Dendritic cell and NK cell reciprocal cross talk promotes gamma interferon-dependent immunity to blood-stage Plasmodium chabaudi AS infection in mice

Infection and Immunity

Volumn 77, Issue 2, 2009, Pages 770-782

  Ing, Rebecca ^a   Stevenson, Mary M ^a,b  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD4 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 15; INTERLEUKIN 2; CYTOKINE;

ACCESSORY CELL; ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL INTERACTION; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; ERYTHROCYTE; IN VITRO STUDY; INNATE IMMUNITY; INTERFERON PRODUCTION; LYMPHOCYTOPOIESIS; MALARIA; MOUSE; NATURAL KILLER CELL; NONHUMAN; PARASITEMIA; PLASMODIUM CHABAUDI; PRIORITY JOURNAL; PROTOZOAL INFECTION; SPLEEN CELL; TH1 CELL; WILD TYPE; ANIMAL; CELL COMMUNICATION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PARASITOLOGY; PHYSIOLOGY;

ANIMALS; CELL COMMUNICATION; CYTOKINES; DENDRITIC CELLS; GENE EXPRESSION REGULATION; INTERFERON-GAMMA; KILLER CELLS, NATURAL; MALARIA; MICE; MICE, KNOCKOUT; PLASMODIUM CHABAUDI;

EID: 60549111028     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00994-08     Document Type: Article

References (46)

1. Ahvazi, B. C., P. Jacobs, and M. M. Stevenson. 1995. Role of macrophage-derived nitric oxide in suppression of lymphocyte proliferation during blood-stage malaria. J. Leukoc. Biol. 58:23-31.
2. Alii, R. S., and A. Khar. 2004. Interleukin-12 secreted by mature dendritic cells mediates activation of NK cell function. FEBS Lett. 559:71-76.
3. Artavanis-Tsakonas, K., K. Eleme, K. L. McQueen, N. W. Cheng, P. Parham, D. M. Davis, and E, M. Riley. 2003. Activation of a subset of human NK cells upon contact with Plasmodium falciparum-infected erythrocytes. J. Immunol. 171:5396-5405.
4. Artavanis-Tsakonas, K., and E. M. Riley. 2002. Innate immune response to malaria: rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes. J. Immunol. 169:2956-2963.
5. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18:767-811.
6. Baratin, M., S. Roetynck, C. Lepolard, C. Falk, S. Sawadogo, S. Uematsu, S. Akira, B. Ryffel, J. G. Tiraby, L. Alexopoulou, C. J. Kirs elm ing, J. Gysin, E. Vivier, and S. Ugolini, 2005. Natural killer cell and macrophage cooperation in MyD88-dependent innate responses to Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 102:14747-14752.
7. Caminschi, I., F. Ahmet, K. Heger, J. Brady, S. L. Nutt, D. VremeC., S. Pietersz, M. H. Lahoud, L. Schofield, D. S. Hansen, M. O'Keeffe, M. J. Smyth, S. Bedoui, G. M. Davey, J. A. Villadangos, W. R. Heath, and K. Shortman. 2007. Putative lKDCs are functionally and developmentally similar to natural killer cells, but not to dendritic cells. J. Exp. Med. 204:2579-2590.
8. Chan, C. W., E. Crafton, H. N. Fan, J. Flook, K. Yoshimura, M. Skarica, D. Brockstedt, T. W. Dubensky, M. F. Stins, L. L. Lanier, D. M. Pardoll, and F. Housseau. 2006. Interferon-producing killer dendritic cells provide a link between innate and adaptive immunity. Nat. Med. 12:207-213.
9. Chen, W., W. Jin, N. Hardegen, K. J. Lei, L. Li, N. Marines, G. McGrady, and S. M. Wahl. 2003. Conversion of peripheral CD4 + CD25-naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198:1875-1886.
10. bright NK cells are enriched at inflammatory sites and can engage with monocytes in a reciprocal program of activation. J. Immunol. 173:6418-6426.
11. Degli-Esposti, M. A., and M. J. Smyth. 2005. Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat. Rev. Immunol. 5:112-124.
12. de Souza, J. B., K. H. Williamson, T. Otani, and J. H. Playfair. 1997. Early gamma interferon responses in lethal and nonlethal murine blood-stage malaria. Infect. Immun. 65:1593-1598.
13. Feau, S., V. Facchinetti, F. Granucci, S. Citterio, D. Jarrossay, S. Seresini, M. P. Protti, A. Lanzavecchia, and P. Ricciardi-Castagnoli. 2005. Dendritic cell-derived IL-2 production is regulated by 1L-15 in humans and in mice. Blood 105:697-702.
14. Ferlazzo, G., M. Pack, D. Thomas, C. Paludan, D. Schmid, T. Strowig, G. Bougras, W. A. Muller, L. Moretta, and C. Munz. 2004. 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 101:16606-16611.
15. Fernandez, N. C., A. Lozier, C. Flament, P. Ricciardi-Castagnoli, D. Bellet, M. Suter, M. Perricaudet, T. Tursz, E. Maraskovsky, and L. Zitvogel. 1999. Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate anti-tumor immune responses in vivo. Nat. Med. 5:405-411.
16. Gerosa, F., B. Baldani-Guerra, C. Nisii, V. Marchesini, G. Carra, and G. Trinchieri. 2002. Reciprocal activating interaction between natural killer cells and dendritic cells. J. Exp. Med. 195:327-333.
17. Gerosa, F., A. Gobbi, P. Zorzi, S. Burg, F. Briere, G. Carra, and G. Trinchieri. 2005. The reciprocal interaction of NK cells with plasmacytoid or myeloid dendritic cells profoundly affects innate resistance functions. J. Immunol. 174:727-734.
18. Granucci, F., S. Feau, V. Angeli, F. Trottein, and P. Ricciardi-Castagnoli. 2003. Early IL-2 production by mouse dendritic cells is the result of micro-bial-induced priming. J. Immunol. 170:5075-5081.
19. Granucci, F., I. Zanoni, N. Pavelka, S. L. Van Dommelen, C. E. Andoniou, F. Belardelli, M. A. Degli-Esposti, and P. Ricciardi-Castagnoli. 2004. A contribution of mouse dendritic cell-derived IL-2 for NK cell activation. J. Exp. Med. 200:287-295.
20. Hisaeda, H., Y. Maekawa, D. Iwakawa, H. Okada, K. Himeno, K. Kishihara, S. Tsukumo, and K. Yasutomo. 2004. Escape of malaria parasites from host immunity requires CD4+ CD25+ regulatory T cells. Nat. Med. 10:29-30.
21. Hisaeda, H., K. Tetsutani, T. Imai, C. Moriya, L. Tu, S. Hamano, X. Duan, B. Chou, H. Ishida, A. Aramaki, J. Shen, K. J. Ishii, C. Coban, S. Akira, K. Takeda, K. Yasutomo, M. Torii, and K. Himeno. 2008. Malaria parasites require TLR9 signaling for immune evasion by activating regulatory T cells. J. Immunol. 180:2496-2503.
22. Hubert, P., N. Jacobs, J. H. Caberg, J. Boniver, and P. Delvenne. 2007. The cross-talk between dendritic and regulatory T cells: good or evil? J. Leukoc. Biol. 82:781-794.
