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Review

Viral inhibitors of NKG2D ligands for tumor surveillance

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Pages 1375-1387 | Received 18 Feb 2016, Accepted 14 Jun 2016, Published online: 29 Jun 2016

References

  • Ferlazzo G, Thomas D, Lin SL, et al. The abundant NK cells in human secondary lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic. J Immunol. 2004;172:1455–1462.
  • Robertson MJ. Role of chemokines in the biology of natural killer cells. J Leukoc Biol. 2002;71:173–183.
  • Anfossi N, Andre P, Guia S, et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity. 2006;25:331–342.
  • Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol. 2001;22:633–640.
  • Lanier LL. NKG2D receptor and its ligands in host defense. Cancer Immunol Res. 2015;3:575–582.
  • Zafirova B, Wensveen FM, Gulin M, et al. Regulation of immune cell function and differentiation by the NKG2D receptor. Cell Mol Life Sci. 2011;68:3519–3529.
  • Koch J, Steinle A, Watzl C, et al. Activating natural cytotoxicity receptors of natural killer cells in cancer and infection. Trends Immunol. 2013;34:182–191.
  • Knight A, Arnouk H, Britt W, et al. CMV-independent lysis of glioblastoma by ex vivo expanded/activated Vδ1+ γδ T cells. PLoS One. 2013;8:e68729.
  • Poggi A, Zocchi MR. Gammadelta T lymphocytes as a first line of immune defense: old and new ways of antigen recognition and implications for cancer immunotherapy. Front Immunol. 2014;5:575.
  • Champsaur M, Lanier LL. Effect of NKG2D ligand expression on host immune responses. Immunol Rev. 2010;235:267–285.
  • Ullrich E, Koch J, Cerwenka A, et al. New prospects on the NKG2D/NKG2DL system for oncology. Oncoimmunology. 2013;2:e26097.
  • Diefenbach A, Tomasello E, Lucas M, et al. Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D. Nat Immunol. 2002;3:1142–1149.
  • Chang C, Dietrich J, Harpur AG, et al. Cutting edge: KAP10, a novel transmembrane adapter protein genetically linked to DAP12 but with unique signaling properties. J Immunol. 1999;163:4651–4654.
  • Wu J, Song Y, Bakker AB, et al. An activating immunoreceptor complex formed by NKG2D and DAP10. Science. 1999;285:730–732.
  • Zou Z, Nomura M, Takihara Y, et al. Isolation and characterization of retinoic acid-inducible cDNA clones in F9 cells: a novel cDNA family encodes cell surface proteins sharing partial homology with MHC class I molecules. J Biochem. 1996;119:319–328.
  • Carapito R, Bahram S. Genetics, genomics, and evolutionary biology of NKG2D ligands. Immunol Rev. 2015;267:88–116.
  • Raulet DH, Gasser S, Gowen BG, et al. Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol. 2013;31:413–441.
  • de Martel C, Ferlay J, Franceschi S, et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 2012;13:607–615.
  • Finton KA, Strong RK. Structural insights into activation of antiviral NK cell responses. Immunol Rev. 2012;250:239–257.
  • Mesri EA, Feitelson MA, Munger K. Human viral oncogenesis: a cancer hallmarks analysis. Cell Host Microbe. 2014;15:266–282.
  • Beltran D, Lopez-Verges S. NK Cells during dengue disease and their recognition of dengue virus-infected cells. Front Immunol. 2014;5:192.
  • Li Y, Mariuzza RA. Structural basis for recognition of cellular and viral ligands by NK cell receptors. Front Immunol. 2014;5:123.
  • Raulet DH. Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol. 2003;3:781–790.
  • Ogasawara K, Lanier LL. NKG2D in NK and T cell-mediated immunity. J Clin Immunol. 2005;25:534–540.
  • Muller S, Zocher G, Steinle A, et al. Structure of the HCMV UL16-MICB complex elucidates select binding of a viral immunoevasin to diverse NKG2D ligands. PLoS Pathog. 2010;6:e1000723.
  • Bennett NJ, Ashiru O, Morgan FJE, et al. Intracellular sequestration of the NKG2D ligand ULBP3 by human cytomegalovirus. J Immunol. 2010;185:1093–1102.
  • Ashiru O, Bennett NJ, Boyle LH, et al. NKG2D ligand MICA is retained in the cis-Golgi apparatus by human cytomegalovirus protein UL142. J Virol. 2009;83:12345–12354.
