at Publisher · View at Google Scholar · View at Scopus
  100. A. J. Eisfeld, M. B. Yee, A. Erazo, A. Abendroth, and P. R. Kinchington, “Downregulation of class I major histocompatibility complex surface expression by varicella-zoster virus involves open reading frame 66 protein kinase-dependent and -independent mechanisms,” Journal of Virology, vol. 81, no. 17, pp. 9034–9049, 2007. View at Publisher · View at Google Scholar · View at Scopus
  101. C. C. Leong, T. L. Chapman, P. J. Bjorkman et al., “Modulation of natural killer cell cytotoxicity in human cytomegalovirus infection: The role of endogenous class I major histocompatibility complex and a viral class I homolog,” Journal of Experimental Medicine, vol. 187, no. 10, pp. 1681–1687, 1998. View at Publisher · View at Google Scholar · View at Scopus
  102. D. Cosman, N. Fanger, L. Borges et al., “A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules,” Immunity, vol. 7, no. 2, pp. 273–282, 1997. View at Publisher · View at Google Scholar · View at Scopus
  103. M. R. Wills, O. Ashiru, M. B. Reeves et al., “Human cytomegalovirus encodes an MHC Class I-like molecule (UL142) that functions to inhibit NK cell lysis,” Journal of Immunology, vol. 175, no. 11, pp. 7457–7465, 2005. View at Google Scholar · View at Scopus
  104. M. Llano, M. Gumá, M. Ortega, A. Angulo, and M. López-Botet, “Differential effects of US2, US6, and US11 human cytomegalovirus proteins of HLA class Ia and HLA-E expression: Impact on target susceptibility to NK cell subsets,” European Journal of Immunology, vol. 33, no. 10, pp. 2744–2754, 2003. View at Publisher · View at Google Scholar · View at Scopus
  105. M. Wittenbrink, J. Spreu, and A. Steinle, “Differential NKG2D binding to highly related human NKG2D ligands ULBP2 and RAET1G is determined by a single amino acid in the α2 domain,” European Journal of Immunology, vol. 39, no. 6, pp. 1642–1651, 2009. View at Publisher · View at Google Scholar · View at Scopus
  106. S. Müller, G. Zocher, A. Steinle, and T. Stehle, “Structure of the HCMV UL16-MICB complex elucidates select binding of a viral immunoevasin to diverse NKG2D ligands,” PLoS Pathogens, vol. 6, no. 1, Article ID e1000723, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. M. Colonna, S. Jonjic, and C. Watzl, “Natural killer cells: fighting viruses andmuch more,” Nature Immunology, vol. 12, no. 2, pp. 107–110, 2011. View at Publisher · View at Google Scholar · View at Scopus
  108. E. S. Mocarski, “Immune escape and exploitation strategies of cytomegaloviruses: impact on and imitation of the major histocompatibility system,” Cellular Microbiology, vol. 6, no. 8, pp. 707–717, 2004. View at Publisher · View at Google Scholar · View at Scopus
  109. S. Ishido, J. K. Choi, B. S. Lee et al., “Inhibition of natural killer cell-mediated cytotoxicity by Kaposi's sarcoma-associated herpesvirus K5 protein,” Immunity, vol. 13, no. 3, pp. 365–374, 2000. View at Google Scholar · View at Scopus
  110. S. Dupuy, M. Lambert, D. Zucman et al., “Human herpesvirus 8 (HHV8) sequentially shapes the NK cell repertoire during the course of asymptomatic infection and Kaposi sarcoma,” PLoS Pathogens, vol. 8, no. 1, Article ID e1002486, 2012. View at Publisher · View at Google Scholar
  111. R. E. Means, J. K. Choi, H. Nakamura, Y. H. Chung, S. Ishido, and J. U. Jung, “Immune evasion strategies of Kaposi's sarcoma-associated herpesvirus,” Current Topics in Microbiology and Immunology, vol. 269, pp. 187–201, 2002. View at Google Scholar · View at Scopus
  112. R. Tomazin, N. E. G. Van Schoot, K. Goldsmith et al., “Herpes simplex virus type 2 ICP47 inhibits human TAP but not mouse tap,” Journal of Virology, vol. 72, no. 3, pp. 2560–2563, 1998. View at Google Scholar · View at Scopus
  113. M. Lafon, C. Prehaud, F. Megret et al., “Modulation of HLA-G expression in human neural cells after neurotropic viral infections,” Journal of Virology, vol. 79, no. 24, pp. 15226–15237, 2005. View at Publisher · View at Google Scholar · View at Scopus
  114. D. S. Kaufman, R. A. Schoon, and P. J. Leibson, “Role for major histocompatibility complex class I in regulating natural killer cell-mediated killing of virus-infected cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 17, pp. 8337–8341, 1992. View at Google Scholar · View at Scopus
  115. I. Y. Pappworth, E. C. Wang, and M. Rowe, “The switch from latent to productive infection in Epstein-Barr virus-infected B cells is associated with sensitization to NK cell killing,” Journal of Virology, vol. 81, no. 2, pp. 474–482, 2007. View at Publisher · View at Google Scholar · View at Scopus