23. Ing, R., P. Gros, and M. M. Stevenson. 2005. lnterleukin-15 enhances innate and adaptive immune responses to blood-stage malaria infection in mice. Infect. Immun. 73:3172-3177.
24. Ing, R., M. Segura, N. Thawani, M. Tarn, and M. M. Stevenson. 2006. Interaction of mouse dendritic cells and malaria-infected erythrocytes: uptake, maturation, and antigen presentation. J. Immunol. 176:441-50.
25. Leisewitz, A. L., K. A. Rockett, B. Gumede, M. Jones, B. Urban, and D. P. Kwiatkowski, 2004. Response of the splenic dendritic cell population to malaria infection. Infect. Immun. 72:4233-239.
26. Luyendyk, J., O. R. Olivas, L. A. Ginger, and A. C. Avery. 2002. Antigen-presenting cell function during Plasmodium yoelii infection. Infect. Immun. 70:2941-2949.
27. Mailliard, R. B., Y. I. Son, R. Redlinger, P. T. Coates, A. Giermasz, P. A. Morel, W. J. Storkus, and P. Kalinski. 2003. Dendritic cells mediate NK cell help for Thl and CTL responses: two-signal requirement for the induction of NK cell helper function. J. Immunol. 171:2366-2373.
28. Mohan, K., P. Moulin, and M. M. Stevenson. 1997. Natural killer cell cytokine production, not cytotoxicity, contributes to resistance against blood-stage Plasmodium chabaudi AS infection. J. Immunol. 159:4990-4998.
29. Newman, K. C., D. S. Korbel, J, C. Hafalla, and E. M. Riley. 2006. Cross-talk with myeloid accessory cells regulates human natural killer cell interferon-gamma responses to malaria. PLoS Pathog. 2:ell8.
30. Perry, J. A., A. Rush, R. J. Wilson, C. S. Olver, and A. C. Avery. 2004. Dendritic cells from malaria-infected mice are fully functional APC. J. Immunol. 172:475-482.
31. Piccioli, D., S. Sbrana, E. Melandri, and N. M. Valiante. 2002. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J. Exp. Med. 195:335-341.
32. Sam, H., and M. M. Stevenson. 1999. Early IL-12 p70, but not p40, production by splenic macrophages correlates with host resistance to blood-stage Plasmodium chabaudi AS malaria. Clin. Exp. Immunol. 117:343-349.
33. Scorza, T., S. Magez, L. Brys, and P. De Baeselier. 1999. Hemozoin is a key factor in the induction of malaria-associated immunosuppression. Parasite Immunol. 21:545-554.
34. Seixas, E., C. Cross, S. Quin, and J. Langhorne. 2001. Direct activation of dendritic cells by the malaria parasite, Plasmodium chabaudi chabaudi. Eur. J. Immunol. 31:2970-2978.
35. Setoguchi, R., S. Hori, T. Takahashi, and S. Sakaguchi. 2005. Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by 1L-2 neutralization. J. Exp. Med. 201:723-735.
36. Sponaas, A. M., E. T. Cadman, C. Voisine, V. Harrison, A. Boonstra, A. O'Garra, and J. Langhorne. 2006. Malaria infection changes the ability of splenic dendritic cell populations to stimulate antigen-specific T cells. J. Exp. Med. 203:1427-1433.
37. Stevenson, M. M., and E. M. Riley. 2004. Innate immunity to malaria. Nat. Rev. Immunol. 4:169-180.
38. Stevenson, M. M., M. F. Tarn, S. F. Wolf, and A. Sher. 1995. lL-12-induced protection against blood-stage Plasmodium chabaudi AS requires IFN-gamma and TNF-alpha and occurs via a nitric oxide-dependent mechanism. J. Immunol. 155:2545-2556.
39. Su, Z., and M. M. Stevenson. 2000. Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect. Immun. 68:4399-4406.
40. Su, Z., and M. M. Stevenson. 2002. IL-12 is required for antibody-mediated protective immunity against blood-stage Plasmodium chabaudi AS malaria infection in mice. J. Immunol. 168:1348-1355.
41. Taieb, J., N. Chaput, C. Menard, L. Apetoh, E. Ullrich, M. Bonmort, M. Pequignot, N. Casares, M. Terme, C. Flament, P. Opolon, Y. Lecluse, D. Metivier, E. Tomasello, E. Vivier, F. Ghiringhelli, F. Martin, D. Klatzmann, T. Poynard, T. Tursz, G. Raposo, H. Yagita, B. Ryffel, G. Kroemer, and L. Zitvogel. 2006. A novel dendritic cell subset involved in tumor immunosur-veillance. Nat. Med. 12:214-219.
42. Thornton, A. M., E. E. Donovan, C. A. Piccirillo, and E. M. Shevach. 2004. Cutting edge: IL-2 is critically required for the in vitro activation of CD4+CD25+ T cell suppressor function. J. Immunol. 172:6519-6523.
43. Walther, M., J. E. Tongren, L. Andrews, D. Korbel, E. King, H. Fletcher, R. F. Andersen, P. Bejon, F. Thompson, S. J. Dunachie, F. Edele, J. B. de Souza, R. E. Sinden, S. C. Gilbert, E. M. Riley, and A. V. Hill. 2005. Upregulation of TGF-beta, FOXP3, and CD4 + CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 23:287-296.
44. Wong, K. A., and A, Rodriguez. 2008. Plasmodium infection and endotoxic shock induce the expansion of regulatory dendritic cells. J. Immunol. 180: 716-726.
45. Wykes, M. N., X. Q. Liu, L. Beattie, D. I. StanisiC., K. J. Stacey, M. J. Smyth, R. Thomas, and M. F. Good. 2007. Plasmodium strain determines dendritic cell function essential for survival from malaria. PLoS Pathog. 3:e96.
46. Wykes, M. N., X. Q. Liu, S. Jiang, C. Hirunpetcharat, and M. F. Good. 2007. Systemic tumor necrosis factor generated during lethal Plasmodium infections impairs dendritic cell function. J. Immunol. 179:3982-3987.