Priming of NK cell anti-viral effector mechanisms by direct recognition of human cytomegalovirus

Frontiers in Immunology

Volumn 4, Issue FRB, 2013, Pages

  Muntasell, Aura ^a   Costa Garcia, Marcel ^b   Vera, Andrea ^a   Marina Garcia, Noemí ^b   Kirschning, Carsten J ^c   López Botet, Miguel ^a,b  

^a HOSPITAL DEL MAR   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

HCMV; NK cells; Pathogen associated pattern recognition receptors

Indexed keywords

BETA INTERFERON; CD56 ANTIGEN; CD69 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MESSENGER RNA; PATTERN RECOGNITION RECEPTOR; TOLL LIKE RECEPTOR 2;

ANTIGEN RECOGNITION; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOTOXICITY; DEGRANULATION; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IMMUNE RESPONSE; NATURAL KILLER CELL; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; VIRUS CELL INTERACTION;

EID: 84883715742     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00040     Document Type: Article

References (54)

1. Akira, S., Uematsu, S., and Takeuchi, O. (2006). Pathogen recognition and innate immunity. Cell 124, 783-801.
2. Alter, G., Malenfant, J. M., and Altfeld, M. (2004). CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 294, 15-22.
3. Athie-Morales, V., O'Connor, G. M., and Gardiner, C. M. (2008). Activation of human NK cells by the bacterial pathogen-associated molecular pattern muramyl dipeptide. J. Immunol. 180, 4082-4089.
4. Barbalat, R., Lau, L., Locksley, R. M., and Barton, G. M. (2009). Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat. Immunol. 10, 1200-1207.
5. Becker, I., Salaiza, N., Aguirre, M., Delgado, J., Carrillo-Carrasco, N., Kobeh, L. G., et al. (2003). Leishmania lipophosphoglycan (LPG) activates NK cells through toll-like receptor-2. Mol. Biochem. Parasitol. 130, 65-74.
6. Bieback, K., Lien, E., Klagge, I. M., Avota, E., Schneider-Schaulies, J., Duprex, W. P., et al. (2002). Hemagglutinin protein of wild-type measles virus activates toll-like receptor 2 signaling. J. Virol. 76, 8729-8736.
7. Biron, C. A., Byron, K. S., and Sullivan, J. L. (1989). Severe herpesvirus infections in an adolescent without natural killer cells. N. Engl. J. Med. 320, 1731-1735.
8. Biron, C. A., Nguyen, K. B., Pien, G. C., Cousens, L. P., and Salazar-Mather, T. P. (1999). Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 17, 189-220.
9. Boehme, K. W., Guerrero, M., and Compton, T. (2006). Human cytomegalovirus envelope glycoproteins B and H are necessary for TLR2 activation in permissive cells. J. Immunol. 177, 7094-7102.
10. Carvalho, A., Cunha, C., Carotti, A., Aloisi, T., Guarrera, O., Di Ianni, M., et al. (2009). Polymorphisms in Toll-like receptor genes and susceptibility to infections in allogeneic stem cell transplantation. Exp. Hematol. 37, 1022-1029.
11. Chalifour, A., Jeannin, P., Gauchat, J. F., Blaecke, A., Malissard, M., N'Guyen, T., et al. (2004). Direct bacterial protein PAMP recognition by human NK cells involves TLRs and triggers alpha-defensin production. Blood 104, 1778-1783.
12. Chang, S., Dolganiuc, A., and Szabo, G. (2007). Toll-like receptors 1 and 6 are involved in TLR2-mediated macrophage activation by hepatitis C virus core and NS3 proteins. J. Leukoc. Biol. 82, 479-487.
13. Compton, T. (2004). Receptors and immune sensors: the complex entry path of human cytomegalovirus. Trends Cell Biol. 14, 5-8.
14. DeFilippis, V. R., Sali, T., Alvarado, D., White, L., Bresnahan, W., and Fruh, K. J. (2010). Activation of the interferon response by human cytomegalovirus occurs via cytoplasmic double-stranded DNA but not glycoprotein B. J. Virol. 84, 8913-8925.
15. Duluc, D., Tan, F., Scotet, M., Blanchard, S., Fremaux, I., Garo, E., et al. (2009). PolyI:C plus IL-2 or IL-12 induce IFN-gamma production by human NK cells via autocrine IFN-beta. Eur. J. Immunol. 39, 2877-2884.
16. Eriksson, M., Meadows, S. K., Basu, S., Mselle, T. F., Wira, C. R., and Sentman, C. L. (2006). TLRs mediate IFN-gamma production by human uterine NK cells in endometrium. J. Immunol. 176, 6219-6224.
