Journal of Clinical Immunology

, Volume 29, Issue 3, pp 265–273 | Cite as

Dendritic Cell Interactions with NK Cells from Different Tissues

Article

Abstract

Introduction

In recent years, it has been realized that innate lymphocytes do not act in isolation but potentiate their efficiency by interacting with each other, resulting even in the regulation of adaptive immune response. One such cross-talk exists between dendritic cells (DCs) and natural killer (NK) cells. Here, we summarize recent studies on which subsets of these two innate immune components participate in this interaction, how it influences immune responses, and to which extent similar stimuli are integrated by DCs and NK cells during innate immunity.

Conclusion

We suggest that this cross-talk should be harnessed by activating both of these innate leucocyte populations with new adjuvant formulations for immunotherapies.

Keywords

Myeloid dendritic cells plasmacytoid dendritic cells natural killer cell subsets interleukin-12 interleukin-15 type I interferon DC/NK cell cross-talk 

References

  1. 1.
    Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392:245–52.PubMedGoogle Scholar
  2. 2.
    Trinchieri G. Biology of natural killer cells. Adv Immunol 1989;47:187–376.PubMedGoogle Scholar
  3. 3.
    Ljunggren HG, Karre K. Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J Exp Med 1985;162:1745–59.PubMedGoogle Scholar
  4. 4.
    Yokoyama WM, Kim S, French AR. The dynamic life of natural killer cells. Annu Rev Immunol 2004;22:405–29.PubMedGoogle Scholar
  5. 5.
    Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, et al. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol 2001;19:197–223.PubMedGoogle Scholar
  6. 6.
    Lanier LL. NK cell recognition. Annu Rev Immunol 2005;23:225–74.PubMedGoogle Scholar
  7. 7.
    Long EO. Negative signaling by inhibitory receptors: the NK cell paradigm. Immunol Rev 2008;224:70–84.PubMedGoogle Scholar
  8. 8.
    Perussia B, Starr S, Abraham S, Fanning V, Trinchieri G. Human natural killer cells analyzed by B73.1, a monoclonal antibody blocking Fc receptor functions. I. Characterization of the lymphocyte subset reactive with B73.1. J Immunol 1983;130:2133–41.PubMedGoogle Scholar
  9. 9.
    Perussia B, Acuto O, Terhorst C, Faust J, Lazarus R, Fanning V, et al. Human natural killer cells analyzed by B73.1, a monoclonal antibody blocking Fc receptor functions. II. Studies of B73.1 antibody-antigen interaction on the lymphocyte membrane. J Immunol 1983;130:2142–8.PubMedGoogle Scholar
  10. 10.
    Moretta A, Sivori S, Vitale M, Pende D, Morelli L, Augugliaro R, et al. Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells. J Exp Med 1995;182:875–84.PubMedGoogle Scholar
  11. 11.
    Biassoni R, Cantoni C, Falco M, Verdiani S, Bottino C, Vitale M, et al. The human leukocyte antigen (HLA)-C-specific “activatory” or “inhibitory” natural killer cell receptors display highly homologous extracellular domains but differ in their transmembrane and intracytoplasmic portions. J Exp Med 1996;183:645–50.PubMedGoogle Scholar
  12. 12.
    Bottino C, Sivori S, Vitale M, Cantoni C, Falco M, Pende D, et al. A novel surface molecule homologous to the p58/p50 family of receptors is selectively expressed on a subset of human natural killer cells and induces both triggering of cell functions and proliferation. Eur J Immunol 1996;26:1816–24.PubMedGoogle Scholar
  13. 13.
