Immune adjuvant efficacy of CpG oligonucleotide in cancer treatment is founded specifically upon TLR9 function in plasmacytoid dendritic cells

Cancer Research

Volumn 71, Issue 20, 2011, Pages 6428-6437

  Nierkens, Stefan ^a,b   Den Brok, Martijn H ^b   Garcia, Zacharias ^a,f   Togher, Susan ^a   Wagenaars, Jori ^b   Wassink, Melissa ^b   Boon, Louis ^c   Ruers, Theo J ^d   Figdor, Carl G ^b   Schoenberger, Stephen P ^a   Adema, Gosse J ^b   Janssen, Edith M ^e  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c BIOCEROS   (Netherlands)

^d NETHERLANDS CANCER INSTITUTE   (Netherlands)

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

^f INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD11B ANTIGEN; CD8ALPHA ANTIGEN; CPG OLIGODEOXYNUCLEOTIDE; CYTOCHROME C; GAMMA INTERFERON; GLYCOPROTEIN P 15095; HERMES ANTIGEN; INTERFERON RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TOLL LIKE RECEPTOR 9; TUMOR ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; ARTICLE; CANCER IMMUNOTHERAPY; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CELL INTERACTION; CELL ISOLATION; CELL MATURATION; CONTROLLED STUDY; CROSS PRESENTATION; CRYOABLATION; IMMUNE RESPONSE; IN VIVO STUDY; INTERNALIZATION; LYMPHOCYTE PROLIFERATION; MALIGNANT NEOPLASTIC DISEASE; MELANOMA CELL; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T CELL DEPLETION; TUMOR ABLATION; TUMOR IMMUNITY; UPREGULATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGENS, CD80; ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CROSS-PRIMING; DENDRITIC CELLS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OLIGODEOXYRIBONUCLEOTIDES; RECEPTOR, INTERFERON ALPHA-BETA; SKIN NEOPLASMS; TOLL-LIKE RECEPTOR 9; UP-REGULATION;

EID: 80054015074     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-2154     Document Type: Article

References (34)

1. Kennedy JE. Innovation: high-intensity focused ultrasound in the treatment of solid tumours. Nat Rev Cancer 2005;5:321-7. (Pubitemid 40488637)
2. den Brok MH, Sutmuller RP, van der Voort R, Bennink EJ, Figdor CG, Ruers TJ, et al. In situ tumor ablation creates an antigen source for the generation of antitumor immunity. Cancer Res 2004;64:4024-9. (Pubitemid 38697319)
3. den Brok MH, Sutmuller RP, Nierkens S, Bennink EJ, Frielink C, Toonen LW, et al. Efficient loading of dendritic cells following cryo and radiofrequency ablation in combination with immune modulation induces anti-tumour immunity. Br J Cancer 2006;95:896-905. (Pubitemid 44498106)
4. Nierkens S, den Brok MH, Sutmuller RP, Grauer OM, Bennink E, Morgan ME, et al. In vivo colocalization of antigen and CpG within dendritic cells is associated with the efficacy of cancer immunotherapy. Cancer Res 2008;68:5390-6.
5. den Brok MH, Sutmuller RP, Nierkens S, Bennink EJ, Toonen LW, Figdor CG, et al. Synergy between in situ cryoablation and TLR9 stimulation results in a highly effective in vivo dendritic cell vaccine. Cancer Res 2006;66:7285-92. (Pubitemid 44197710)
6. Nierkens S, den Brok MH, Roelofsen T, Wagenaars JA, Figdor CG, Ruers TJ, et al. Route of administration of the TLR9 agonist CpG critically determines the efficacy of cancer immunotherapy in mice. PLoS One 2009;4:e8368.
7. den Haan JM, Lehar SM, Bevan MJ. CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med 2000;192:1685-96.
8. Bedoui S, Prato S, Mintern J, Gebhardt T, Zhan Y, Lew AM, et al. Characterization of an immediate splenic precursor of CD8+ dendritic cells capable of inducing antiviral T cell responses. J Immunol 2009;182:4200-7.
9. Janssen E, Tabeta K, Barnes MJ, Rutschmann S, McBride S, Bahjat KS, et al. Efficient T cell activation via a Toll-Interleukin 1 receptor-independent pathway. Immunity 2006;24:787-99. (Pubitemid 43867366)
10. Krug A, Veeraswamy R, Pekosz A, Kanagawa O, Unanue ER, Colonna M, et al. Interferon-producing cells fail to induce proliferation of naive T cells but can promote expansion and T helper 1 differentiation of antigen-experienced unpolarized T cells. J Exp Med 2003;197:899-906. (Pubitemid 36437866)
11. Naranjo-Gomez M, Fernandez MA, Bofill M, Singh R, Navarrete CV, Pujol-Borrell R, et al. Primary alloproliferative TH1 response induced by immature plasmacytoid dendritic cells in collaboration with myeloid DCs. Am J Transplant 2005;5:2838-48. (Pubitemid 43923944)
12. Kasturi SP, Pulendran B. Cross-presentation: avoiding trafficking chaos? Nat Immunol 2008;9:461-3. (Pubitemid 351560512)
13. Colonna M, Cella M. Cross-presentation: plasmacytoid dendritic cells are in the business. Immunity 2007;27:419-21. (Pubitemid 47418673)
14. Yoneyama H, Matsuno K, Toda E, Nishiwaki T, Matsuo N, Nakano A, et al. Plasmacytoid DCs help lymph node DCs to induce anti-HSV CTLs. J Exp Med 2005;202:425-35. (Pubitemid 41126960)
15. Falo LD Jr, Kovacsovics-Bankowski M, Thompson K, Rock KL. Targeting antigen into the phagocytic pathway in vivo induces protective tumour immunity. Nat Med 1995;1:649-53.
16. Lin ML, Zhan Y, Proietto AI, Prato S, Wu L, Heath WR, et al. Selective suicide of cross-presenting CD8+ dendritic cells by cytochrome c injection shows functional heterogeneity within this subset. Proc Natl Acad Sci U S A 2008;105:3029-34. (Pubitemid 351723662)
17. Reboulet RA, Hennies CM, Garcia Z, Nierkens S, Janssen EM. Prolonged antigen storage endows merocytic dendritic cells with enhanced capacity to prime anti-tumor responses in tumor-bearing mice. J Immunol 2010;185:3337-47.
18. Allan RS, Waithman J, Bedoui S, Jones CM, Villadangos JA, Zhan Y, et al. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 2006;25:153-62. (Pubitemid 44066832)
19. Megjugorac NJ, Jacobs ES, Izaguirre AG, George TC, Gupta G, Fitzgerald-Bocarsly P. Image-based study of interferongenic interactions between plasmacytoid dendritic cells and HSV-infected monocyte-derived dendritic cells. Immunol Invest 2007;36:739-61.
20. Piccioli D, Sammicheli C, Tavarini S, Nuti S, Frigimelica E, Manetti AG, et al. Human plasmacytoid dendritic cells are unresponsive to bacterial stimulation and require a novel type of cooperation with myeloid dendritic cells for maturation. Blood 2009;113:4232-9.
21. Villadangos JA, Young L. Antigen-presentation properties of plasmacytoid dendritic cells. Immunity 2008;29:352-61.
22. Mouries J, Moron G, Schlecht G, Escriou N, Dadaglio G, Leclerc C. Plasmacytoid dendritic cells efficiently cross-prime naive T cells in vivo after TLR activation. Blood 2008;112:3713-22.
23. Kuwajima S, Sato T, