Whatever turns you on: Accessory-cell-dependent activation of NK cells by pathogens

Nature Reviews Immunology

Volumn 7, Issue 4, 2007, Pages 279-291

  Newman, Kirsty C ^a   Riley, Eleanor M ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CD11B ANTIGEN; CD14 ANTIGEN; CD16 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CD97 ANTIGEN; CYTOKINE; DECAY ACCELERATING FACTOR; FAS ANTIGEN; GAMMA INTERFERON; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; GLYCOPROTEIN P 15095; INTERFERON RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 18; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PERFORIN; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 10; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; UNINDEXED DRUG;

ACCESSORY CELL; BACTERIAL INFECTION; CELL MEMBRANE PERMEABILITY; CYTOKINE PRODUCTION; CYTOTOXICITY; DENDRITIC CELL; EXPERIMENTAL MOUSE; HELMINTH; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 2; HUMAN; IMMUNE RESPONSE; INFLUENZA VIRUS; INFLUENZA VIRUS A; INNATE IMMUNITY; LACTOBACILLUS CASEI; LEISHMANIA; LEISHMANIA MAJOR; LISTERIA MONOCYTOGENES; LYMPHOCYTE ACTIVATION; MACROPHAGE; MONOCYTE; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NATURAL KILLER CELL; NECATOR AMERICANUS; NONHUMAN; PATHOGENESIS; PLASMODIUM CHABAUDI; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; REVIEW; SALMONELLA ENTERITIDIS; SENDAI VIRUS; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; TOXOPLASMA GONDII; TRYPANOSOMA CRUZI; UPREGULATION; VIRUS INFECTION;

ANIMALS; ANTIGEN-PRESENTING CELLS; BACTERIAL INFECTIONS; CELL COMMUNICATION; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; RECEPTOR CROSS-TALK; SIGNAL TRANSDUCTION; VIRUS DISEASES;

EID: 33947590063     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri2057     Document Type: Review

References (131)

1. Herberman, R. B. et al. Natural killer cells: characteristics and regulation of activity. Immunol. Rev. 44, 43-70 (1979).
2. Ljunggren, H. & Karre, K. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol. Today 11, 237-244 (1990).
3. Smyth, M. J. et al. Activation of NK cell cytotoxicity. Mol. Immunol. 42, 501-510 (2005).
4. Lodoen, M. B. & Lanier, L. L. Natural killer cells as an initial defense against pathogens. Curr. Opin. Immunol. 18, 391-398 (2006).
5. Mandelboim, O. et al. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409, 1055-1060 (2001).
6. Smith, H. R. et al. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl Acad. Sci. USA 99, 8826-8831 (2002).
7. Arase, H., Mocarski, E. S., Campbell, A. E., Hill, A. B. & Lanier, L. L. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296, 1323-1326 (2002).
8. Piguet, V. Receptor modulation in viral replication: HIV, HSV, HHV-8 and HPV: same goal, different techniques to interfere with MHC-I antigen presentation. Curr. Top. Microbiol. Immunol. 285, 199-217 (2005).
9. Haller, D., Serrant, P., Granato, D., Schiffrin, E. J. & Blum, S. Activation of human NK cells by staphylococci and lactobacilli requires cell contact-dependent costimulation by autologous monocytes. Clin. Diagn. Lab. Immunol. 9, 649-657 (2002).
10. Wherry, J. C., Schreiber, R. D. & Unanue, E. R. Regulation of γ interferon production by natural killer cells in scid mice: roles of tumor necrosis factor and bacterial stimuli. Infect. Immun. 59, 1709-1715. (1991).
11. Newman, K. C., Korbel, D. S., Hafalla, J. C. & Riley, E. M. Cross-talk with myeloid accessory cells regulates human natural killer cell interferon-γ responses to malaria. PLoS Pathog. 2, e118 (2006). The authors demonstrate that the magnitude of the NK-cell response to P. falciparum is regulated by contact-dependent and soluble signals from monocytes and myeloid DCs.
12. Olsen, I. et al. Bovine NK cells can produce γ interferon in response to the secreted mycobacterial proteins ESAT-6 and MPP14 but not in response to MPB70. Infect. Immun. 73, 5628-5635 (2005).
