NK cell-mediated killing of target cells triggers robust antigen-specific T cell-mediated and humoral responses

Blood

Volumn 113, Issue 26, 2009, Pages 6593-6602

  Krebs, Philippe ^a   Barnes, Michael J ^a   Lampe, Kristin ^b   Whitley, Karen ^a   Bahjat, Keith S ^c   Beutler, Bruce ^a   Janssen, Edith ^b   Hoebe, Kasper ^b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c PROVIDENCE PORTLAND MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; H 2KB PROTEIN, MOUSE; H-2KB PROTEIN, MOUSE; H2 ANTIGEN; IMMUNOGLOBULIN G; MYD88 PROTEIN, MOUSE; OVA 323 339; OVA 323-339; OVA 8; OVA-8; OVALBUMIN; PEPTIDE FRAGMENT; T LYMPHOCYTE RECEPTOR; TICAM 1 PROTEIN, MOUSE; TICAM-1 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL KILLING; CELLULAR IMMUNITY; CONTROLLED STUDY; HOST CELL; HUMORAL IMMUNITY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TUMOR CELL; ANIMAL; ANTIBODY SPECIFICITY; BIOSYNTHESIS; C3H MOUSE; C57BL MOUSE; CYTOTOXICITY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LISTERIA MONOCYTOGENES; LYMPHOCYTE ACTIVATION; MOUSE MUTANT; PHYSIOLOGY; VACCINATION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ANTIBODY SPECIFICITY; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; H-2 ANTIGENS; IMMUNOGLOBULIN G; IMMUNOLOGIC MEMORY; KILLER CELLS, NATURAL; LISTERIA MONOCYTOGENES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MYELOID DIFFERENTIATION FACTOR 88; OVALBUMIN; PEPTIDE FRAGMENTS; T-CELL ANTIGEN RECEPTOR SPECIFICITY; VACCINATION;

EID: 69249248229     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-01-201467     Document Type: Article

References (50)

1. Blankenstein T. The role of inflammation in tumour growth and tumour suppression. Novartis Found Symp. 2004;256:205-210.
2. Gallucci S, Lolkema M, Matzinger P. Natural adjuvants: endogenous activators of dendritic cells. Nat Med. 1999;5:1249-1255. (Pubitemid 29535601)
3. Degli-Esposti MA, Smyth MJ. Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat Rev Immunol. 2005;5:112-124.
4. Kelly JM, Darcy PK, Markby JL, et al. Induction of tumor-specific T cell memory by NK cell-mediated tumor rejection. Nat Immunol. 2002;3:83-90. (Pubitemid 34065622)
5. Levitsky HI, Lazenby A, Hayashi RJ, Pardoll DM. In vivo priming of two distinct antitumor effector populations: the role of MHC class I expression. J Exp Med. 1994;179:1215-1224.
6. Janssen E, Tabeta K, Barnes MJ, et al. Efficient T cell activation via a Toll-interleukin 1 receptorin-dependent pathway. Immunity. 2006;24:787-799. (Pubitemid 43867366)
7. Fossum S, Rolstad B. The roles of interdigitating cells and natural killer cells in the rapid rejection of allogeneic lymphocytes. Eur J Immunol. 1986; 16:440-450. (Pubitemid 16104529)
8. Raez LE, Cassileth PA, Schlesselman JJ, et al. Induction of CD8 T-cell-Ifn-gamma response and positive clinical outcome after immunization with gene-modified allogeneic tumor cells in advanced non-small-cell lung carcinoma. Cancer Gene Ther. 2003;10:850-858.
9. Schendel DJ, Frankenberger B, Jantzer P, et al. Expression of B7.1 (CD80) in a renal cell carcinoma line allows expansion of tumor-associated cytotoxic T lymphocytes in the presence of an alloresponse. Gene Ther. 2000;7:2007-2014. (Pubitemid 32036766)
10. Karre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature. 1986;319:675-678. (Pubitemid 16119452)
11. Ljunggren HG, Karre K. In search of the "missing self": MHC molecules and NK cell recognition. Immunol Today. 1990;11:237-244.
12. Long EO. Regulation of immune responses through inhibitory receptors. Annu Rev Immunol. 1999;17:875-904. (Pubitemid 29241142)
13. Tangri S, Mothe BR, Eisenbraun J, et al. Rationally engineered therapeutic proteins with reduced immunogenicity. J Immunol. 2005;174: 3187-3196. (Pubitemid 40354020)
14. Alignani D, Maletto B, Liscovsky M, et al. Orally administered OVA/CpG-ODN induces specific mucosal and systemic immune response in young and aged mice. J Leukocyte Biol. 2005;77: 898-905. (Pubitemid 40770841)
15. Brockstedt DG, Bahjat KS, Giedlin MA, et al. Killed but metabolically active microbes: a new vaccine paradigm for eliciting effector T-cell responses and protective immunity. Nat Med. 2005; 11:853-860.
16. Obeid M, Tesniere A, Ghiringhelli F, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med. 2007;13:54-61. (Pubitemid 46067386)
17. Lee RK, Spielman J, Zhao DY, Olsen KJ, Podack ER. Perforin, Fas ligand, and tumor necrosis factor are the major cytotoxic molecules used by lymphokine-activated killer cells. J Immunol. 1996;157:1919-1925. (Pubitemid 126449664)
18. Lodoen MB, Lanier LL. Natural killer cells as an initial defense against pathogens. Curr Opin Immunol. 2006;18:391-398. (Pubitemid 43947576)
19. Warren HS, Smyth MJ. NK cells and apoptosis. Immunol Cell Biol. 1999;77:64-75.
20. Bennett SR, Carbone FR, Karamalis F, Miller JF, Heath WR. Induction of a CD8+ cytotoxic T lymphocyte response by cross-priming requires cognate CD4+ T cell help. J Exp Med. 1997;186:65-70. (Pubitemid 27304848)
21. Ehst BD, Ingulli E, Jenkins MK. Development of a novel transgenic mouse for the study of interactions between CD4 and CD8 T cells during graft rejection. Am J Transplant. 2003;3:1355-1362. (Pubitemid 37288079)
22. Gerosa F, Baldani-Guerra B, Nisii C, et al. Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med. 2002;195: 327-333. (Pubitemid 34461490)
23. Chen CJ, Kono H, Golenbock D, et al. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat Med. 2007;13:851-856. (Pubitemid 47038190)
24. Miwa K, Asano M, Horai R, et al. Caspase 1-independent IL-1beta release and inflammation induced by the apoptosis inducer Fas ligand. Nat Med. 1998;4:1287-1292. (Pubitemid 28512110)
25. Chaix J, Tessmer MS, Hoebe K et al. Cutting edge: priming of NK cells by IL-18. J Immunol. 2008;181:1627-1631.
26. Apetoh L, Ghiringhelli F, Tesniere A et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med. 2007;13:1050-1059. (Pubitemid 47517504)