17. Girart, M. V., Fuertes, M. B., Domaica, C. I., Rossi, L. E., and Zwirner, N. W. (2007). Engagement of TLR3, TLR7, and NKG2D regulate IFN-gamma secretion but not NKG2D-mediated cytotoxicity by human NK cells stimulated with suboptimal doses of IL-12. J. Immunol. 179, 3472-3479.
18. Gorski, K. S., Waller, E. L., Bjornton-Severson, J., Hanten, J. A., Riter, C. L., Kieper, W. C., et al. (2006). Distinct indirect pathways govern human NK-cell activation by TLR-7 and TLR-8 agonists. Int. Immunol. 18, 1115-1126.
19. Hart, O. M., Athie-Morales, V., O'Connor, G. M., and Gardiner, C. M. (2005). TLR7/8-mediated activation of human NK cells results in accessory cell-dependent IFN-gamma production. J. Immunol. 175, 1636-1642.
20. Hornung, V., Rothenfusser, S., Britsch, S., Krug, A., Jahrsdorfer, B., Giese, T., et al. (2002). Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J. Immunol. 168, 4531-4537.
21. Janson, P. C., Marits, P., Thorn, M., Ohlsson, R., and Winqvist, O. (2008). CpG methylation of the IFNG gene as a mechanism to induce immunosuppression in tumor-infiltrating lymphocytes. J. Immunol. 181, 2878-2886.
22. Kang, S. H., Abdel-Massih, R. C., Brown, R. A., Dierkhising, R. A., Kremers, W. K., and Razonable, R. R. (2012). Homozygosity for the toll-like receptor 2 R753Q single-nucleotide polymorphism is a risk factor for cytomegalovirus disease after liver transplantation. J. Infect. Dis. 205, 639-646.
23. Kannan, Y., Yu, J., Raices, R. M., Seshadri, S., Wei, M., Caligiuri, M. A., et al. (2011). IkappaBzeta augments IL-12- and IL-18-mediated IFN-gamma production in human NK cells. Blood 117, 2855-2863.
24. Kijpittayarit, S., Eid, A. J., Brown, R. A., Paya, C. V., and Razonable, R. R. (2007). Relationship between Toll-like receptor 2 polymorphism and cytomegalovirus disease after liver transplantation. Clin. Infect. Dis. 44, 1315-1320.
25. Krug, A., French, A. R., Barchet, W., Fischer, J. A., Dzionek, A., Pingel, J. T., et al. (2004). TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 21, 107-119.
26. Lanier, L. L. (2008). Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 9, 495-502.
27. Leoni, V., Gianni, T., Salvioli, S., and Campadelli-Fiume, G. (2012). Herpes simplex virus glycoproteins gH/gL and gB bind Toll-like receptor 2, and soluble gH/gL is sufficient to activate NF-kappaB. J. Virol. 86, 6555-6562.
28. Magri, G., Muntasell, A., Romo, N., Saez-Borderias, A., Pende, D., Geraghty, D. E., et al. (2011). NKp46 and DNAM-1 NK-cell receptors drive the response to human cytomegalovirus-infected myeloid dendritic cells overcoming viral immune evasion strategies. Blood 117, 848-856.
29. Marcenaro, E., Ferranti, B., Falco, M., Moretta, L., and Moretta, A. (2008). Human NK cells directly recognize Mycobacterium bovis via TLR2 and acquire the ability to kill monocyte-derived DC. Int. Immunol. 20, 1155-1167.
30. Marr, K. J., Jones, G. J., Zheng, C., Huston, S. M., Timm-McCann, M., Islam, A., et al. (2009). Cryptococcus neoformans directly stimulates perforin production and rearms NK cells for enhanced anticryptococcal microbicidal activity. Infect. Immun. 77, 2436-2446.
31. Martinez, J., Huang, X., and Yang, Y. (2008). Direct action of type I IFN on NK cells is required for their activation in response to vaccinia viral infection in vivo. J. Immunol. 180, 1592-1597.
32. Martinez, J., Huang, X., and Yang, Y. (2010). Direct TLR2 signaling is critical for NK cell activation and function in response to vaccinia viral infection. PLoS Pathog. 6:e1000811. doi:10.1371/journal.ppat.1000811
33. Meng, G., Rutz, M., Schiemann, M., Metzger, J., Grabiec, A., Schwandner, R., et al. (2004). Antagonistic antibody prevents toll-like receptor 2-driven lethal shock-like syndromes. J. Clin. Invest. 113, 1473-1481.
34. Miettinen, M., Sareneva, T., Julkunen, I., and Matikainen, S. (2001). IFNs activate toll-like receptor gene expression in viral infections. Genes Immun. 2, 349-355.
35. Miyake, T., Satoh, T., Kato, H., Matsushita, K., Kumagai, Y., Vandenbon, A., et al. (2010). IkappaBzeta is essential for natural killer cell activation in response to IL-12 and IL-18. Proc. Natl. Acad. Sci. U.S.A. 107, 17680-17685.