13. Orange, J. S. & Biron, C. A. An absolute and restricted requirement for IL-12 in natural killer cell IFN-γ production and antiviral defense. Studies of natural killer and T cell responses in contrasting viral infections. J. Immunol. 156, 1138-1142 (1996).
14. Monteiro, J. M., Harvey, C. & Trinchieri, G. Role of interleukin-12 in primary influenza virus infection. J. Virol. 72, 4825-4831 (1998).
15. Scharton-Kersten, T., Afonso, L. C., Wysocka, M., Trinchieri, G. & Scott, P. IL-12 is required for natural killer cell activation and subsequent T helper 1 cell development in experimental leishmaniasis. J. Immunol. 154, 5320-5330 (1995).
16. Heinzel, F. P., Rerko, R. M., Ling, P., Hakimi, J. & Schoenhaut, D. S. Interleukin 12 is produced in vivo during endotoxemia and stimulates synthesis of γ interferon. Infect. Immun. 62, 4244-4249 (1994).
17. Nomura, T. et al. Essential role of interleukin-12 (IL-12) and IL-18 for γ interferon production induced by listeriolysin O in mouse spleen cells. Infect. Immun. 70, 1049-1055 (2002).
18. Nguyen, K. B. et al. Coordinated and distinct roles for IFN-αβ, IL-12, and IL-15 regulation of NK cell responses to viral infection. J. Immunol. 169, 4279-4287 (2002).
19. Orange, J. S. & Biron, C. A. Characterization of early IL-12, IFN-αβ, and TNF effects on antiviral state and NK cell responses during murine cytomegalovirus infection. J. Immunol. 156, 4746-4756 (1996).
20. - bone marrow cells. J. Immunol. 171, 683-690 (2003).
21. Hunter, C. A., Gabriel, K. E., Radzanowski, T., Neyer, L. E. & Remington, J. S. Type I interferons enhance production of IFN-γ by NK cells. Immunol. Lett. 59, 1-5 (1997).
22. Carson, W. E. et al. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J. Exp. Med. 180, 1395-1403 (1994).
23. Malmgaard, L. & Paludan, S. R. Interferon (IFN)-α/β, interleukin (IL)-12 and IL-18 coordinately induce production of IFN-γ during infection with herpes simplex virus type 2. J. Gen. Virol. 84, 2497-2500 (2003).
24. Gorak, P. M., Engwerda, C. R. & Kaye, P. M. Dendritic cells, but not macrophages, produce IL-12 immediately following Leishmania donovani infection. Eur. J. Immunol. 28, 687-695 (1998).
25. Dalod, M. et al. Dendritic cell responses to early murine cytomegalovirus infection: subset functional specialization and differential regulation by interferon α/β. J. Exp. Med. 197, 885-898 (2003).
26. Hanabuchi, S. et al. Human plasmacytoid predendritic cells activate NK cells through glucocorticoid-induced tumor necrosis factor receptor-ligand (GITRL). Blood 107, 3617-3623 (2006).
27. Atochina, O. & Harn, D. LNFPIII/LeX-stimulated macrophages activate natural killer cells via CD40-CD40L interaction. Clin. Diagn. Lab. Immunol. 12, 1041-1049 (2005).
28. Kamath, A. T., Sheasby, C. E. & Tough, D. F. Dendritic cells and NK cells stimulate bystander T cell activation in response to TLR agonists through secretion of IFN-αβ and IFN-γ. J. Immunol. 174, 767-776 (2005).
29. Siren, J. et al. Cytokine and contact-dependent activation of natural killer cells by influenza A or Sendai virus-infected macrophages. J. Gen. Virol. 85, 2357-2364 (2004).
30. Jinushi, M. et al. Critical role of MHC class I-related chain A and B expression on IFN-α-stimulated dendritic cells in NK cell activation: impairment in chronic hepatitis C virus infection. J. Immunol. 170, 1249-1256 (2003).
31. Cardillo, F., Voltarelli, J. C., Reed, S. G. & Silva, J. S. Regulation of Trypanosoma cruzi infection in mice by γ interferon and interleukin 10: role of NK cells. Infect. Immun. 64, 128-134 (1996).