  • Wilkinson GWG, Tomasec P, Stanton RJ, et al. Modulation of natural killer cells by human cytomegalovirus. J Clin Virol. 2008;41:206–212.
  • Fielding CA, Aicheler R, Stanton RJ, et al. Two novel human cytomegalovirus NK cell evasion functions target MICA for lysosomal degradation. PLoS Pathog. 2014;10:e1004058.
  • Seidel E, Le VT, Bar-On Y, et al. Dynamic co-evolution of host and pathogen: HCMV downregulates the prevalent allele MICA *008 to escape elimination by NK cells. Cell Rep. 2015;10:968–982.
  • Nachmani D, Lankry D, Wolf DG, et al. The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat Immunol. 2010;11:806–813.
  • Wang R, Natarajan K, Revilleza MJR, et al. Structural basis of mouse cytomegalovirus m152/gp40 interaction with RAE1γ reveals a paradigm for MHC/MHC interaction in immune evasion. Proc Natl Acad Sci U S A. 2012;109:E3578–87.
  • Krmpotic A, Hasan M, Loewendorf A, et al. NK cell activation through the NKG2D ligand MULT-1 is selectively prevented by the glycoprotein encoded by mouse cytomegalovirus gene m145. J Exp Med. 2005;201:211–220.
  • Lodoen MB, Abenes G, Umamoto S, et al. The cytomegalovirus m155 gene product subverts natural killer cell antiviral protection by disruption of H60-NKG2D interactions. J Exp Med. 2004;200:1075–1081.
  • Lenac T, Budt M, Arapovic J, et al. The herpesviral Fc receptor fcr-1 down-regulates the NKG2D ligands MULT-1 and H60. J Exp Med. 2006;203:1843–1850.
  • Giuliani E, Vassena L, Cerboni C, et al. Release of Soluble ligands for the activating NKG2D receptor: one more immune evasion strategy evolved by HIV-1? Curr Drug Targets. 2016;17:54–64.
  • Richard J, Pham TNQ, Ishizaka Y, et al. Viral protein R upregulates expression of ULBP2 on uninfected bystander cells during HIV-1 infection of primary CD4+ T lymphocytes. Virology. 2013;443:248–256.
  • Matusali G, Potesta M, Santoni A, et al. The human immunodeficiency virus type 1 Nef and Vpu proteins downregulate the natural killer cell-activating ligand PVR. J Virol. 2012;86:4496–4504.
  • Thomas M, Boname JM, Field S, et al. Down-regulation of NKG2D and NKp80 ligands by Kaposi’s sarcoma-associated herpesvirus K5 protects against NK cell cytotoxicity. Proc Natl Acad Sci U S A. 2008;105:1656–1661.
  • Thomas M, Wills M, Lehner PJ. Natural killer cell evasion by an E3 ubiquitin ligase from Kaposi’s sarcoma-associated herpesvirus. Biochem Soc Trans. 2008;36:459–463.
  • Wen C, He X, Ma H, et al. Hepatitis C virus infection downregulates the ligands of the activating receptor NKG2D. Cell Mol Immunol. 2008;5:475–478.
  • Imran M, Waheed Y, Manzoor S, et al. Interaction of Hepatitis C virus proteins with pattern recognition receptors. Virol J. 2012;9:126.
  • Sene D, Levasseur F, Abel M, et al. Hepatitis C virus (HCV) evades NKG2D-dependent NK cell responses through NS5A-mediated imbalance of inflammatory cytokines. PLoS Pathog. 2010;6:e1001184.
  • Russier M, Reynard S, Carnec X, et al. The exonuclease domain of Lassa virus nucleoprotein is involved in antigen-presenting-cell-mediated NK cell responses. J Virol. 2014;88:13811–13820.
  • Lazear E, Peterson LW, Nelson CA, et al. Crystal structure of the cowpox virus-encoded NKG2D ligand OMCP. J Virol. 2013;87:840–850.
  • McSharry BP, Burgert HG, Owen DP, et al. Adenovirus E3/19K promotes evasion of NK cell recognition by intracellular sequestration of the NKG2D ligands major histocompatibility complex class I chain-related proteins A and B. J Virol. 2008;82:4585–4594.
  • Campbell TM, McSharry BP, Steain M, et al. Varicella-zoster virus and herpes simplex virus 1 differentially modulate NKG2D ligand expression during productive infection. J Virol. 2015;89:7932–7943.