36. Mocarski, E. S., and Courcelle, C. T. (2001). "Cytomegaloviruses and their replication," in Fields Virology, eds D. M. Knipe, P. M. Howley, D. E. Griffin, and R. A. Lamb (Philadelphia: Lippincott, Williams and Wilkins), 2629-2673.
37. Mori, S., Jewett, A., Cavalcanti, M., Murakami-Mori, K., Nakamura, S., and Bonavida, B. (1998). Differential regulation of human NK cell-associated gene expression following activation by IL-2, IFN-alpha and PMA/ionomycin. Int. J. Oncol. 12, 1165-1170.
38. Muntasell, A., Magri, G., Pende, D., Angulo, A., and Lopez-Botet, M. (2010). Inhibition of NKG2D expression in NK cells by cytokines secreted in response to human cytomegalovirus infection. Blood 115, 5170-5179.
39. Nowlin, D. M., Cooper, N. R., and Compton, T. (1991). Expression of a human cytomegalovirus receptor correlates with infectibility of cells. J. Virol. 65, 3114-3121.
40. Orange, J. S., and Ballas, Z. K. (2006). Natural killer cells in human health and disease. Clin. Immunol. 118, 1-10.
41. Perez-Villar, J. J., Melero, I., Gismondi, A., Santoni, A., and Lopez-Botet, M. (1996). Functional analysis of alpha 1 beta 1 integrin in human natural killer cells. Eur. J. Immunol. 26, 2023-2029.
42. Perrot, I., Deauvieau, F., Massacrier, C., Hughes, N., Garrone, P., Durand, I., et al. (2010). TLR3 and Rig-like receptor on myeloid dendritic cells and Rig-like receptor on human NK cells are both mandatory for production of IFN-gamma in response to double-stranded RNA. J. Immunol. 185, 2080-2088.
43. Rathinam, V. A., Jiang, Z., Waggoner, S. N., Sharma, S., Cole, L. E., Waggoner, L., et al. (2010). The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11, 395-402.
44. Rice, G. P., Schrier, R. D., and Oldstone, M. B. (1984). Cytomegalovirus infects human lymphocytes and monocytes: virus expression is restricted to immediate-early gene products. Proc. Natl. Acad. Sci. U.S.A. 81, 6134-6138.
45. Roda, J. M., Parihar, R., and Carson, W. E. III. (2005). CpG-containing oligodeoxynucleotides act through TLR9 to enhance the NK cell cytokine response to antibody-coated tumor cells. J. Immunol. 175, 1619-1627.
46. Romo, N., Magri, G., Muntasell, A., Heredia, G., Baia, D., Angulo, A., et al. (2011). Natural killer cell-mediated response to human cytomegalovirus-infected macrophages is modulated by their functional polarization. J. Leukoc. Biol. 90, 717-726.
47. Sinzger, C., Schmidt, K., Knapp, J., Kahl, M., Beck, R., Waldman, J., et al. (1999). Modification of human cytomegalovirus tropism through propagation in vitro is associated with changes in the viral genome. J. Gen. Virol. 80(Pt 11), 2867-2877.
48. Sivori, S., Falco, M., Della, C. M., Carlomagno, S., Vitale, M., Moretta, L., et al. (2004). CpG and double-stranded RNA trigger human NK cells by Toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 101, 10116-10121.
49. Szomolanyi-Tsuda, E., Liang, X., Welsh, R. M., Kurt-Jones, E. A., and Finberg, R. W. (2006). Role for TLR2 in NK cell-mediated control of murine cytomegalovirus in vivo. J. Virol. 80, 4286-4291.
50. Tabeta, K., Georgel, P., Janssen, E., Du, X., Hoebe, K., Crozat, K., et al. (2004). Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl. Acad. Sci. U.S.A. 101, 3516-3521.
51. Waddell, S. J., Popper, S. J., Rubins, K. H., Griffiths, M. J., Brown, P. O., Levin, M., et al. (2010). Dissecting interferon-induced transcriptional programs in human peripheral blood cells. PLoS ONE 5:e9753. doi:10.1371/journal.pone.0009753
52. Wang, P., Gu, Y., Zhang, Q., Han, Y., Hou, J., Lin, L., et al. (2012). Identification of resting and type I IFN-activated human NK cell miRNomes reveals microRNA-378 and microRNA-30e as negative regulators of NK cell cytotoxicity. J. Immunol. 189, 211-221.
53. Zhu, J., Martinez, J., Huang, X., and Yang, Y. (2007). Innate immunity against vaccinia virus is mediated by TLR2 and requires TLR-independent production of IFN-beta. Blood 109, 619-625.
54. Zucchini, N., Bessou, G., Traub, S., Robbins, S. H., Uematsu, S., Akira, S., et al. (2008). Cutting edge: overlapping functions of TLR7 and TLR9 for innate defense against a herpesvirus infection. J. Immunol. 180, 5799-5803.