Il-18-based combinatorial adjuvants promote the intranodal production of ccl19 by nk cells and dendritic cells of cancer patients

OncoImmunology

Volumn 2, Issue 9, 2013, Pages

  Wong, Jeffrey L ^a   Muthuswamy, Ravikumar ^a   Bartlett, David L ^a,b   Kalinski, Pawel ^a,b,c  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Adjuvant; CCL19; Colorectal cancer; Dendritic cell; IL 18; Lymph node; Natural killer cell

Indexed keywords

ALPHA INTERFERON; CHEMOKINE RECEPTOR CCR7; GAMMA INTERFERON; GRANZYME B; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 2; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL STIMULATION; COLORECTAL CANCER; CYTOKINE PRODUCTION; DENDRITIC CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; LYMPH NODE; NATURAL KILLER CELL; PROTEIN EXPRESSION; UPREGULATION;

EID: 84890258401     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.4161/onci.26245     Document Type: Article

References (56)

1. Martin-Fontecha A, Sebastiani S, Höpken UE, Uguccioni M, Lipp M, Lanzavecchia A, Sallusto F. Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J Exp Med 2003; 198:615- 21; PMID:12925677; http://dx.doi.org/10.1084/ jem.20030448
2. Baekkevold ES, Yamanaka T, Palframan RT, Carlsen HS, Reinholt FP, von Andrian UH, Brandtzaeg P, Haraldsen G. The CCR7 ligand elc (CCL19) is transcytosed in high endothelial venules and mediates T cell recruitment. J Exp Med 2001; 193:1105- 12; PMID:11342595; http://dx.doi.org/10.1084/ jem.193.9.1105
3. Braun A, Worbs T, Moschovakis GL, Halle S, Hoffmann K, Bölter J, Münk A, Förster R. Afferent lymph-derived T cells and DCs use different chemokine receptor CCR7-dependent routes for entry into the lymph node and intranodal migration. Nat Immunol 2011; 12:879-87; PMID:21841786; http:// dx.doi.org/10.1038/ni.2085
4. Worbs T, Mempel TR, Bölter J, von Andrian UH, Förster R. CCR7 ligands stimulate the intranodal motility of T lymphocytes in vivo. J Exp Med 2007; 204:489-95; PMID:17325198; http://dx.doi. org/10.1084/jem.20061706
5. Asperti-Boursin F, Real E, Bismuth G, Trautmann A, Donnadieu E. CCR7 ligands control basal T cell motility within lymph node slices in a phosphoinositide 3-kinase-independent manner. J Exp Med 2007; 204:1167-79; PMID:17485513; http://dx.doi. org/10.1084/jem.20062079
6. Okada T, Cyster JG. CC chemokine receptor 7 contributes to Gi-dependent T cell motility in the lymph node. J Immunol 2007; 178:2973-8; PMID:17312142
7. Friedman RS, Jacobelli J, Krummel MF. Surfacebound chemokines capture and prime T cells for synapse formation. Nat Immunol 2006; 7:1101-8; PMID:16964261; http://dx.doi.org/10.1038/ni1384
8. Scimone ML, Felbinger TW, Mazo IB, Stein JV, Von Andrian UH, Weninger W. CXCL12 mediates CCR7-independent homing of central memory cells, but not naive T cells, in peripheral lymph nodes. J Exp Med 2004; 199:1113-20; PMID:15096537; http://dx.doi.org/10.1084/jem.20031645
9. Yang L, Yu Y, Kalwani M, Tseng TW, Baltimore D. Homeostatic cytokines orchestrate the segregation of CD4 and CD8 memory T-cell reservoirs in mice. Blood 2011; 118:3039-50; PMID:21791416; http:// dx.doi.org/10.1182/blood-2011-04-349746
10. Mocikat R, Braumüller H, Gumy A, Egeter O, Ziegler H, Reusch U, Bubeck A, Louis J, Mailhammer R, Riethmüller G, et al. Natural killer cells activated by MHC class I(low) targets prime dendritic cells to induce protective CD8 T cell responses. Immunity 2003; 19:561-9; PMID:14563320; http://dx.doi. org/10.1016/S1074-7613(03)00264-4
11. Martín-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, Sallusto F. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 2004; 5:1260-5; PMID:15531883; http://dx.doi. org/10.1038/ni1138
12. Adam C, King S, Allgeier T, Braumüller H, Lüking C, Mysliwietz J, Kriegeskorte A, Busch DH, Röcken M, Mocikat R. DC-NK cell cross talk as a novel CD4+ T-cell-independent pathway for antitumor CTL induction. Blood 2005; 106:338- 44; PMID:15769894; http://dx.doi.org/10.1182/ blood-2004-09-3775