  • Matthews NC, Goodier MR, Robey RC, et al. Killing of Kaposi’s sarcoma-associated herpesvirus-infected fibroblasts during latent infection by activated natural killer cells. Eur J Immunol. 2011;41:1958–1968.
  • Schepis D, D’Amato M, Studahl M, et al. Herpes simplex virus infection downmodulates NKG2D ligand expression. Scand J Immunol. 2009;69:429–436.
  • Li Y, Wang JJ, Gao S, et al. Decreased peripheral natural killer cells activity in the immune activated stage of chronic hepatitis B. PLoS One. 2014;9:e86927.
  • Jensen H, Andresen L, Nielsen J, et al. Vesicular stomatitis virus infection promotes immune evasion by preventing NKG2D-ligand surface expression. PLoS One. 2011;6:e23023.
  • Toka FN, Nfon C, Dawson H, et al. Natural killer cell dysfunction during acute infection with foot-and-mouth disease virus. Clin Vaccine Immunol. 2009;16:1738–1749.
  • Guo H, Kumar P, Moran TM, et al. The functional impairment of natural killer cells during influenza virus infection. Immunol Cell Biol. 2009;87:579–589.
  • Thanapati S, Das R, Tripathy AS. Phenotypic and functional analyses of NK and NKT-like populations during the early stages of chikungunya infection. Front Microbiol. 2015;6:895.
  • Brandstadter JD, Huang X, Yang Y. NK cell-extrinsic IL-18 signaling is required for efficient NK-cell activation by vaccinia virus. Eur J Immunol. 2014;44:2659–2666.
  • Pappworth IY, Wang EC, Rowe M. The switch from latent to productive infection in epstein-barr virus-infected B cells is associated with sensitization to NK cell killing. J Virol. 2007;81:474–482.
  • Fortin C, Huang X, Yang Y. Both NK cell-intrinsic and -extrinsic STAT1 signaling are required for NK cell response against vaccinia virus. J Immunol. 2013;191:363–368.
  • Siren J, Sareneva T, Pirhonen J, et al. Cytokine and contact-dependent activation of natural killer cells by influenza A or Sendai virus-infected macrophages. J Gen Virol. 2004;85:2357–2364.
  • Ogawa T, Tsuji-Kawahara S, Yuasa T, et al. Natural killer cells recognize friend retrovirus-infected erythroid progenitor cells through NKG2D-RAE-1 interactions In Vivo. J Virol. 2011;85:5423–5435.
  • Klingel K, Fabritius C, Sauter M, et al. The activating receptor NKG2D of natural killer cells promotes resistance against enterovirus-mediated inflammatory cardiomyopathy. J Pathol. 2014;234:164–177.
  • Walsh KB, Lodoen MB, Edwards RA, et al. Evidence for differential roles for NKG2D receptor signaling in innate host defense against coronavirus-induced neurological and liver disease. J Virol. 2008;82:3021–3030.
  • Deb C, Howe CL. NKG2D contributes to efficient clearance of picornavirus from the acutely infected murine brain. J Neurovirol. 2008;14:261–266.
  • Fang M, Lanier LL, Sigal LJ. A role for NKG2D in NK cell-mediated resistance to poxvirus disease. PLoS Pathog. 2008;4:e30.
  • Draghi M, Pashine A, Sanjanwala B, et al. NKp46 and NKG2D recognition of infected dendritic cells is necessary for NK cell activation in the human response to influenza infection. J Immunol. 2007;178:2688–2698.
  • Chisholm SE, Howard K, Gomez MV, et al. Expression of ICP0 is sufficient to trigger natural killer cell recognition of herpes simplex virus-infected cells by natural cytotoxicity receptors. J Infect Dis. 2007;195:1160–1168.
  • Rickinson AB, Long HM, Palendira U, et al. Cellular immune controls over Epstein-Barr virus infection: new lessons from the clinic and the laboratory. Trends Immunol. 2014;35:159–169.
  • Williams LR, Quinn LL, Rowe M, et al. Induction of the lytic cycle sensitizes Epstein-Barr virus-infected B cells to NK cell killing that is counteracted by virus-mediated NK cell evasion mechanisms in the late lytic cycle. J Virol. 2015;90:947–958.