32. Tripp, C. S., Wolf, S. F. & Unanue, E. R. Interleukin 12 and tumor necrosis factor α are costimulators of interferon γ production by natural killer cells in severe combined immunodeficiency mice with listeriosis, and interleukin 10 is a physiologic antagonist. Proc. Natl Acad. Sci. USA 90, 3725-3729. (1993).
33. Scott, M. J. et al. CD40-CD154 interactions between macrophages and natural killer cells during sepsis are critical for macrophage activation and are not interferon γ dependent. Clin. Exp. Immunol. 137, 469-477 (2004).
34. Gazzinelli, R. T., Hieny, S., Wynn, T. A., Wolf, S. & Sher, A. Interleukin 12 is required for the T-lymphocyte-independent induction of interferon γ by an intracellular parasite and induces resistance in T-cell-deficient hosts. Proc. Natl Acad. Sci. USA 90, 6115-6119 (1993).
35. He, X. S. et al. T cell-dependent production of IFN-γ by NK cells in response to influenza A virus. J. Clin. Invest. 114, 1812-1819 (2004).
36. Artavanis-Tsakonas, K. et al. Activation of a subset of human NK cells upon contact with Plasmodium falciparum-infected erythrocytes. J. Immunol. 171, 5396-5405 (2003).
37. Gerosa, F. et al. The reciprocal interaction of NK cells with plasmacytoid or myeloid dendritic cells profoundly affects innate resistance functions. J. Immunol. 174, 727-734 (2005).
38. Liang, S., Wei, H., Sun, R. & Tian, Z. IFNα regulates NK cell cytotoxicity through STAT1 pathway. Cytokine 23, 190-199 (2003).
39. Marshall, J. D., Heeke, D. S., Abbate, C., Yee, P. & Van Nest, G. Induction of interferon-γ from natural killer cells by immunostimulatory CpG DNA is mediated through plasmacytoid-dendritic-cellproduced interferon-α and tumour necrosis factor-α. Immunology 117, 38-46 (2006).
40. Freudenberg, M. A. et al. Cutting edge: a murine, IL-12-independent pathway of IFN-γ induction by Gram-negative bacteria based on STAT4 activation by Type I IFN and IL-18 signaling. J. Immunol. 169, 1665-1668 (2002).
41. Zhou, J., Zhang, J., Lichtenheld, M. G. & Meadows, G. G. A role for NF-κB activation in perforin expression of NK cells upon IL-2 receptor signaling. J. Immunol. 169, 1319-1325 (2002).
42. Schluns, K. S., Stoklasek, T. & Lefrancois, L. The roles of interleukin-15 receptor α: trans-presentation, receptor component, or both? Int. J. Biochem. Cell Biol. 37, 1567-1571 (2005). This Review article provides a succinct description of the unusual mechanism of IL-15 trans-presentation, in which IL-15 is secreted and then re-bound to the source cell before being presented to the target cell.
43. Borg, C. et al. NK cell activation by dendritic cells (DCs) requires the formation of a synapse leading to IL-12 polarization in DCs. Blood 104, 3267-3275 (2004). The authors show that IL-12, one of the most potent NK-cell activating cytokines, is focally secreted by the accessory cell at the immune synapse and that optimal IL-12 signalling therefore requires direct contact between the accessory cell and the NK cell.
44. Hunter, C. A. et al. The role of the CD28/B7 interaction in the regulation of NK cell responses during infection with Toxoplasma gondii. J. Immunol. 158, 2285-2293 (1997).
45. Warschkau, H. & Kiderlen, A. F. A monoclonal antibody directed against the murine macrophage surface molecule F4/80 modulates natural immune response to Listeria monocytogenes. J. Immunol. 163, 3409-3416 (1999).
46. Capasso, M. et al. Costimulation via CD55 on human CD4+ T cells mediated by CD97. J. Immunol. 177, 1070-1077 (2006).
47. Hamerman, J. A., Ogasawara, K. & Lanier, L. L. Cutting edge: Toll-like receptor signaling in macrophages induces ligands for the NKG2D receptor. J. Immunol. 172, 2001-2005 (2004).
48. Andoniou, C. E. et al. Interaction between conventional dendritic cells and natural killer cells is integral to the activation of effective antiviral immunity. Nature Immunol. 6, 1011-1019 (2005). This study shows that myeloid DCs have a crucial role in NK-cell responses to MCMV infection; this is in addition to the previously documented role for pDCs.