13. Smith DE. The biological paths of IL-1 family members IL-18 and IL-33. J Leukoc Biol 2011; 89:383- 92; PMID:20952658; http://dx.doi.org/10.1189/ jlb.0810470
14. Kastenmüller W, Torabi-Parizi P, Subramanian N, Lämmermann T, Germain RN. A spatially-organized multicellular innate immune response in lymph nodes limits systemic pathogen spread. Cell 2012; 150:1235-48; PMID:22980983; http://dx.doi. org/10.1016/j.cell.2012.07.021
15. Mailliard RB, Alber SM, Shen H, Watkins SC, Kirkwood JM, Herberman RB, Kalinski P. IL-18- induced CD83+CCR7+ NK helper cells. J Exp Med 2005; 202:941-53; PMID:16203865; http://dx.doi. org/10.1084/jem.20050128
16. Takeda K, Tsutsui H, Yoshimoto T, Adachi O, Yoshida N, Kishimoto T, Okamura H, Nakanishi K, Akira S. Defective NK cell activity and Th1 response in IL-18-deficient mice. Immunity 1998; 8:383- 90; PMID:9529155; http://dx.doi.org/10.1016/ S1074-7613(00)80543-9
17. Wong JL, Mailliard RB, Moschos SJ, Edington H, Lotze MT, Kirkwood JM, Kalinski P. Helper activity of natural killer cells during the dendritic cell-mediated induction of melanoma-specific cytotoxic T cells. J Immunother 2011; 34:270-8; PMID:21389871; http://dx.doi.org/10.1097/CJI.0b013e31820b370b
18. Bromley SK, Mempel TR, Luster AD. Orchestrating the orchestrators: chemokines in control of T cell traffic. Nat Immunol 2008; 9:970-80; PMID:18711434; http://dx.doi.org/10.1038/ni.f.213
19. Shi FD, Ljunggren HG, La Cava A, Van Kaer L. Organ-specific features of natural killer cells. Nat Rev Immunol 2011; 11:658-71; PMID:21941294; http:// dx.doi.org/10.1038/nri3065
20. Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity 2006; 25:373-81; PMID:16979569; http://dx.doi.org/10.1016/j. immuni.2006.08.007
21. Fuertes MB, Woo SR, Burnett B, Fu YX, Gajewski TF. Type I interferon response and innate immune sensing of cancer. Trends Immunol 2013; 34:67- 73; PMID:23122052; http://dx.doi.org/10.1016/j. it.2012.10.004
22. Mailliard RB, Son YI, Redlinger R, Coates PT, Giermasz A, Morel PA, Storkus WJ, Kalinski P. Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J Immunol 2003; 171:2366-73; PMID:12928383
23. Langenkamp A, Nagata K, Murphy K, Wu L, Lanzavecchia A, Sallusto F. Kinetics and expression patterns of chemokine receptors in human CD4+ T lymphocytes primed by myeloid or plasmacytoid dendritic cells. Eur J Immunol 2003; 33:474- 82; PMID:12645946; http://dx.doi.org/10.1002/ immu.200310023
24. Sallusto F, Palermo B, Lenig D, Miettinen M, Matikainen S, Julkunen I, Forster R, Burgstahler R, Lipp M, Lanzavecchia A. Distinct patterns and kinetics of chemokine production regulate dendritic cell function. Eur J Immunol 1999; 29:1617- 25; PMID:10359116; http://dx.doi.org/10.1002/ (SICI )1521-4141(199905)29: 051617: :AIDIMMU1617 3.0.CO;2-3
25. Vissers JL, Hartgers FC, Lindhout E, Teunissen MB, Figdor CG, Adema GJ. Quantitative analysis of chemokine expression by dendritic cell subsets in vitro and in vivo. J Leukoc Biol 2001; 69:785-93; PMID:11358988
26. Kaiser A, Donnadieu E, Abastado JP, Trautmann A, Nardin A. CC chemokine ligand 19 secreted by mature dendritic cells increases naive T cell scanning behavior and their response to rare cognate antigen. J Immunol 2005; 175:2349-56; PMID:16081805
27. Ngo VN, Tang HL, Cyster JG. Epstein-Barr virusinduced molecule 1 ligand chemokine is expressed by dendritic cells in lymphoid tissues and strongly attracts naive T cells and activated B cells. J Exp Med 1998; 188:181-91; PMID:9653094; http://dx.doi. org/10.1084/jem.188.1.181
28. Katou F, Ohtani H, Nakayama T, Nagura H, Yoshie O, Motegi K. Differential expression of CCL19 by DC-Lamp+ mature dendritic cells in human lymph node versus chronically inflamed skin. J Pathol 2003; 199:98-106; PMID:12474232; http://dx.doi. org/10.1002/path.1255
