Human cytomegalovirus-induced NKG2hi CD57hi natural killer cells are effectors dependent on humoral antiviral immunity

Journal of Virology

Volumn 87, Issue 13, 2013, Pages 7717-7725

  Wu, Zeguang ^a   Sinzger, Christian ^a   Frascaroli, Giada ^a   Reichel, Johanna ^b   Bayer, Carina ^a   Wang, Li ^a   Schirmbeck, Reinhold ^a   Mertens, Thomas ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD57 ANTIGEN;

ADAPTIVE IMMUNITY; ADOPTIVE IMMUNOTHERAPY; ANTIBODY SPECIFICITY; ARTICLE; CELLULAR IMMUNITY; CROSS LINKING; CYTOTOXICITY; HUMAN CYTOMEGALOVIRUS; HUMORAL IMMUNITY; MACROPHAGE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL;

ANTIBODIES, VIRAL; ANTIGENS, CD57; CELL LINE, TUMOR; CYTOMEGALOVIRUS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GPI-LINKED PROTEINS; HUMANS; IMMUNITY, HUMORAL; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; MACROPHAGES; NEUTRALIZATION TESTS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; RECEPTORS, IGG; STATISTICS, NONPARAMETRIC;

EID: 84880382483     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01096-13     Document Type: Article

References (50)