  • Azimi N, Jacobson S, Tanaka Y, et al. Immunostimulation by induced expression of NKG2D and its MIC ligands in HTLV-1-associated neurologic disease. Immunogenetics. 2006;58:252–258.
  • Dandekar AA, O’Malley K, Perlman S. Important roles for gamma interferon and NKG2D in gammadelta T-cell-induced demyelination in T-cell receptor beta-deficient mice infected with a coronavirus. J Virol. 2005;79:9388–9396.
  • Zou Y, Chen T, Han M, et al. Increased killing of liver NK cells by Fas/Fas ligand and NKG2D/NKG2D ligand contributes to hepatocyte necrosis in virus-induced liver failure. J Immunol. 2010;184:466–475.
  • Vilarinho S, Ogasawara K, Nishimura S, et al. Blockade of NKG2D on NKT cells prevents hepatitis and the acute immune response to hepatitis B virus. Proc Natl Acad Sci U S A. 2007;104:18187–18192.
  • Ichim CV. Revisiting immunosurveillance and immunostimulation: implications for cancer immunotherapy. J Transl Med. 2005;3:8.
  • Outzen HC, Custer RP, Eaton GJ, et al. Spontaneous and induced tumor incidence in germfree “nude” mice. J Reticuloendothel Soc. 1975;17:1–9.
  • Chester C, Fritsch K, Kohrt HE. Natural killer cell immunomodulation: targeting activating, inhibitory, and co-stimulatory receptor signaling for cancer immunotherapy. Front Immunol. 2015;6:601.
  • Iannello A, Thompson TW, Ardolino M, et al. Immunosurveillance and immunotherapy of tumors by innate immune cells. Curr Opin Immunol. 2016;38:52–58.
  • Dahlberg CIM, Sarhan D, Chrobok M, et al. Natural killer cell-based therapies targeting cancer: possible strategies to gain and sustain anti-tumor activity. Front Immunol. 2015;6:605.
  • Talmadge JE, Meyers KM, Prieur DJ, et al. Role of NK cells in tumour growth and metastasis in beige mice. Nature. 1980;284:622–624.
  • Gorelik E, Wiltrout RH, Okumura K, et al. Role of NK cells in the control of metastatic spread and growth of tumor cells in mice. Int J Cancer. 1982;30:107–112.
  • Haliotis T, Ball JK, Dexter D, et al. Spontaneous and induced primary oncogenesis in natural killer (NK)-cell-deficient beige mutant mice. Int J Cancer. 1985;35:505–513.
  • Harning R, Koo GC, Szalay J. Regulation of the metastasis of murine ocular melanoma by natural killer cells. Invest Ophthalmol Vis Sci. 1989;30:1909–1915.
  • Roder JC, Haliotis T, Klein M, et al. A new immunodeficiency disorder in humans involving NK cells. Nature. 1980;284:553–555.
  • Kobayashi N. Malignant neoplasms in registered cases of primary immunodeficiency syndrome. Jpn J Clin Oncol. 1985;15 Suppl 1:307–312.
  • Giri N, Alter BP, Penrose K, et al. Immune status of patients with inherited bone marrow failure syndromes. Am J Hematol. 2015;90:702–708.
  • Smyth MJ, Hayakawa Y, Takeda K, et al. New aspects of natural-killer-cell surveillance and therapy of cancer. Nat Rev Cancer. 2002;2:850–861.
  • Imai K, Matsuyama S, Miyake S, et al. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet. 2000;356:1795–1799.
  • Strayer DR, Carter WA, Mayberry SD, et al. Low natural cytotoxicity of peripheral blood mononuclear cells in individuals with high familial incidences of cancer. Cancer Res. 1984;44:370–374.
  • Bovbjerg DH, Valdimarsdottir H. Familial cancer, emotional distress, and low natural cytotoxic activity in healthy women. Ann Oncol. 1993;4:745–752.
  • Bouvard V, Baan R, Straif K, et al. A review of human carcinogens–part B: biological agents. Lancet Oncol. 2009;10:321–322.
  • Andrade F, Fellows E, Jenne DE, et al. Granzyme H destroys the function of critical adenoviral proteins required for viral DNA replication and granzyme B inhibition. EMBO J. 2007;26:2148–2157.
  • Tang H, Li C, Wang L, et al. Granzyme H of cytotoxic lymphocytes is required for clearance of the hepatitis B virus through cleavage of the hepatitis B virus X protein. J Immunol. 2012;188:824–831.