    Sivori S, Pende D, Bottino C, Marcenaro E, Pessino A, Biassoni R, et al. NKp46 is the major triggering receptor involved in the natural cytotoxicity of fresh or cultured human NK cells. Correlation between surface density of NKp46 and natural cytotoxicity against autologous, allogeneic or xenogeneic target cells. Eur J Immunol 1999;29:1656–66.PubMedGoogle Scholar
  14. 14.
    Pogge von Strandmann E, Simhadri VR, von Tresckow B, Sasse S, Reiners KS, Hansen HP, et al. Human leukocyte antigen-B-associated transcript 3 is released from tumor cells and engages the NKp30 receptor on natural killer cells. Immunity 2007;27:965–74.PubMedGoogle Scholar
  15. 15.
    Mandelboim O, Lieberman N, Lev M, Paul L, Arnon TI, Bushkin Y, et al. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 2001;409:1055–60.PubMedGoogle Scholar
  16. 16.
    Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999;285:727–9.PubMedGoogle Scholar
  17. 17.
    Cosman D, Mullberg J, Sutherland CL, Chin W, Armitage R, Fanslow W, et al. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 2001;14:123–33.PubMedGoogle Scholar
  18. 18.
    Bottino C, Castriconi R, Pende D, Rivera P, Nanni M, Carnemolla B, et al. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J Exp Med 2003;198:557–67.PubMedGoogle Scholar
  19. 19.
    Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005;436:1186–90.PubMedGoogle Scholar
  20. 20.
    Campbell JJ, Qin S, Unutmaz D, Soler D, Murphy KE, Hodge MR, et al. Unique subpopulations of CD56+ NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire. J Immunol 2001;166:6477–82.PubMedGoogle Scholar
  21. 21.
    Jacobs R, Hintzen G, Kemper A, Beul K, Kempf S, Behrens G, et al. CD56bright cells differ in their KIR repertoire and cytotoxic features from CD56dim NK cells. Eur J Immunol 2001;31:3121–7.PubMedGoogle Scholar
  22. 22.
    Cooper MA, Fehniger TA, Turner SC, Chen KS, Ghaheri BA, Ghayur T, et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56bright subset. Blood 2001;97:3146–51.PubMedGoogle Scholar
  23. 23.
    Penna G, Sozzani S, Adorini L. Cutting edge: selective usage of chemokine receptors by plasmacytoid dendritic cells. J Immunol 2001;167:1862–6.PubMedGoogle Scholar
  24. 24.
    Papadopoulos EJ, Sassetti C, Saeki H, Yamada N, Kawamura T, Fitzhugh DJ, et al. Fractalkine, a CX3C chemokine, is expressed by dendritic cells and is up-regulated upon dendritic cell maturation. Eur J Immunol 1999;29:2551–9.PubMedGoogle Scholar
  25. 25.
    Megjugorac NJ, Young HA, Amrute SB, Olshalsky SL, Fitzgerald-Bocarsly P. Virally stimulated plasmacytoid dendritic cells produce chemokines and induce migration of T and NK cells. J Leukoc Biol 2004;75:504–14.PubMedGoogle Scholar
  26. 26.
    Bazan JF, Bacon KB, Hardiman G, Wang W, Soo K, Rossi D, et al. A new class of membrane-bound chemokine with a CX3C motif. Nature 1997;385:640–4.PubMedGoogle Scholar
  27. 27.
    Nishimura M, Umehara H, Nakayama T, Yoneda O, Hieshima K, Kakizaki M, et al. Dual functions of fractalkine/CX3C ligand 1 in trafficking of perforin +/granzyme B + cytotoxic effector lymphocytes that are defined by CX3CR1 expression. J Immunol 2002;168:6173–80.PubMedGoogle Scholar
  28. 28.
    Buentke E, Heffler LC, Wilson JL, Wallin RP, Lofman C, Chambers BJ, et al. Natural killer and dendritic cell contact in lesional atopic dermatitis skin–Malassezia-influenced cell interaction. J Invest Dermatol 2002;119:850–7.PubMedGoogle Scholar
  29. 29.
    Borg C, Terme M, Taieb J, Menard C, Flament C, Robert C, et al. Novel mode of action of c-kit tyrosine kinase inhibitors leading to NK cell-dependent antitumor effects. J Clin Invest 2004;114:379–88.PubMedGoogle Scholar
