The adjuvant effects of the toll-like receptor 3 ligand polyinosinic-cytidylic acid poly (I:C) on antigen-specific CD8+ T cell responses are partially dependent on NK cells with the induction of a beneficial cytokine milieu

Vaccine

Volumn 24, Issue 24, 2006, Pages 5119-5132

  Salem, Mohamed L ^a   EL Naggar, Sabry A ^a   Kadima, Andre ^a   Gillanders, William E ^a   Cole, David J ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

CD8+ T cells; Cytokines; Dendritic cells; Double stranded RNA; IFN; M ; NK cells; OT 1 cells; OVA; Poly (I:C); TLR3; Vaccination

Indexed keywords

ALPHA INTERFERON; CD11B ANTIGEN; CD3 ANTIGEN; CYTOKINE; GAMMA INTERFERON; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 10; INTERLEUKIN 12 RECEPTOR BETA2; INTERLEUKIN 15; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PEPTIDE; POLYINOSINIC POLYCYTIDYLIC ACID; SERYLISOLEUCYLISOLEUCYLASPARAGINYLPHENYLALANYLGLUTAMYLLYSYLLEUCINE; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; LYMPHOCYTE COUNT; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; VACCINATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CHEMOKINES; CYTOKINES; INTERFERON TYPE I; KILLER CELLS, NATURAL; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PEPTIDES; POLY I-C; TIME FACTORS; TOLL-LIKE RECEPTOR 3; VACCINATION;

EID: 33744521498     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2006.04.010     Document Type: Article

References (68)