49. Jinushi, M. 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. 171, 5423-5429 (2003).
50. Vankayalapati, R. et al. Role of NK cell-activating receptors and their ligands in the lysis of mononuclear phagocytes infected with an intracellular bacterium. J. Immunol. 175, 4611-4617 (2005).
51. Nedvetzki, S. et al. Reciprocal regulation of natural killer cells and macrophages associated with distinct immune synapses. Blood 11 January 2007 (doi:10.1182/blood-2006-10-052977).
52. Welte, S., Kuttruff, S., Waldhauer, I. & Steinle, A. Mutual activation of natural killer cells and monocytes mediated by NKp80-AICL interaction. Nature Immunol. 7, 1334-1342 (2006). The authors report an addition to the growing list of molecular interactions that can contribute to accessory-cell activation of NK cells and identify AICL as a ligand for the NK-cell receptor NKp80.
53. Badgwell, B., Parihar, R., Magro, C., Dierksheide, J., Russo, T. & Carson, W. E. 3rd. Natural killer cells contribute to the lethality of a murine model of Escherichia coli infection. Surgery 132, 205-212 (2002).
54. Li, M. O., Wan, Y. Y., Sanjabi, S., Robertson, A. K. & Flavell, R. A. Transforming growth factor-β regulation of immune responses. Annu. Rev. Immunol. 24, 99-146 (2006).
55. Neyer, L. E. et al. Role of interleukin-10 in regulation of T-cell-dependent and T-cell-independent mechanisms of resistance to Toxoplasma gondii. Infect. Immun. 65, 1675-1682 (1997).
56. Hunter, C. A., Bermudez, L., Beernink, H., Waegell, W. & Remington, J. S. Transforming growth factor-β inhibits interleukin-12-induced production of interferon-γ by natural killer cells: a role for transforming growth factor-β in the regulation of T cell-independent resistance to Toxoplasma gondii. Eur. J. Immunol. 25, 994-1000 (1995).
57. Schierloh, P. et al. NK cell activity in tuberculosis is associated with impaired CD11a and ICAM-1 expression: a regulatory role of monocytes in NK activation. Immunology 116, 541-552 (2005).
58. Laouar, Y., Sutterwala, F. S., Gorelik, L. & Flavell, R. A. Transforming growth factor-β controls T helper type 1 cell development through regulation of natural killer cell interferon-γ. Nature Immunol. 6, 600-607 (2005).
59. Nylen, S., Maasho, K., McMahon-Pratt, D. & Akuffo, H. Leishmanial amastigote antigen P-2 induces major histocompatibility complex class II-dependent natural killer-cell reactivity in cells from healthy donors. Scand. J. Immunol. 59, 294-304 (2004).
60. Andrews, D. M. et al. Cross-talk between dendritic cells and natural killer cells in viral infection. Mol. Immunol. 42, 547-555 (2005).
61. Delale, T. et al. MyD88-dependent and -independent murine cytomegalovirus sensing for IFN-α release and initiation of immune responses in vivo. J. Immunol. 175, 6723-6732 (2005).
62. Takeda, K., Kaisho, T. & Akira, S. Toll-like receptors. Annu. Rev. Immunol. 21, 335-376 (2003).
63. Krug, A. et al. TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 21, 107-119 (2004).
64. Krug, A. et al. Herpes simplex virus type 1 activates murine natural interferon-producing cells through tolllike receptor 9. Blood 103, 1433-1437 (2004).
65. Hochrein, H. et al. Herpes simplex virus type-1 induces IFN-α production via Toll-like receptor 9-dependent and -independent pathways. Proc. Natl Acad. Sci. USA 101, 11416-11421 (2004).
66. Malmgaard, L., Melchjorsen, J., Bowie, A. G., Mogensen, S. C. & Paludan, S. R. Viral activation of macrophages through TLR-dependent and- independent pathways. J. Immunol. 173, 6890-6898 (2004).
67. Pollara, G. et al. Herpes simplex virus type-1-induced activation of myeloid dendritic cells: the roles of virus cell interaction and paracrine type I IFN secretion. J. Immunol. 173, 4108-4119 (2004).