  30. 30.
    Dalbeth N, Gundle R, Davies RJ, Lee YC, McMichael AJ, Callan MF. CD56bright NK cells are enriched at inflammatory sites and can engage with monocytes in a reciprocal program of activation. J Immunol 2004;173:6418–26.PubMedGoogle Scholar
  31. 31.
    Carrega P, Morandi B, Costa R, Frumento G, Forte G, Altavilla G, et al. Natural killer cells infiltrating human nonsmall-cell lung cancer are enriched in CD56brightCD16- cells and display an impaired capability to kill tumor cells. Cancer 2008;112:863–75.PubMedGoogle Scholar
  32. 32.
    Schleypen JS, Baur N, Kammerer R, Nelson PJ, Rohrmann K, Grone EF, et al. Cytotoxic markers and frequency predict functional capacity of natural killer cells infiltrating renal cell carcinoma. Clin Cancer Res 2006;12:718–25.PubMedGoogle Scholar
  33. 33.
    Schleypen JS, Von Geldern M, Weiss EH, Kotzias N, Rohrmann K, Schendel DJ, et al. Renal cell carcinoma-infiltrating natural killer cells express differential repertoires of activating and inhibitory receptors and are inhibited by specific HLA class I allotypes. Int J Cancer 2003;106:905–12.PubMedGoogle Scholar
  34. 34.
    Buckley CD, Simmons DL. Sticky moments with sticky molecules. Immunol Today 2000;21:601–3.PubMedGoogle Scholar
  35. 35.
    Fehniger TA, Cooper MA, Nuovo GJ, Cella M, Facchetti F, Colonna M, et al. CD56bright natural killer cells are present in human lymph nodes and are activated by T cell derived IL-2: a potential new link between adaptive and innate immunity. Blood 2003;102:3052–57.Google Scholar
  36. 36.
    Ferlazzo G, Thomas D, Lin SL, Goodman K, Morandi B, Muller WA, et al. The abundant NK cells in human lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic. Journal of Immunology 2004;172:1455–62.Google Scholar
  37. 37.
    Westermann J, Pabst R. Distribution of lymphocyte subsets and natural killer cells in the human body. Clin Investig 1992;70:539–44.PubMedGoogle Scholar
  38. 38.
    Trepel F. Number and distribution of lymphocytes in man. A critical analysis. Klin Wochenschr 1974;52:511–5.PubMedGoogle Scholar
  39. 39.
    Cella M, Fuchs A, Vermi W, Facchetti F, Otero K, Lennerz JK, et al. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 2009;457:722–5.PubMedGoogle Scholar
  40. 40.
    Luci C, Reynders A, Ivanov II, Cognet C, Chiche L, Chasson L, et al. Influence of the transcription factor RORgammat on the development of NKp46+ cell populations in gut and skin. Nat Immunol 2009;10:75–82.PubMedGoogle Scholar
  41. 41.
    Sanos SL, Bui VL, Mortha A, Oberle K, Heners C, Johner C, et al. RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46 + cells. Nat Immunol 2009;10:83–91.PubMedGoogle Scholar
  42. 42.
    Satoh-Takayama N, Vosshenrich CA, Lesjean-Pottier S, Sawa S, Lochner M, Rattis F, et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 2008;29:958–70.PubMedGoogle Scholar
  43. 43.
    Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Stevens S, Flavell RA. Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 2008;29:947–57.PubMedGoogle Scholar
  44. 44.
    Morandi B, Bougras G, Muller WA, Ferlazzo G, Münz C. NK cells of human secondary lymphoid tissues enhance T cell polarization via IFN-gamma secretion. Eur J Immunol 2006;36:2394–400.PubMedGoogle Scholar
  45. 45.
    Strowig T, Brilot F, Arrey F, Bougras G, Thomas D, Muller WA, et al. Tonsilar natural killer cells restrict B cell transformation by the Epstein Barr virus via IFN-γ. PLoS Pathog 2008;4:e27.PubMedGoogle Scholar