1. Medzhitov R., and Janeway Jr. C.A. Innate immunity: impact on the adaptive immune response. Curr Opin Immunol 9 1 (1997) 4-9
2. Takeda K., and Akira S. Toll-like receptors in innate immunity. Int Immunol 17 1 (2005) 1-14
3. Akira S., Takeda K., and Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2 8 (2001) 675-680
4. Alexopoulou L., Holt A.C., Medzhitov R., and Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413 6857 (2001) 732-738
5. Banchereau J., and Steinman R.M. Dendritic cells and the control of immunity. Nature 392 6673 (1998) 245-252
6. Gelman A.E., Zhang J., Choi Y., and Turka L.A. Toll-like receptor ligands directly promote activated CD4+ T cell survival. J Immunol 172 10 (2004) 6065-6073
7. Matsumoto M., Kikkawa S., Kohase M., Miyake K., and Seya T. Establishment of a monoclonal antibody against human Toll-like receptor 3 that blocks double-stranded RNA-mediated signaling. Biochem Biophys Res Commun 293 5 (2002) 1364-1369
8. Meusel T.R., Kehoe K.E., and Imani F. Protein kinase R regulates double-stranded RNA induction of TNF-alpha but not IL-1 beta mRNA in human epithelial cells. J Immunol 168 12 (2002) 6429-6435
9. Durand V., Wong S.Y., Tough D.F., and Le Bon A. Shaping of adaptive immune responses to soluble proteins by TLR agonists: a role for IFN-alpha/beta. Immunol Cell Biol 82 6 (2004) 596-602
10. Lore K., Betts M.R., Brenchley J.M., Kuruppu J., Khojasteh S., Perfetto S., et al. Toll-like receptor ligands modulate dendritic cells to augment cytomegalovirus- and HIV-1-specific T cell responses. J Immunol 171 8 (2003) 4320-4328
11. Fujimoto C., Nakagawa Y., Ohara K., and Takahashi H. Polyriboinosinic polyribocytidylic acid [poly(I:C)]/TLR3 signaling allows class I processing of exogenous protein and induction of HIV-specific CD8+ cytotoxic T lymphocytes. Int Immunol 16 1 (2004) 55-63
12. Mattei F., Schiavoni G., Belardelli F., and Tough D.F. IL-15 is expressed by dendritic cells in response to type I IFN, double-stranded RNA, or lipopolysaccharide and promotes dendritic cell activation. J Immunol 167 3 (2001) 1179-1187
13. Burkett P.R., Koka R., Chien M., Chai S., Chan F., Ma A., et al. IL-15R alpha expression on CD8+ T cells is dispensable for T cell memory. Proc Natl Acad Sci USA 100 8 (2003) 4724-4729
14. Ahonen C.L., Doxsee C.L., McGurran S.M., Riter T.R., Wade W.F., Barth R.J., et al. Combined TLR and CD40 triggering induces potent CD8+ T cell expansion with variable dependence on type I IFN. J Exp Med 199 6 (2004) 775-784
15. Wang L., Smith D., Bot S., Dellamary L., Bloom A., and Bot A. Noncoding RNA danger motifs bridge innate and adaptive immunity and are potent adjuvants for vaccination. J Clin Invest 110 8 (2002) 1175-1184
16. Salem M.L., Kadima A.N., Cole D.J., and Gillanders W.E. Defining the antigen-specific T-cell response to vaccination and poly(I:C)/TLR3 signaling: evidence of enhanced primary and memory CD8 T-cell responses and antitumor immunity. J Immunother 28 3 (2005) 220-228
17. Belardelli F., and Ferrantini M. Cytokines as a link between innate and adaptive antitumor immunity. Trends Immunol 23 4 (2002) 201-208
18. Honda K., Sakaguchi S., Nakajima C., Watanabe A., Yanai H., Matsumoto M., et al. Selective contribution of IFN-alpha/beta signaling to the maturation of dendritic cells induced by double-stranded RNA or viral infection. Proc Natl Acad Sci USA 100 19 (2003) 10872-10877
19. de Jong E.C., Vieira P.L., Kalinski P., Schuitemaker J.H., Tanaka Y., Wierenga E.A., et al. Microbial compounds selectively induce Th1 cell-promoting or Th2 cell-promoting dendritic cells in vitro with diverse th cell-polarizing signals. J Immunol 168 4 (2000) 1704-1709
20. Hoebe K., Janssen E.M., Kim S.O., Alexopoulou L., Flavell R.A., Han J., et al. Upregulation of costimulatory molecules induced by lipopolysaccharide and double-stranded RNA occurs by Trif-dependent and Trif-independent pathways. Nat Immunol 4 12 (2003) 1223-1229
21. Diebold S.S., Montoya M., Unger H., Alexopoulou L., Roy P., Haswell L.E., et al. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 424 6946 (2003) 324-328
22. Shrikant P., Khoruts A., and Mescher M.F. CTLA-4 blockade reverses CD8+ T cell tolerance to tumor by a CD4+ T cell- and IL-2-dependent mechanism. Immunity 11 4 (1999) 483-493