29. Pietilä TE, Veckman V, Lehtonen A, Lin R, Hiscott J, Julkunen I. Multiple NF-kappaB and IFN regulatory factor family transcription factors regulate CCL19 gene expression in human monocyte-derived dendritic cells. J Immunol 2007; 178:253-61; PMID:17182562
30. Means TK, Hayashi F, Smith KD, Aderem A, Luster AD. The Toll-like receptor 5 stimulus bacterial flagellin induces maturation and chemokine production in human dendritic cells. J Immunol 2003; 170:5165- 75; PMID:12734364
31. Raulet DH, Guerra N. Oncogenic stress sensed by the immune system: role of natural killer cell receptors. Nat Rev Immunol 2009; 9:568-80; PMID:19629084; http://dx.doi.org/10.1038/ nri2604
32. Ge MQ, Ho AW, Tang Y, Wong KH, Chua BY, Gasser S, Kemeny DM. NK cells regulate CD8+ T cell priming and dendritic cell migration during influenza A infection by IFN-γ and perforin-dependent mechanisms. J Immunol 2012; 189:2099-109; PMID:22869906; http://dx.doi.org/10.4049/ jimmunol.1103474
33. 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; PMID:11828007; http://dx.doi.org/10.1084/jem.20010938
34. Pak-Wittel MA, Yang L, Sojka DK, Rivenbark JG, Yokoyama WM. Interferon-γ mediates chemokine- dependent recruitment of natural killer cells during viral infection. Proc Natl Acad Sci U S A 2013; 110:E50-9; PMID:23248310; http://dx.doi. org/10.1073/pnas.1220456110
35. Watt SV, Andrews DM, Takeda K, Smyth MJ, Hayakawa Y. IFN-gamma-dependent recruitment of mature CD27(high) NK cells to lymph nodes primed by dendritic cells. J Immunol 2008; 181:5323-30; PMID:18832688
36. Ferlazzo G, Pack M, Thomas D, Paludan C, Schmid D, Strowig T, Bougras G, Muller WA, Moretta L, Münz C. 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 U S A 2004; 101:16606-11; PMID:15536127; http:// dx.doi.org/10.1073/pnas.0407522101
37. Van Elssen CH, Vanderlocht J, Frings PW, Senden- Gijsbers BL, Schnijderberg MC, van Gelder M, Meek B, Libon C, Ferlazzo G, Germeraad WT, et al. Klebsiella pneumoniae-triggered DC recruit human NK cells in a CCR5-dependent manner leading to increased CCL19-responsiveness and activation of NK cells. Eur J Immunol 2010; 40:3138- 49; PMID:20865789; http://dx.doi.org/10.1002/ eji.201040496
38. Fernandez NC, Lozier A, Flament C, Ricciardi-Castagnoli P, Bellet D, Suter M, Perricaudet M, Tursz T, Maraskovsky E, Zitvogel L. Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate anti-tumor immune responses in vivo. Nat Med 1999; 5:405-11; PMID:10202929; http:// dx.doi.org/10.1038/7403
39. Hillinger S, Yang SC, Zhu L, Huang M, Duckett R, Atianzar K, Batra RK, Strieter RM, Dubinett SM, Sharma S. EBV-induced molecule 1 ligand chemokine (ELC/CCL19) promotes IFN-gamma-dependent antitumor responses in a lung cancer model. J Immunol 2003; 171:6457-65; PMID:14662845
40. Hillinger S, Yang SC, Batra RK, Strieter RM, Weder W, Dubinett SM, Sharma S. CCL19 reduces tumour burden in a model of advanced lung cancer. Br J Cancer 2006; 94:1029-34; PMID:16598185; http:// dx.doi.org/10.1038/sj.bjc.6603061
41. Westermann J, Nguyen-Hoai T, Baldenhofer G, Höpken UE, Lipp M, Dörken B, Pezzutto A. CCL19 (ELC) as an adjuvant for DNA vaccination: induction of a TH1-type T-cell response and enhancement of antitumor immunity. Cancer Gene Ther 2007; 14:523-32; PMID:17384577; http://dx.doi. org/10.1038/sj.cgt.7701042
42. Nguyen-Hoai T, Baldenhofer G, Ahmed MS, Pham-Duc M, Gries M, Lipp M, Dörken B, Pezzutto A, Westermann J. CCL19 (ELC) improves TH1-polarized immune responses and protective immunity in a murine Her2/neu DNA vaccination model. J Gene Med 2012; 14:128-37; PMID:22228591; http://dx.doi.org/10.1002/jgm.1651
43. Treilleux I, Blay JY, Bendriss-Vermare N, Ray-Coquard I, Bachelot T, Guastalla JP, Bremond A, Goddard S, Pin JJ, Barthelemy-Dubois C, et al. Dendritic cell infiltration and prognosis of early stage breast cancer. Clin Cancer Res 2004; 10:7466-74; PMID:15569976; http://dx.doi.org/10.1158/1078-0432.CCR-04-0684