1. Lee SH, Miyagi T, Biron CA. 2007. Keeping NK cells in highly regulated antiviral warfare. Trends Immunol. 28:252-259.
2. Biron CA, Byron KS, Sullivan JL. 1989. Severe herpesvirus infections in an adolescent without natural killer cells. N. Engl. J. Med. 320:1731-1735.
3. Kuijpers TW, Baars PA, Dantin C, van den Burg M, van Lier RA, Roosnek E. 2008. Human NK cells can control CMV infection in the absence of T cells. Blood 112:914-915.
4. Hertenstein B, Hampl W, Bunjes D, Wiesneth M, Duncker C, Koszinowski U, Heimpel H, Arnold R, Mertens T. 1995. In vivo/ex vivo T cell depletion for GVHD prophylaxis influences onset and course of active cytomegalovirus infection and disease after BMT. Bone Marrow Transplant. 15:387-393.
5. Venema H, van den Berg AP, van Zanten C, van Son WJ, van der Giessen M, The TH. 1994. Natural killer cell responses in renal transplant patients with cytomegalovirus infection. J. Med. Virol. 42:188-192.
6. Wilkinson GW, Tomasec P, Stanton RJ, Armstrong M, Prod'homme V, Aicheler R, McSharry BP, Rickards CR, Cochrane D, Llewellyn-Lacey S, Wang EC, Griffin CA, Davison AJ. 2008. Modulation of natural killer cells by human cytomegalovirus. J. Clin. Virol. 41:206-212.
7. Dokun AO, Kim S, Smith HR, Kang HS, Chu DT, Yokoyama WM. 2001. Specific and nonspecific NK cell activation during virus infection. Nat. Immunol. 2:951-956.
8. O'Leary JG, Goodarzi M, Drayton DL, von Andrian UH. 2006. T celland B cell-independent adaptive immunity mediated by natural killer cells. Nat. Immunol. 7:507-516.
9. Sun JC, Beilke JN, Lanier LL. 2009. Adaptive immune features of natural killer cells. Nature 457:557-561.
10. Guma M, Angulo A, Vilches C, Gomez-Lozano N, Malats N, LopezBotet M. 2004. Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104:3664-3671.
11. hi natural killer cell subset during acute human cytomegalovirus infection. Proc. Natl. Acad. Sci. U. S. A. 108:14725-14732.
12. Guma M, Cabrera C, Erkizia I, Bofill M, Clotet B, Ruiz L, Lopez-Botet M. 2006. Human cytomegalovirus infection is associated with increased proportions of NK cells that express the CD94/NKG2C receptor in aviremic HIV-1-positive patients. J. Infect. Dis. 194:38-41.
13. Brunetta E, Fogli M, Varchetta S, Bozzo L, Hudspeth KL, Marcenaro E, Moretta A, Mavilio D. 2010. Chronic HIV-1 viremia reverses NKG2A/ NKG2C ratio on natural killer cells in patients with human cytomegalovirus co-infection. AIDS 24:27-34.
14. Bjorkstrom NK, Lindgren T, Stoltz M, Fauriat C, Braun M, Evander M, Michaelsson J, Malmberg KJ, Klingstrom J, Ahlm C, Ljunggren HG. 2011. Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J. Exp. Med. 208:13-21.
15. Beziat V, Dalgard O, Asselah T, Halfon P, Bedossa P, Boudifa A, Hervier B, Theodorou I, Martinot M, Debre P, Bjorkstrom NK, Malmberg KJ, Marcellin P, Vieillard V. 2012. CMV drives clonal expansion of NKG2C+ NK cells expressing self-specific KIRs in chronic hepatitis patients. Eur. J. Immunol. 42:447-457.
16. Petersen L, Roug AS, Skovbo A, Thysen AH, Eskelund CW, Hokland ME. 2009. The CD94/NKG2C-expressing NK cell subset is augmented in chronic lymphocytic leukemia patients with positive human cytomegalovirus serostatus. Viral Immunol. 22:333-337.
17. Foley B, Cooley S, Verneris MR, Pitt M, Curtsinger J, Luo X, LopezVerges S, Lanier LL, Weisdorf D, Miller JS. 2012. Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood 119: 2665-2674.
18. Della Chiesa M, Falco M, Podesta M, Locatelli F, Moretta L, Frassoni F, Moretta A. 2012. Phenotypic and functional heterogeneity of human NK cells developing after umbilical cord blood transplantation: a role for human cytomegalovirus? Blood 119:399-410.
19. dim NK-cell differentiation uncoupled from NK-cell education. Blood 116:3853-3864.
20. dimCD16+ NK-cell subset. Blood 116:3865-3874.
21. Sinclair J, Sissons P. 2006. Latency and reactivation of human cytomegalovirus. J. Gen. Virol. 87:1763-1779.
22. Bayer C, Varani S, Wang L, Walther P, Zhou S, Straschewski S, Bachem M, Soderberg-Naucler C, Mertens T, Frascaroli G. 2013. Human cytomegalovirus infection of m1 and m2 macrophages triggers inflammation and autologous T-cell proliferation. J. Virol. 87:67-79.
23. Romo N, Magri G, Muntasell A, Heredia G, Baia D, Angulo A, Guma M, Lopez-Botet M. 2011. Natural killer cell-mediated response to human cytomegalovirus-infected macrophages is modulated by their functional polarization. J. Leukoc. Biol. 90:717-726.
24. Riegler S, Hebart H, Einsele H, Brossart P, Jahn G, Sinzger C. 2000. Monocyte-derived dendritic cells are permissive to the complete replicative cycle of human cytomegalovirus. J. Gen. Virol. 81:393-399.
25. Sinzger C, Eberhardt K, Cavignac Y, Weinstock C, Kessler T, Jahn G, Davignon JL. 2006. Macrophage cultures are susceptible to lytic productive infection by endothelial-cell-propagated human cytomegalovirus strains and present viral IE1 protein to CD4+ T cells despite late downregulation of MHC class II molecules. J. Gen. Virol. 87:1853-1862.