27. Williams MA, Holmes BJ, Sun JC, Bevan MJ. Developing and maintaining protective CD8+ memory T cells. Immunol Rev. 2006;211:146-153. (Pubitemid 43882968)
28. Harty JT, Tvinnereim AR, White DW. CD8+ T cell effector mechanisms in resistance to infection. Annu Rev Immunol. 2000;18:275-308. (Pubitemid 30365382)
29. Ladel CH, Flesch IE, Arnoldi J, Kaufmann SH. Studies with MHC-deficient knock-out mice reveal impact of both MHC I- and MHC II-dependent T cell responses on Listeria monocytogenes infection. J Immunol. 1994;153:3116-3122. (Pubitemid 24292536)
30. Fang M, Lanier LL, Sigal LJ. A role for NKG2D in NK cell-mediated resistance to poxvirus disease. PLoS Pathog. 2008;4:e30. (Pubitemid 351340717)
31. Robbins SH, Bessou G, Cornillon A, et al. Natural killer cells promote early CD8 T cell responses against cytomegalovirus. PLoS Pathog. 2007;3: e123. (Pubitemid 47359092)
32. 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;4:175-181. (Pubitemid 36193020)
33. Hahm B, Trifilo MJ, Zuniga EI, Oldstone MB. Viruses evade the immune system through type I interferon-mediated STAT2-dependent, but STAT1-independent, signaling. Immunity. 2005; 22:247-257. (Pubitemid 40255715)
34. Park DR, Thomsen AR, Frevert CW, et al. Fas (CD95) induces proinflammatory cytokine responses by human monocytes and monocytederived macrophages. J Immunol. 2003;170: 6209-6216.
35. Iyoda T, Shimoyama S, Liu K, et al. The CD8+ dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J Exp Med. 2002; 195:1289-1302. (Pubitemid 34564331)
36. Jusforgues-Saklani H, Uhl M, Blachere N, et al. Antigen persistence is required for dendritic cell licensing and CD8+ T cell cross-priming. J Immunol. 2008;181:3067-3076.
37. Hoebe K, Janssen EM, Kim SO, et al. Upregulation of costimulatory molecules induced by lipopolysaccharide and double-stranded RNA occurs by Trif-dependent and Trif-independent pathways. Nat Immunol. 2003;4:1223-1229. (Pubitemid 37540691)
38. Moretta A. The dialogue between human natural killer cells and dendritic cells. Curr Opin Immunol. 2005;17:306-311. (Pubitemid 40692667)
39. Moretta L, Ferlazzo G, Bottino C, et al. Effector and regulatory events during natural killer-dendritic cell interactions. Immunol Rev. 2006;214: 219-228. (Pubitemid 44707913)
40. Vitale M, Della CM, Carlomagno S. et al. NK-dependent DC maturation is mediated by TNFalpha and IFNgamma released upon engagement of the NKp30 triggering receptor. Blood. 2005;106: 566-571. (Pubitemid 40981252)
41. Walzer T, Dalod M, Vivier E, Zitvogel L. Natural killer cell-dendritic cell crosstalk in the initiation of immune responses. Expert Opin Biol Ther. 2005; 5(Suppl 1):S49-S59. (Pubitemid 41243345)
42. Zitvogel L, Terme M, Borg C, Trinchieri G. Dendritic cell-NK cell cross-talk: regulation and physiopathology. Curr Top Microbiol Immunol. 2006; 298:157-174.
43. Fernandez NC, Lozier A, Flament C, et al. Dendritic cells directly trigger NK cell functions: crosstalk relevant in innate anti-tumor immune responses in vivo. Nat Med. 1999;5:405-411. (Pubitemid 29180578)
44. Morandi B, Bougras G, Muller WA, Ferlazzo G, Munz C. NK cells of human secondary lymphoid tissues enhance T cell polarization via IFN-gamma secretion. Eur J Immunol. 2006;36:2394-2400. (Pubitemid 44420596)
45. Kalinski P, Giermasz A, Nakamura Y et al. Helper role of NK cells during the induction of anticancer responses by dendritic cells. Mol Immunol. 2005; 42:535-539. (Pubitemid 39655965)
46. Adam C, King S, Allgeier T et al. DC-NK cell cross talk as a novel CD4+ T-cell-independent pathway for antitumor CTL induction. Blood. 2005;106: 338-344. (Pubitemid 40967210)
47. Mocikat R, Braumuller H, Gumy A, et al. Natural killer cells activated by MHC class I(low) targets prime dendritic cells to induce protective CD8 T cell responses. Immunity. 2003;19:561-569. (Pubitemid 37311437)
48. Westwood JA, Kelly JM, Tanner JE, et al. Cutting edge: novel priming of tumor-specific immunity by NKG2D-triggered NK cell-mediated tumor rejection and Th1-independent CD4+ T cell pathway. J Immunol. 2004;172:757-761.
49. Chiesa S, Tomasello E, Vivier E, Vely F. Coordination of activating and inhibitory signals in natural killer cells. Mol Immunol. 2005;42:477-484. (Pubitemid 39655957)
50. Diefenbach A, Raulet DH. The innate immune response to tumors and its role in the induction of T-cell immunity. Immunol Rev. 2002;188:9-21. (Pubitemid 35398861)