23. Pilaro A.M., Taub D.D., McCormick K.L., Williams H.M., Sayers T.J., Fogler W.E., et al. TNF-alpha is a principal cytokine involved in the recruitment of NK cells to liver parenchyma. J Immunol 153 1 (1994) 333-342
24. Wang J., Sun R., Wei H., Dong Z., Gao B., and Tian Z. Poly I:C prevents T cell-mediated hepatitis via an NK-dependent mechanism. J Hepatol 44 3 (2006) 446-454
25. Dong Z., Wei H., Sun R., Hu Z., Gao B., and Tian Z. Involvement of natural killer cells in PolyI:C-induced liver injury. J Hepatol 41 6 (2004) 966-973
26. Dong Z.J., Wei H.M., Sun R., Tian Z.G., and Gao B. Isolation of murine hepatic lymphocytes using mechanical dissection for phenotypic and functional analysis of NK1.1+ cells. World J Gastroenterol 10 13 (2004) 1928-1933
27. Shaw S.G., Maung A.A., Steptoe R.J., Thomson A.W., and Vujanovic N.L. Expansion of functional NK cells in multiple tissue compartments of mice treated with Flt3-ligand: implications for anti-cancer and anti-viral therapy. J Immunol 161 6 (1998) 2817-2824
28. Belladonna M.L., Renauld J.C., Bianchi R., Vacca C., Fallarino F., Orabona C., et al. IL-23 and IL-12 have overlapping, but distinct, effects on murine dendritic cells. J Immunol 168 11 (2002) 5448-5454
29. Blattman J.N., Cheng L.E., and Greenberg P.D. CD8(+) T cell responses: it's all downhill after their prime. Nat Immunol 3 7 (2002) 601-602
30. Webb S.J., Harrison D.J., and Wyllie A.H. Apoptosis: an overview of the process and its relevance in disease. Adv Pharmacol 41 (1997) 1-34
31. Kawabe Y., and Ochi A. Programmed cell death and extrathymic reduction of Vbeta8+ CD4+ T cells in mice tolerant to Staphylococcus aureus enterotoxin B. Nature 349 6306 (1991) 245-248
32. Valenzuela J., Schmidt C., and Mescher M. The roles of IL-12 in providing a third signal for clonal expansion of naive CD8 T cells. J Immunol 169 12 (2002) 6842-6849
33. Harmala L.A., Ingulli E.G., Curtsinger J.M., Lucido M.M., Schmidt C.S., Weigel B.J., et al. The adjuvant effects of Mycobacterium tuberculosis heat shock protein 70 result from the rapid and prolonged activation of antigen-specific CD8+ T cells in vivo. J Immunol 169 10 (2002) 5622-5629
34. Rubinstein M.P., Kadima A.N., Salem M.L., Nguyen C.L., Gillanders W.E., and Cole D.J. Systemic administration of IL-15 augments the antigen-specific primary CD8+ T cell response following vaccination with peptide-pulsed dendritic cells. J Immunol 169 9 (2002) 4928-4935
35. Salem M.L., Kadima A.N., Zhou Y., Nguyen C.L., Rubinstein M.P., Demcheva M., et al. Paracrine release of IL-12 stimulates IFN-gamma production and dramatically enhances the antigen-specific T cell response after vaccination with a novel peptide-based cancer vaccine. J Immunol 172 9 (2004) 5159-5167
36. Tham E.L., and Mescher M.F. The poststimulation program of CD4 versus CD8 T cells (death versus activation-induced nonresponsiveness). J Immunol 169 4 (2002) 1822-1828
37. Deeths M.J., Kedl R.M., and Mescher M.F. CD8+ T cells become nonresponsive (anergic) following activation in the presence of costimulation. J Immunol 163 1 (1999) 102-110
38. Curtsinger J.M., Schmidt C.S., Mondino A., Lins D.C., Kedl R.M., Jenkins M.K., et al. Inflammatory cytokines provide a third signal for activation of naive CD4+ and CD8+ T cells. J Immunol 162 6 (1999) 3256-3262
39. Hermans I.F., Silk J.D., Gileadi U., Salio M., Mathew B., Ritter G., et al. NKT cells enhance CD4+ and CD8+ T cell responses to soluble antigen in vivo through direct interaction with dendritic cells. J Immunol 171 10 (2003) 5140-5147
40. Curtsinger J.M., Valenzuela J.O., Agarwal P., Lins D., and Mescher M.F. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J Immunol 174 8 (2005) 4465-4469
41. Belardelli F. Role of interferons and other cytokines in the regulation of the immune response. Apmis 103 3 (1995) 161-179
42. Frucht D.M., Fukao T., Bogdan C., Schindler H., O'Shea J.J., and Koyasu S. IFN-gamma production by antigen-presenting cells: mechanisms emerge. Trends Immunol 22 10 (2001) 556-560
43. Luft T., Pang K.C., Thomas E., Hertzog P., Hart D.N., Trapani J., et al. Type I IFNs enhance the terminal differentiation of dendritic cells. J Immunol 161 4 (1998) 1947-1953
44. Kamath A.T., Sheasby C.E., and Tough D.F. Dendritic cells and NK cells stimulate bystander T cell activation in response to TLR agonists through secretion of IFN-alphabeta and IFN-gamma. J Immunol 174 2 (2005) 767-776