68. Kato, H. et al. Cell type-specific involvement of RIG-I in antiviral response. Immunity 23, 19-28 (2005). This study reveals that the mechanism by which an accessory cell detects infection by RNA viruses depends both on the cell type and the specific virus.
69. Yoneyama, M. et al. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175, 2851-2858 (2005).
70. Kato, H. et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441, 101-105 (2006).
71. Gitlin, L. et al. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl Acad. Sci. USA 103, 8459-8464 (2006).
72. Bowie, A. G. & Haga, I. R. The role of Toll-like receptors in the host response to viruses. Mol. Immunol. 42, 859-867 (2005).
73. Nishibori, T., Xiong, H., Kawamura, I., Arakawa, M. & Mitsuyama, M. Induction of cytokine gene expression by listeriolysin O and roles of macrophages and NK cells. Infect. Immun. 64, 3188-3195 (1996).
74. Datta, S. K. et al. Vaccination with irradiated Listeria induces protective T cell immunity. Immunity 25, 143-152 (2006).
75. Ito, Y. et al. Seeligeriolysin O, a protein toxin of Listeria seeligeri, stimulates macrophage cytokine production via Toll-like receptors in a profile different from that induced by other bacterial ligands. Int. Immunol. 17, 1597-1606 (2005).
76. Mariathasan, S. et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440, 228-232 (2006).
77. Yun, C. H. et al. Natural killer cells and Helicobacter pylori infection: bacterial antigens and interleukin-12 act synergistically to induce γ interferon production. Infect. Immun. 73, 1482-1490 (2005).
78. Winau, F. et al. Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity 24, 105-117 (2006).
79. Ferwerda, G. et al. NOD2 and toll-like receptors are nonredundant recognition systems of Mycobacterium tuberculosis. PLoS Pathog. 1, 279-285 (2005). In this study the authors show that intracellular NLRs and cell-surface TLRs can have a synergistic role in the induction of inflammatory cytokines by M. tuberculosis.
80. Denis, M., Keen, D. L., Parlane, N. A., Storset, A. K. & Buddle, B. M. Bovine natural killer cells restrict the replication of Mycobacterium bovis in bovine macrophages and enhance IL-12 release by infected macrophages. Tuberculosis 87, 53-62 (2006).
81. Brill, K. J. et al. Human natural killer cells mediate killing of intracellular Mycobacterium tuberculosis H37Rv via granule-independent mechanisms. Infect. Immun. 69, 1755-1765 (2001).
82. Junqueira-Kipnis, A. P. et al. NK cells respond to pulmonary infection with Mycobacterium tuberculosis, but play a minimal role in protection. J. Immunol. 171, 6039-6045 (2003).
83. Feng, C. G. et al. NK cell-derived IFN-γ differentially regulates innate resistance and neutrophil response in T cell-deficient hosts infected with Mycobacterium tuberculosis. J. Immunol. 177, 7086-7093 (2006).
84. Korbel, D., Finney, O. & Riley, E. Natural killer cells and innate immunity to protozoan pathogens. Int. J. Parasitol. 34, 1517-1528 (2004).
85. Stevenson, M. M., Tam, M. F., Wolf, S. F. & Sher, A. IL-12-induced protection against blood-stage Plasmodium chabaudi AS requires IFN-γ and TNF-α and occurs via a nitric oxide-dependent mechanism. J. Immunol. 155, 2545-2556 (1995).
86. Mohan, K., Moulin, P. & Stevenson, M. Natural killer cell cytokine production, not cytotoxicity, contributes to resistance against blood-stage Plasmodium chabaudi AS infection. J. Immunol. 159, 4990-4998 (1997).
87. Baratin, M. et al. Natural killer cell and macrophage cooperation in MyD88-dependent innate responses to Plasmodium falciparum. Proc. Natl Acad. Sci. USA 102, 14747-14752 (2005).
88. Krishnegowda, G. et al. Induction of proinflammatory responses in macrophages by the glycosylphosphatid ylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J. Biol. Chem. 280, 8606-8616 (2005).
89. Heinzel, F. P., Schoenhaut, D. S., Rerko, R. M., Rosser, L. E. & Gately, M. K. Recombinant interleukin 12 cures mice infected with Leishmania major. J. Exp. Med. 177, 1505-1509 (1993).