44. Tarhini AA, Millward M, Mainwaring P, Kefford R, Logan T, Pavlick A, Kathman SJ, Laubscher KH, Dar MM, Kirkwood JM. A phase 2, randomized study of SB-485232, rhIL-18, in patients with previously untreated metastatic melanoma. Cancer 2009; 115:859-68; PMID:19140204; http://dx.doi. org/10.1002/cncr.24100
45. Smyth MJ, Swann J, Kelly JM, Cretney E, Yokoyama WM, Diefenbach A, Sayers TJ, Hayakawa Y. NKG2D recognition and perforin effector function mediate effective cytokine immunotherapy of cancer. J Exp Med 2004; 200:1325-35; PMID:15545356; http://dx.doi.org/10.1084/jem.20041522
46. Terme M, Ullrich E, Aymeric L, Meinhardt K, Desbois M, Delahaye N, Viaud S, Ryffel B, Yagita H, Kaplanski G, et al. IL-18 induces PD-1-dependent immunosuppression in cancer. Cancer Res 2011; 71:5393-9; PMID:21724589; http://dx.doi. org/10.1158/0008-5472.CAN-11-0993
47. Terme M, Ullrich E, Aymeric L, Meinhardt K, Coudert JD, Desbois M, Ghiringhelli F, Viaud S, Ryffel B, Yagita H, et al. Cancer-induced immunosuppression: IL-18-elicited immunoablative NK cells. Cancer Res 2012; 72:2757-67; PMID:22427351; http://dx.doi.org/10.1158/0008-5472.CAN-11-3379
48. Fridman WH, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012; 12:298-306; PMID:22419253; http://dx.doi.org/10.1038/ nrc3245
49. Dieu-Nosjean MC, Antoine M, Danel C, Heudes D, Wislez M, Poulot V, Rabbe N, Laurans L, Tartour E, de Chaisemartin L, et al. Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol 2008; 26:4410-7; PMID:18802153; http://dx.doi. org/10.1200/JCO.2007.15.0284
50. de Chaisemartin L, Goc J, Damotte D, Validire P, Magdeleinat P, Alifano M, Cremer I, Fridman WH, Sautès-Fridman C, Dieu-Nosjean MC. Characterization of chemokines and adhesion molecules associated with T cell presence in tertiary lymphoid structures in human lung cancer. Cancer Res 2011; 71:6391-9; PMID:21900403; http://dx.doi. org/10.1158/0008-5472.CAN-11-0952
51. Martinet L, Garrido I, Filleron T, Le Guellec S, Bellard E, Fournie JJ, Rochaix P, Girard JP. Human solid tumors contain high endothelial venules: association with T-and B-lymphocyte infiltration and favorable prognosis in breast cancer. Cancer Res 2011; 71:5678-87; PMID:21846823; http://dx.doi. org/10.1158/0008-5472.CAN-11-0431
52. Middel P, Brauneck S, Meyer W, Radzun HJ. Chemokine-mediated distribution of dendritic cell subsets in renal cell carcinoma. BMC Cancer 2010; 10:578; PMID:20969772; http://dx.doi. org/10.1186/1471-2407-10-578
53. Correale P, Rotundo MS, Botta C, Del Vecchio MT, Ginanneschi C, Licchetta A, Conca R, Apollinari S, De Luca F, Tassone P, et al. Tumor infiltration by T lymphocytes expressing chemokine receptor 7 (CCR7) is predictive of favorable outcome in patients with advanced colorectal carcinoma. Clin Cancer Res 2012; 18:850-7; PMID:22142823; http://dx.doi. org/10.1158/1078-0432.CCR-10-3186
54. Mailliard RB, Wankowicz-Kalinska A, Cai Q, Wesa A, Hilkens CM, Kapsenberg ML, Kirkwood JM, Storkus WJ, Kalinski P. alpha-type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. Cancer Res 2004; 64:5934-7; PMID:15342370; http://dx.doi.org/10.1158/0008-5472.CAN-04-1261
55. Muthuswamy R, Mueller-Berghaus J, Haberkorn U, Reinhart TA, Schadendorf D, Kalinski P. PGE(2) transiently enhances DC expression of CCR7 but inhibits the ability of DCs to produce CCL19 and attract naive T cells. Blood 2010; 116:1454-9; PMID:20498301; http://dx.doi.org/10.1182/ blood-2009-12-258038
56. Muthuswamy R, Urban J, Lee JJ, Reinhart TA, Bartlett D, Kalinski P. Ability of mature dendritic cells to interact with regulatory T cells is imprinted during maturation. Cancer Res 2008; 68:5972-8; PMID:18632653; http://dx.doi.org/10.1158/0008-5472.CAN-07-6818