26. Sinzger C, Hahn G, Digel M, Katona R, Sampaio KL, Messerle M, Hengel H, Koszinowski U, Brune W, Adler B. 2008. Cloning and sequencing of a highly productive, endotheliotropic virus strain derived from human cytomegalovirus TB40/E. J. Gen. Virol. 89:359-368.
27. Couzi L, Pitard V, Sicard X, Garrigue I, Hawchar O, Merville P, Moreau JF, Dechanet-Merville J. 2012. Antibody-dependent anticytomegalovirus activity of human gammadelta T cells expressing CD16 (FcgammaRIIIa). Blood 119:1418-1427.
28. Duske H, Sputtek A, Binder T, Kroger N, Schrepfer S, Eiermann T. 2011. Assessment of physiologic natural killer cell cytotoxicity in vitro. Hum. Immunol. 72:1007-1012.
29. Goodridge JP, Witt CS, Christiansen FT, Warren HS. 2003. KIR2DL4 (CD158d) genotype influences expression and function in NK cells. J. Immunol. 171:1768-1774.
30. Eller MA, Currier JR. 2012. OMIP-007: phenotypic analysis of human natural killer cells. Cytometry A 81:447-449.
31. Bowles JA, Weiner GJ. 2005. CD16 polymorphisms and NK activation induced by monoclonal antibody-coated target cells. J. Immunol. Methods 304:88-99.
32. Chapman TL, Heikeman AP, Bjorkman PJ. 1999. The inhibitory receptor LIR-1 uses a common binding interaction to recognize class I MHC molecules and the viral homolog UL18. Immunity 11:603-613.
33. Braud VM, Allan DS, O'Callaghan CA, Soderstrom K, D'Andrea A, Ogg GS, Lazetic S, Young NT, Bell JI, Phillips JH, Lanier LL, McMichael AJ. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:795-799.
34. Magri G, Muntasell A, Romo N, Saez-Borderias A, Pende D, Geraghty DE, Hengel H, Angulo A, Moretta A, Lopez-Botet M. 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.
35. Munoz-Cobo B, Solano C, Benet I, Costa E, Remigia MJ, de la Camara R, Nieto J, Lopez J, Amat P, Garcia-Noblejas A, Bravo D, Clari MA, Navarro D. 2012. Functional profile of cytomegalovirus (CMV)-specific CD8(+) T cells and kinetics of NKG2C(+) NK Cells associated with the resolution of CMV DNAemia in allogeneic stem cell transplant recipients. J. Med. Virol. 84:259-267.
36. Fouts AE, Chan P, Stephan JP, Vandlen R, Feierbach B. 2012. Antibodies against the gH/gL/UL128/UL130/UL131 complex comprise the majority of the anti-cytomegalovirus (anti-CMV) neutralizing antibody response in CMV hyperimmune globulin. J. Virol. 86:7444-7447.
37. Grzywacz B, Kataria N, Verneris MR. 2007. CD56(dim)CD16(+)NK cells downregulate CD16 following target cell induced activation of matrix metalloproteinases. Leukemia 21:356-359, author reply, 359.
38. Liu Q, Sun Y, Rihn S, Nolting A, Tsoukas PN, Jost S, Cohen K, Walker B, Alter G. 2009. Matrix metalloprotease inhibitors restore impaired NK cell-mediated antibody-dependent cellular cytotoxicity in human immunodeficiency virus type 1 infection. J. Virol. 83:8705-8712.
39. D'Orazio JA, Burke GW, Stein-Streilein J. 1995. Staphylococcal enterotoxin B activates purified NK cells to secrete IFN-gamma but requires T lymphocytes to augment NK cytotoxicity. J. Immunol. 154:1014-1023.
40. Parsons MS, Zipperlen K, Gallant M, Grant M. 2010. Killer cell immunoglobulin-like receptor 3DL1 licenses CD16-mediated effector functions of natural killer cells. J. Leukoc. Biol. 88:905-912.
41. Beziat V, Liu LL, Malmberg JA, Ivarsson MA, Sohlberg E, Bjorklund AT, Retiere C, Sverremark-Ekstrom E, Traherne J, Ljungman P, Schaffer M, Price DA, Trowsdale J, Michaelsson J, Ljunggren HG, Malmberg KJ. 2013. NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood 121:2678-2688.
42. Noyola DE, Fortuny C, Muntasell A, Noguera-Julian A, MunozAlmagro C, Alarcon A, Juncosa T, Moraru M, Vilches C, Lopez-Botet M. 2012. Influence of congenital human cytomegalovirus infection and the NKG2C genotype on NK-cell subset distribution in children. Eur. J. Immunol. 42:3256-3266.
43. Koch J, Steinle A, Watzl C, Mandelboim O. 2013. Activating natural cytotoxicity receptors of natural killer cells in cancer and infection. Trends Immunol. 34:182-191.
44. Lanier LL. 2008. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 9:495-502.
45. Lanier LL. 2005. NK cell recognition. Annu. Rev. Immunol. 23:225-274.
46. Zhang T, Scott JM, Hwang I, Kim S. 2013. Cutting edge: antibodydependent memory-like NK cells distinguished by FcRgamma deficiency. J. Immunol. 190:1402-1406.
47. Lanier LL. 2003. Natural killer cell receptor signaling. Curr. Opin. Immunol. 15:308-314.
48. Kaiser BK, Pizarro JC, Kerns J, Strong RK. 2008. Structural basis for NKG2A/CD94 recognition of HLA-E. Proc. Natl. Acad. Sci. U. S. A. 105: 6696-6701.
49. Tomasec P, Braud VM, Rickards C, Powell MB, McSharry BP, Gadola S, Cerundolo V, Borysiewicz LK, McMichael AJ, Wilkinson GW. 2000. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287:1031.
50. Huang Y, Lei Y, Zhang H, Zhang M, Dayton A. 2011. Interleukin-12 treatment down-regulates STAT4 and induces apoptosis with increasing ROS production in human natural killer cells. J. Leukoc. Biol. 90:87-97.