  46. 46.
    Romagnani C, Juelke K, Falco M, Morandi B, D’Agostino A, Costa R, et al. CD56brightCD16- killer Ig-like receptor- NK cells display longer telomeres and acquire features of CD56dim NK cells upon activation. J Immunol 2007;178:4947–55.PubMedGoogle Scholar
  47. 47.
    Chan A, Hong DL, Atzberger A, Kollnberger S, Filer AD, Buckley CD, et al. CD56bright human NK cells differentiate into CD56dim cells: role of contact with peripheral fibroblasts. J Immunol 2007;179:89–94.PubMedGoogle Scholar
  48. 48.
    Huntington ND, Legrand N, Alves NL, Jaron B, Weijer K, Plet A, et al. IL-15 trans-presentation promotes human NK cell development and differentiation in vivo. J Exp Med 2009;206:25–34.PubMedGoogle Scholar
  49. 49.
    Freud AG, Becknell B, Roychowdhury S, Mao HC, Ferketich AK, Nuovo GJ, et al. A human CD34 + subset resides in lymph nodes and differentiates into CD56bright natural killer cells. Immunity 2005;22:295–304.PubMedGoogle Scholar
  50. 50.
    Vosshenrich CA, Garcia-Ojeda ME, Samson-Villeger SI, Pasqualetto V, Enault L, Richard-Le Goff O, et al. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat Immunol 2006;7:1217–24.PubMedGoogle Scholar
  51. 51.
    Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature 2009;457:557–61.PubMedGoogle Scholar
  52. 52.
    Lucas M, Schachterle W, Oberle K, Aichele P, Diefenbach A. Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 2007;26:503–17.PubMedGoogle Scholar
  53. 53.
    Kassim SH, Rajasagi NK, Zhao X, Chervenak R, Jennings SR. In vivo ablation of CD11c-positive dendritic cells increases susceptibility to herpes simplex virus type 1 infection and diminishes NK and T-cell responses. J Virol 2006;80:3985–93.PubMedGoogle Scholar
  54. 54.
    Andrews DM, Scalzo AA, Yokoyama WM, Smyth MJ, Degli-Esposti MA. Functional interactions between dendritic cells and NK cells during viral infection. Nat Immunol 2003;4:175–81.PubMedGoogle Scholar
  55. 55.
    Fernandez NC, Lozier A, Flament C, Ricciardi-Castagnoli P, Bellet D, Suter M, et al. Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate anti-tumor immune responses in vivo. Nat Med 1999;5:405–11.PubMedGoogle Scholar
  56. 56.
    Ferlazzo G, Tsang ML, Moretta L, Melioli G, Steinman RM, Münz C. Human dendritic cells activate resting NK cells and are recognized via the NKp30 receptor by activated NK cells. J Exp Med 2002;195:343–51.PubMedGoogle Scholar
  57. 57.
    Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, Trinchieri G. Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med 2002;195:327–33.PubMedGoogle Scholar
  58. 58.
    Piccioli D, Sbrana S, Melandri E, Valiante NM. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J Exp Med 2002;195:335–41.PubMedGoogle Scholar
  59. 59.
    Ferlazzo G, Thomas D, Pack M, Paludan C, Schmid D, Strowig T, et al. Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc Natl Acad Sci USA 2004;101:16606–11.PubMedGoogle Scholar
  60. 60.
    Vitale M, Della Chiesa M, Carlomagno S, Romagnani C, Thiel A, Moretta L, et al. The small subset of CD56brightCD16- natural killer cells is selectively responsible for both cell proliferation and interferon-gamma production upon interaction with dendritic cells. Eur J Immunol 2004;34:1715–22.PubMedGoogle Scholar
  61. 61.
    Bajenoff M, Breart B, Huang AY, Qi H, Cazareth J, Braud VM, et al. Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. J Exp Med 2006;203:619–31.PubMedGoogle Scholar
  62. 62.