  • Wu J, Zhang XJ, Shi KQ, et al. Hepatitis B surface antigen inhibits MICA and MICB expression via induction of cellular miRNAs in hepatocellular carcinoma cells. Carcinogenesis. 2014;35:155–163.
  • Caja F, Vannucci L. TGFβ: a player on multiple fronts in the tumor microenvironment. J Immunotoxicol. 2015;12:300–307.
  • Kumthip K, Maneekarn N. The role of HCV proteins on treatment outcomes. Virol J. 2015;12:217.
  • Cesarman E, Mesri EA. Kaposi sarcoma-associated herpesvirus and other viruses in human lymphomagenesis. Curr Top Microbiol Immunol. 2007;312:263–287.
  • Wang XM, Xu CG. [Diagnostic value of serum levels of BamHI-W, LMP-1 and BZLF1 in NK/T-cell lymphoma]. Zhonghua Xue Ye Xue Za Zhi. 2013;34:36–40.
  • Robinson AR, Kwek SS, Kenney SC, et al. The B-cell specific transcription factor, Oct-2, promotes Epstein-Barr virus latency by inhibiting the viral immediate-early protein, BZLF1. PLoS Pathog. 2012;8:e1002516.
  • Chou YY, Gao JI, Chang SF, et al. Rapamycin inhibits lipopolysaccharide induction of granulocyte-colony stimulating factor and inducible nitric oxide synthase expression in macrophages by reducing the levels of octamer-binding factor-2. FEBS J. 2011;278:85–96.
  • Tikhmyanova N, Schultz DC, Lee T, et al. Identification of a new class of small molecules that efficiently reactivate latent Epstein-Barr Virus. ACS Chem Biol. 2014;9:785–795.
  • Yoshida N, Chihara D. Incidence of adult T-cell leukemia/lymphoma in nonendemic areas. Curr Treat Options Oncol. 2015;16:7.
  • Quaresma JA, Yoshikawa GT, Koyama RV, et al. HTLV-1, immune response and autoimmunity. Viruses. 2015;8:5.
  • Norris PJ, Hirschkorn DF, DeVita DA, et al. Human T cell leukemia virus type 1 infection drives spontaneous proliferation of natural killer cells. Virulence. 2010;1:19–28.
  • Wen KW, Damania B. Kaposi sarcoma-associated herpesvirus (KSHV): molecular biology and oncogenesis. Cancer Lett. 2010;289:140–150.
  • Dupuy S, Lambert M, Zucman D, et al. Human Herpesvirus 8 (HHV8) sequentially shapes the NK cell repertoire during the course of asymptomatic infection and Kaposi sarcoma. PLoS Pathog. 2012;8:e1002486.
  • Rohner E, Wyss N, Heg Z, et al. HIV and human herpesvirus 8 co-infection across the globe: systematic review and meta-analysis. Int J Cancer. 2016;138:45–54.
  • Andrei G, Snoeck R. Kaposi’s sarcoma-associated herpesvirus: the role of lytic replication in targeted therapy. Curr Opin Infect Dis. 2015;28:611–624.
  • Lambert PJ, Shahrier AZ, Whitman AG, et al. Targeting the PI3K and MAPK pathways to treat Kaposi’s-sarcoma-associated herpes virus infection and pathogenesis. Expert Opin Ther Targets. 2007;11:589–599.
  • Chitadze G, Bhat J, Lettau M, et al. Generation of soluble NKG2D ligands: proteolytic cleavage, exosome secretion and functional implications. Scand J Immunol. 2013;78:120–129.
  • Matusali G, Tchidjou HK, Pontrelli G, et al. Soluble ligands for the NKG2D receptor are released during HIV-1 infection and impair NKG2D expression and cytotoxicity of NK cells. Faseb J. 2013;27:2440–2450.
  • Richard J, Sindhu S, Pham TNQ, et al. HIV-1 Vpr up-regulates expression of ligands for the activating NKG2D receptor and promotes NK cell-mediated killing. Blood. 2010;115:1354–1363.
  • Pollicino T, Koumbi L. Role natural killer group 2D-ligand interactions in hepatitis B infection. World J Hepatol. 2015;7:819–824.
  • Ashiru O, Boutet P, Fernández-Messina L, et al. Natural killer cell cytotoxicity is suppressed by exposure to the human NKG2D ligand MICA*008 that is shed by tumor cells in exosomes. Cancer Res. 2010;70:481–489.

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