45. Jonuleit H., Knop J., and Enk A.H. Cytokines and their effects on maturation, differentiation and migration of dendritic cells. Arch Dermatol Res 289 1 (1996) 1-8
46. Siegal F.P., Kadowaki N., Shodell M., Fitzgerald-Bocarsly P.A., Shah K., Ho S., et al. The nature of the principal type 1 interferon-producing cells in human blood. Science 284 5421 (1999) 1835-1837
47. Theofilopoulos A.N., Baccala R., Beutler B., and Kono D.H. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol 23 (2005) 307-336
48. Santini S.M., Lapenta C., Logozzi M., Parlato S., Spada M., Di Pucchio T., et al. Type I interferon as a powerful adjuvant for monocyte-derived dendritic cell development and activity in vitro and in Hu-PBL-SCID mice. J Exp Med 191 10 (2000) 1777-1788
49. Biron C.A. Initial and innate responses to viral infections-pattern setting in immunity or disease. Curr Opin Microbiol 2 4 (1999) 374-381
50. Sato M., Taniguchi T., and Tanaka N. The interferon system and interferon regulatory factor transcription factors-studies from gene knockout mice. Cytokine Growth Factor Rev 12 2-3 (2001) 133-142
51. Marrack P., Kappler J., and Mitchell T. Type I interferons keep activated T cells alive. J Exp Med 189 3 (1999) 521-530
52. Gehring S., Gregory S.H., Kuzushita N., and Wands J.R. Type 1 interferon augments DNA-based vaccination against hepatitis C virus core protein. J Med Virol 75 2 (2005) 249-257
53. Kolumam G.A., Thomas S., Thompson L.J., Sprent J., and Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 202 5 (2005) 637-650
54. Djeu J.Y., Heinbaugh J.A., Holden H.T., and Herberman R.B. Augmentation of mouse natural killer cell activity by interferon and interferon inducers. J Immunol 122 1 (1979) 175-181
55. Talmadge J.E., Adams J., Phillips H., Collins M., Lenz B., Schneider M., et al. Immunomodulatory effects in mice of polyinosinic-polycytidylic acid complexed with poly-l-lysine and carboxymethylcellulose. Cancer Res 45 3 (1985) 1058-1065
56. Martin-Fontecha A., Thomsen L.L., 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 5 12 (2004) 1260-1265
57. Kim A., Noh Y.W., Kim K.D., Jang Y.S., Choe Y.K., and Lim J.S. Activated natural killer cell-mediated immunity is required for the inhibition of tumor metastasis by dendritic cell vaccination. Exp Mol Med 36 5 (2004) 428-443
58. Gerosa F., Baldani-Guerra B., Nisii C., Marchesini V., Carra G., and Trinchieri G. Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med 195 3 (2002) 327-333
59. Piccioli D., Sbrana S., Melandri E., and Valiante N.M. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J Exp Med 195 3 (2002) 335-341
60. Andrews D.M., Scalzo A.A., Yokoyama W.M., Smyth M.J., and Degli-Esposti M.A. Functional interactions between dendritic cells and NK cells during viral infection. Nat Immunol 4 2 (2003) 175-181
61. Fernandez N.C., 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 5 4 (1999) 405-411
62. 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 174 2 (2005) 727-734
63. Edwards A.D., Diebold S.S., Slack E.M., Tomizawa H., Hemmi H., Kaisho T., et al. Toll-like receptor expression in murine DC subsets: lack of TLR7 expression by CD8 alpha+ DC correlates with unresponsiveness to imidazoquinolines. Eur J Immunol 33 4 (2003) 827-833
64. Edwards K.M., Kam C.M., Powers J.C., and Trapani J.A. The human cytotoxic T cell granule serine protease granzyme H has chymotrypsin-like (chymase) activity and is taken up into cytoplasmic vesicles reminiscent of granzyme B-containing endosomes. J Biol Chem 274 43 (1999) 30468-30473
65. Hochrein H., O'Keeffe M., and Wagner H. Human and mouse plasmacytoid dendritic cells. Hum Immunol 63 12 (2002) 1103-1110
66. Kadowaki N., Ho S., Antonenko S., Malefyt R.W., Kastelein R.A., Bazan F., et al. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J Exp Med 194 6 (2001) 863-869
67. Schmidt K.N., Leung B., Kwong M., Zarember K.A., Satyal S., Navas T.A., et al. APC-independent activation of NK cells by the Toll-like receptor 3 agonist double-stranded RNA. J Immunol 172 1 (2004) 138-143
68. Salem ML, Kadima A, EL-Naggar S, Rubinstein MM, Gillanders WE, Cole DJ. Defining the ability of cyclophosphamide preconditioning to enhance the antigen-specific CD8 T cell response to peptide vaccination: creation of a beneficial host microenvironment involving type I IFNs and myeloid cells. J Immunotherapy 2006; In Press.