    Garrod KR, Wei SH, Parker I, Cahalan MD. Natural killer cells actively patrol peripheral lymph nodes forming stable conjugates to eliminate MHC-mismatched targets. Proc Natl Acad Sci USA 2007;104:12081–6.PubMedGoogle Scholar
  63. 63.
    Gerosa F, Gobbi A, Zorzi P, Burg S, Briere F, Carra G, et al. The reciprocal interaction of NK cells with plasmacytoid or myeloid dendritic cells profoundly affects innate resistance functions. J Immunol 2005;174:727–34.PubMedGoogle Scholar
  64. 64.
    Gilliet M, Cao W, Liu YJ. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol 2008;8:594–606.PubMedGoogle Scholar
  65. 65.
    Nguyen KB, Salazar-Mather TP, Dalod MY, Van Deusen JB, Wei XQ, Liew FY, et al. Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J Immunol 2002;169:4279–87.PubMedGoogle Scholar
  66. 66.
    Dalod M, Salazar-Mather TP, Malmgaard L, Lewis C, Asselin-Paturel C, Briere F, et al. Interferon alpha/beta and interleukin 12 responses to viral infections: pathways regulating dendritic cell cytokine expression in vivo. J Exp Med 2002;195:517–28.PubMedGoogle Scholar
  67. 67.
    Andoniou CE, van Dommelen SL, Voigt V, Andrews DM, Brizard G, Asselin-Paturel C, et al. Interaction between conventional dendritic cells and natural killer cells is integral to the activation of effective antiviral immunity. Nat Immunol 2005;6:1011–19.PubMedGoogle Scholar
  68. 68.
    Orange JS, Biron CA. An absolute and restricted requirement for IL-12 in natural killer cell IFN-gamma production and antiviral defense. Studies of natural killer and T cell responses in contrasting viral infections. J Immunol 1996;156:1138–42.PubMedGoogle Scholar
  69. 69.
    Brilot F, Strowig T, Roberts SM, Arrey F, Münz C. NK cell survival mediated through the regulatory synapse with human dendritic cells requires IL-15Ralpha. J Clin Invest 2007;117:3316–29.PubMedGoogle Scholar
  70. 70.
    Huntington ND, Puthalakath H, Gunn P, Naik E, Michalak EM, Smyth MJ, et al. Interleukin 15-mediated survival of natural killer cells is determined by interactions among Bim, Noxa and Mcl-1. Nat Immunol 2007;8:856–63.PubMedGoogle Scholar
  71. 71.
    Jinushi M, Takehara T, Tatsumi T, Kanto T, Groh V, Spies T, et al. Autocrine/paracrine IL-15 that is required for type I IFN-mediated dendritic cell expression of MHC class I-related chain A and B is impaired in hepatitis C virus infection. J Immunol 2003;171:5423–9.PubMedGoogle Scholar
  72. 72.
    Kennedy MK, Glaccum M, Brown SN, Butz EA, Viney JL, Embers M, et al. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 2000;191:771–80.PubMedGoogle Scholar
  73. 73.
    Koka R, Burkett PR, Chien M, Chai S, Chan F, Lodolce JP, et al. Interleukin (IL)-15Ralpha-deficient natural killer cells survive in normal but not IL-15Ralpha-deficient mice. J Exp Med 2003;197:977–84.PubMedGoogle Scholar
  74. 74.
    Münz C, Dao T, Ferlazzo G, De Cos MA, Goodman K, Young JW. Mature myeloid dendritic cell subsets have distinct roles for activation and viability of circulating human natural killer cells. Blood 2005;105:266–73.PubMedGoogle Scholar
  75. 75.
    Laouar Y, Sutterwala FS, Gorelik L, Flavell RA. Transforming growth factor-beta controls T helper type 1 cell development through regulation of natural killer cell interferon-gamma. Nat Immunol 2005;6:600–7.PubMedGoogle Scholar
  76. 76.
    Ing R, Stevenson MM. Dendritic cell and NK cell reciprocal cross talk promotes gamma interferon-dependent immunity to blood-stage Plasmodium chabaudi AS infection in mice. Infect Immun 2009;77:770–82.PubMedGoogle Scholar