  116. H. Song, H. Park, J. Kim et al., “IDO metabolite produced by EBV-transformed B cells inhibits surface expression of NKG2D in NK cells via the c-Jun N-terminal kinase (JNK) pathway,” Immunology Letters, vol. 136, no. 2, pp. 187–193, 2011. View at Publisher · View at Google Scholar · View at Scopus
  117. A. Sawada, E. Sato, M. Koyama et al., “NK-cell repertoire is feasible for diagnosing Epstein-Barr virus-infected NK-cell lymphoproliferative disease and evaluating the treatment effect,” American Journal of Hematology, vol. 81, no. 8, pp. 576–581, 2006. View at Publisher · View at Google Scholar · View at Scopus
  118. K. Kida, R. Isozumi, and M. Ito, “Killing of human herpes virus 6-infected cells by lymphocytes cultured with interleukin-2 or -12,” Pediatrics International, vol. 42, no. 6, pp. 631–636, 2000. View at Publisher · View at Google Scholar · View at Scopus
  119. L. Flamand, I. Stefanescu, and J. Menezes, “Human herpesvirus-6 enhances natural killer cell cytotoxicity via IL-15,” Journal of Clinical Investigation, vol. 97, no. 6, pp. 1373–1381, 1996. View at Google Scholar · View at Scopus
  120. B. N. Atedzoe, A. Ahmad, and J. Menezes, “Enhancement of natural killer cell cytotoxicity by the human herpesvirus-7 via IL-15 induction,” Journal of Immunology, vol. 159, no. 10, pp. 4966–4972, 1997. View at Google Scholar · View at Scopus
  121. A. B. Tilden, R. Cauda, and C. E. Grossi, “Demonstration of NK cell-mediated lysis of varicella-zoster virus (VZV)-infected cells: characterization of the effector cells,” Journal of Immunology, vol. 136, no. 11, pp. 4243–4248, 1986. View at Google Scholar · View at Scopus
  122. M. Ito, S. Bandyopadhyay, and M. Matsumoto-Kobayashi, “Interleukin 2 enhances natural killing of varicella-zoster virus-infected targets,” Clinical and Experimental Immunology, vol. 65, no. 1, pp. 182–189, 1986. View at Google Scholar · View at Scopus
  123. A. R. Hayward, M. Herberger, and M. Lazslo, “Cellular interactions in the lysis of varicella-zoster virus infected human fibroblasts,” Clinical and Experimental Immunology, vol. 63, no. 1, pp. 141–146, 1986. View at Google Scholar · View at Scopus
  124. F. Rozenberg, C. Deback, and H. Agut, “Herpes simplex encephalitis: from virus to therapy,” Infectious Disorders Drug Targets, vol. 11, no. 3, pp. 235–250, 2011. View at Google Scholar · View at Scopus
  125. J.-P. Stahl, A. Mailles, L. Dacheux, and P. Morand, “Epidemiology of viral encephalitis in 2011,” Medecine et Maladies Infectieuses, vol. 41, no. 9, pp. 453–464, 2011. View at Publisher · View at Google Scholar
  126. S. Gantt and C. Casper, “Human herpesvirus 8-associated neoplasms: the roles of viral replication and antiviral treatment,” Current Opinion in Infectious Diseases, vol. 24, no. 4, pp. 295–301, 2011. View at Publisher · View at Google Scholar · View at Scopus
  127. G. S. Taylor and D. J. Blackbourn, “Infectious agents in human cancers: lessons in immunity and immunomodulation from gammaherpesviruses EBV and KSHV,” Cancer Letters, vol. 305, no. 2, pp. 263–278, 2011. View at Publisher · View at Google Scholar · View at Scopus
  128. C. Chisholm and L. Lopez, “Cutaneous infections caused by herpesviridae: a review,” Archives of Pathology and Laboratory Medicine, vol. 135, no. 10, pp. 1357–1362, 2011. View at Publisher · View at Google Scholar
  129. L. J. Al-Dujaili, P. P. Clerkin, C. Clement et al., “Ocular herpes simplex virus: how are latency, reactivation, recurrent disease and therapy interrelated?” Future Microbiology, vol. 6, no. 8, pp. 877–907, 2011. View at Google Scholar
  130. A. Berardi, L. Lugli, C. Rossi et al., “Neonatal herpes simplex virus,” Journal of Maternal-Fetal and Neonatal Medicine, vol. 24, supplement 1, pp. 88–90, 2011. View at Publisher · View at Google Scholar
  131. G. Fulci, L. Breymann, D. Gianni et al., “Cyclophosphamide enhances glioma virotherapy by inhibiting innate immune responses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 34, pp. 12873–12878, 2006. View at Publisher · View at Google Scholar · View at Scopus
  132. G. Fulci, N. Dmitrieva, D. Gianni et al., “Depletion of peripheral macrophages and brain microglia increases brain tumor titers of oncolytic viruses,” Cancer Research, vol. 67, no. 19, pp. 9398–9406, 2007. View at Publisher · View at Google Scholar · View at Scopus
  133. H. Wakimoto, G. Fulci, E. Tyminski, and E. A. Chiocca, “Altered expression of antiviral cytokine mRNAs associated with cyclophosphamide's enhancement of viral oncolysis,” Gene Therapy, vol. 11, no. 2, pp. 214–223, 2004. View at Publisher · View at Google Scholar · View at Scopus
  134. W. Haedicke, F. C. S. Ho, A. Chott et al., “Expression of CD94/NKG2A and killer immunoglobulin-like receptors in NK cells and a subset of extranodal cytotoxic T-cell lymphomas,” Blood, vol. 95, no. 11, pp. 3628–3630, 2000. View at Google Scholar · View at Scopus