90. Wei, X. Q. et al. Altered immune responses and susceptibility to Leishmania major and Staphylococcus aureus infection in IL-18-deficient mice. J. Immunol. 163, 2821-2828 (1999).
91. Berberich, C. et al. Dendritic cell (DC)-based protection against an intracellular pathogen is dependent upon DC-derived IL-12 and can be induced by molecularly defined antigens. J. Immunol. 170, 3171-3179 (2003).
92. Bajenoff, M. et al. Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. J. Exp. Med. 203, 619-631 (2006). This fascinating study offers a glimpse of how NK cells and accessory cells interact in lymph nodes in vivo.
93. Becker, I. et al. Leishmania lipophosphoglycan (LPG) activates NK cells through toll-like receptor-2. Mol. Biochem. Parasitol. 130, 65-74 (2003).
94. Flandin, J. F., Chano, F. & Descoteaux, A. RNA interference reveals a role for TLR2 and TLR3 in the recognition of Leishmania donovani promastigotes by interferon-γ-primed macrophages. Eur. J. Immunol. 36, 411-420 (2006).
95. Nylen, S., Maasho, K., Soderstrom, K., Ilg, T. & Akuffo, H. Live Leishmania promastigotes can directly activate primary human natural killer cells to produce interferon-γ. Clin. Exp. Immunol. 131, 457-467 (2003).
96. Bafica, A. et al. Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection. J. Immunol. 177, 3515-3519 (2006). This study demonstrates that TLR9 can have a crucial role in the recognition of the DNA of a non-viral pathogen.
97. Ouaissi, A. et al. The Trypanosoma cruzi Tc52-released protein induces human dendritic cell maturation, signals via Toll-like receptor 2, and confers protection against lethal infection. J. Immunol. 168, 6366-6374 (2002).
98. De Arruda Hinds, L. B. et al. Modulation of B-lymphocyte and NK cell activities by glycoinositolph ospholipid purified from Trypanosoma cruzi. Infect. Immun. 67, 6177-6180 (1999).
99. Yarovinsky, F. et al. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308, 1626-1629 (2005). This study identifies a specific pathogen-derived ligand for the most recently described TLR, TLR11.
100. Aliberti, J. et al. Molecular mimicry of a CCR5 binding-domain in the microbial activation of dendritic cells. Nature Immunol. 4, 485-490 (2003).
101. Loh, J., Chu, D. T., O'Guin, A. K., Yokoyama, W. M. & Virgin, H. W. 4th. Natural killer cells utilize both perforin and γ interferon to regulate murine cytomegalovirus infection in the spleen and liver. J. Virol. 79, 661-667 (2005).
102. Biron, C. A., Nguyen, K. B. & Pien, G. C. Innate immune responses to LCMV infections: natural killer cells and cytokines. Curr. Top. Microbiol. Immunol. 263, 7-27 (2002).
103. Brodskyn, C. I., Barral, A., Boaventura, V., Carvalho, E. & Barral-Netto, M. Parasite-driven in vitro human lymphocyte cytotoxicity against autologous infected macrophages from mucosal leishmaniasis. J. Immunol. 159, 4467-4473 (1997).
104. Hatcher, F. M., Kuhn, R. E., Cerrone, M. C. & Burton, R. C. Increased natural killer cell activity in experimental American trypanosomiasis. J. Immunol. 127, 1126-1130 (1981).
105. Hughes, H. P., Kasper, L. H., Little, J. & Dubey, J. P. Absence of a role for natural killer cells in the control of acute infection by Toxoplasma gondii oocysts. Clin. Exp. Immunol. 72, 394-399 (1988).
106. Ojo-Amaize, E. et al. Positive correlation between degree of parasitemia, interferon titers, and natural killer cell activity in Plasmodium falciparum-infected children. J. Immunol. 127, 2296-2300 (1981).
107. Watford, W. T. et al. Signaling by IL-12 and IL-23 and the immunoregulatory roles of STAT4. Immunol. Rev. 202, 139-156 (2004).
108. O'Shea, J. J., Gadina, M. & Schreiber, R. D. Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell 109, S121-S131 (2002).
109. Korbel, D. S., Newman, K. C., Almeida, C. R., Davis, D. M. & Riley, E. M. Heterogeneous human NK cell responses to Plasmodium falciparum-infected erythrocytes. J. Immunol. 175, 7466-7473 (2005).