  77. 77.
    Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, et al. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 2004;5:1260–5.PubMedGoogle Scholar
  78. 78.
    Kang SJ, Liang HE, Reizis B, Locksley RM. Regulation of hierarchical clustering and activation of innate immune cells by dendritic cells. Immunity 2008;29:819–33.PubMedGoogle Scholar
  79. 79.
    Mocikat R, Braumuller H, Gumy A, Egeter O, Ziegler H, Reusch U, et al. Natural killer cells activated by MHC class Ilow targets prime dendritic cells to induce protective CD8 T cell responses. Immunity 2003;19:561–9.PubMedGoogle Scholar
  80. 80.
    Adam C, King S, Allgeier T, Braumuller H, Luking C, Mysliwietz J, et al. DC-NK cell cross talk as a novel CD4 + T-cell-independent pathway for antitumor CTL induction. Blood 2005;106:338–44.PubMedGoogle Scholar
  81. 81.
    Münz C, Steinman RM, Fujii S. Dendritic cell maturation by innate lymphocytes: coordinated stimulation of innate and adaptive immunity. J Exp Med 2005;202:203–7.PubMedGoogle Scholar
  82. 82.
    Spaggiari GM, Carosio R, Pende D, Marcenaro S, Rivera P, Zocchi MR, et al. NK cell-mediated lysis of autologous antigen-presenting cells is triggered by the engagement of the phosphatidylinositol 3-kinase upon ligation of the natural cytotoxicity receptors NKp30 and NKp46. Eur J Immunol 2001;31:1656–65.PubMedGoogle Scholar
  83. 83.
    Pende D, Castriconi R, Romagnani P, Spaggiari GM, Marcenaro S, Dondero A, et al. Expression of the DNAM-1 ligands, Nectin-2 (CD112) and poliovirus receptor (CD155), on dendritic cells: relevance for natural killer-dendritic cell interaction. Blood 2006;107:2030–6.PubMedGoogle Scholar
  84. 84.
    Della Chiesa M, Vitale M, Carlomagno S, Ferlazzo G, Moretta L, Moretta A. The natural killer cell-mediated killing of autologous dendritic cells is confined to a cell subset expressing CD94/NKG2A, but lacking inhibitory killer Ig-like receptors. Eur J Immunol 2003;33:1657–66.PubMedGoogle Scholar
  85. 85.
    Persson CM, Assarsson E, Vahlne G, Brodin P, Chambers BJ. Critical role of Qa1b in the protection of mature dendritic cells from NK cell-mediated killing. Scand J Immunol 2008;67:30–6.PubMedGoogle Scholar
  86. 86.
    Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002;295:2097–100.PubMedGoogle Scholar
  87. 87.
    Yu G, Xu X, Vu MD, Kilpatrick ED, Li XC. NK cells promote transplant tolerance by killing donor antigen-presenting cells. J Exp Med 2006;203:1851–8.PubMedGoogle Scholar
  88. 88.
    Laffont S, Seillet C, Ortaldo J, Coudert JD, Guery JC. Natural killer cells recruited into lymph nodes inhibit alloreactive T-cell activation through perforin-mediated killing of donor allogeneic dendritic cells. Blood 2008;112:661–71.PubMedGoogle Scholar
  89. 89.
    Hamerman JA, Jarjoura JR, Humphrey MB, Nakamura MC, Seaman WE, Lanier LL. Cutting edge: inhibition of TLR and FcR responses in macrophages by triggering receptor expressed on myeloid cells (TREM)-2 and DAP12. J Immunol 2006;177:2051–5.PubMedGoogle Scholar
  90. 90.
    Nedvetzki S, Sowinski S, Eagle RA, Harris J, Vely F, Pende D, et al. Reciprocal regulation of human natural killer cells and macrophages associated with distinct immune synapses. Blood 2007;109:3776–85.PubMedGoogle Scholar
  91. 91.
    Basu S, Eriksson M, Pioli PA, Conejo-Garcia J, Mselle TF, Yamamoto S, et al. Human uterine NK cells interact with uterine macrophages via NKG2D upon stimulation with PAMPs. Am J Reprod Immunol 2009;61:52–61.PubMedGoogle Scholar