110. Vitale, M. et al. NK-dependent DC maturation is mediated by TNFα and IFNγ released upon engagement of the NKp30 triggering receptor. Blood 106, 566-571 (2005).
111. Piccioli, D., Sbrana, S., Melandri, E. & Valiante, N. M. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J. Exp. Med. 195, 335-341 (2002).
112. Gerosa, F. et al. Reciprocal activating interaction between natural killer cells and dendritic cells. J. Exp. Med. 195, 327-333 (2002). References 111 and 112 are two seminal studies that provide new insights into the bidirectional interactions that can occur between NK cells and DCs.
113. Ferlazzo, G. et al. Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J. Exp. Med. 195, 343-351 (2002).
114. Moretta, A. The dialogue between human natural killer cells and dendritic cells. Curr. Opin. Immunol. 17, 306-311 (2005).
115. Degli-Esposti, M. A. & Smyth, M. J. Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nature Rev. Immunol. 5, 112-124 (2005).
116. Zitvogel, L., Terme, M., Borg, C. & Trinchieri, G. Dendritic cell-NK cell cross-talk: regulation and physiopathology. Curr. Top. Microbiol. Immunol. 298, 157-174 (2006).
117. Hunter, C. A., Chizzonite, R. & Remington, J. S. IL-1β is required for IL-12 to induce production of IFN-γ by NK cells. A role for IL-1β in the T cell-independent mechanism of resistance against intracellular pathogens. J. Immunol. 155, 4347-4354 (1995).
118. D'Orazio, J. A., Burke, G. W. & Stein-Streilein, J. Staphylococcal enterotoxin B activates purified NK cells to secrete IFN-γ but requires T lymphocytes to augment NK cytotoxicity. J. Immunol. 154, 1014-1023 (1995).
119. Takeda, K. et al. Interleukin-12 is involved in the enhancement of human natural killer cell activity by Lactobacillus casei Shirota. Clin. Exp. Immunol. 146, 109-115 (2006).
120. Kawakami, K. et al. Interferon-γ production and host protective response against Mycobacterium tuberculosis in mice lacking both IL-12p40 and IL-18. Microbes Infect. 6, 339-349 (2004).
121. dim natural killer cell subsets respond differentially to direct stimulation with Mycobacterium bovis bacillus Calmette-Guerin. Scand. J. Immunol. 62, 498-506 (2005).
122. Hunter, C. A., Slifer, T. & Araujo, F. Interleukin-12-mediated resistance to Trypanosoma cruzi is dependent on tumor necrosis factor α and γ interferon. Infect. Immun. 64, 2381-2386 (1996).
123. + dendritic cells. Nature Immunol. 1, 83-87 (2000).
124. Reis e Sousa, C. et al. In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J. Exp. Med. 186, 1819-1829 (1997).
125. Gazzinelli, R. T. et al. Role of IL-12 in the initiation of cell mediated immunity by Toxoplasma gondii and its regulation by IL-10 and nitric oxide. J. Eukaryot. Microbiol. 41, 9S (1994).
126. Akuffo, H. et al. Natural killer cells in cross-regulation of IL-12 by IL-10 in Leishmania antigen-stimulated blood donor cells. Clin. Exp. Immunol. 117, 529-534 (1999).
127. Hsieh, G. C. et al. A secreted protein from the human hookworm necator americanus binds selectively to NK cells and induces IFN-γ production. J. Immunol. 173, 2699-2704 (2004).
128. Tabeta, K. et al. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl Acad. Sci. USA 101, 3516-3521 (2004).
129. Carayannopoulos, L. N. & Yokoyama, W. M. Recognition of infected cells by natural killer cells. Curr. Opin. Immunol. 16, 26-33 (2004).
130. Perry, A. K., Chen, G., Zheng, D., Tang, H. & Cheng, G. The host type I interferon response to viral and bacterial infections. Cell Res. 15, 407-422 (2005).
131. Tam, M. A. & Wick, M. J. Differential expansion, activation and effector functions of conventional and plasmacytoid dendritic cells in mouse tissues transiently infected with Listeria monocytogenes. Cell. Microbiol. 8, 1172-1187 (2006).