  92. 92.
    Vankayalapati R, Garg A, Porgador A, Griffith DE, Klucar P, Safi H, et al. Role of NK cell-activating receptors and their ligands in the lysis of mononuclear phagocytes infected with an intracellular bacterium. J Immunol 2005;175:4611–7.PubMedGoogle Scholar
  93. 93.
    Siren J, Sareneva T, Pirhonen J, Strengell M, Veckman V, Julkunen I, et al. Cytokine and contact-dependent activation of natural killer cells by influenza A or Sendai virus-infected macrophages. J Gen Virol 2004;85:2357–64.PubMedGoogle Scholar
  94. 94.
    Saikali P, Antel JP, Newcombe J, Chen Z, Freedman M, Blain M, et al. NKG2D-mediated cytotoxicity toward oligodendrocytes suggests a mechanism for tissue injury in multiple sclerosis. J Neurosci 2007;27:1220–8.PubMedGoogle Scholar
  95. 95.
    Lünemann A, Lünemann JD, Roberts S, Messmer B, Barreira da Silva R, Raine CS, et al. Human NK cells kill resting but not activated microglia via NKG2D- and NKp46-mediated recognition. J Immunol 2008;181:6170–7.PubMedGoogle Scholar
  96. 96.
    Sivori S, Falco M, Della Chiesa M, Carlomagno S, Vitale M, Moretta L, et al. 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 USA 2004;101:10116–21.PubMedGoogle Scholar
  97. 97.
    Colonna M, Navarro F, Bellon T, Llano M, Garcia P, Samaridis J, et al. A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J Exp Med 1997;186:1809–18.PubMedGoogle Scholar
  98. 98.
    Allan DS, McMichael AJ, Braud VM. The ILT family of leukocyte receptors. Immunobiology 2000;202:34–41.PubMedGoogle Scholar
  99. 99.
    Fuchs A, Cella M, Kondo T, Colonna M. Paradoxic inhibition of human natural interferon-producing cells by the activating receptor NKp44. Blood 2005;106:2076–82.PubMedGoogle Scholar
  100. 100.
    Ju X, Zenke M, Hart DN, Clark GJ. CD300a/c regulate type I interferon and TNF-alpha secretion by human plasmacytoid dendritic cells stimulated with TLR7 and TLR9 ligands. Blood 2008;112:1184–94.PubMedGoogle Scholar
  101. 101.
    Palucka AK, Blanck JP, Bennett L, Pascual V, Banchereau J. Cross-regulation of TNF and IFN-alpha in autoimmune diseases. Proc Natl Acad Sci USA 2005;102:3372–7.PubMedGoogle Scholar
  102. 102.
    Cantoni C, Bottino C, Augugliaro R, Morelli L, Marcenaro E, Castriconi R, et al. Molecular and functional characterization of IRp60, a member of the immunoglobulin superfamily that functions as an inhibitory receptor in human NK cells. Eur J Immunol 1999;29:3148–59.PubMedGoogle Scholar
  103. 103.
    Terme M, Ullrich E, Delahaye NF, Chaput N, Zitvogel L. Natural killer cell-directed therapies: moving from unexpected results to successful strategies. Nat Immunol 2008;9:486–94.PubMedGoogle Scholar
  104. 104.
    Kalinski P, Nakamura Y, Watchmaker P, Giermasz A, Muthuswamy R, Mailliard RB. Helper roles of NK and CD8+ T cells in the induction of tumor immunity. Polarized dendritic cells as cancer vaccines. Immunol Res 2006;36:137–46.PubMedGoogle Scholar
  105. 105.
    Moretta A. Natural killer cells and dendritic cells: rendezvous in abused tissues. Nat Rev Immunol 2002;2:957–64.PubMedGoogle Scholar

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© 2Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Laboratory of Immunology and Biotherapy, Department of Human Pathology, School of MedicineUniversity of MessinaMessinaItaly
  2. 2.Viral Immunobiology, Institute of Experimental ImmunologyUniversity Hospital of ZürichZürichSwitzerland

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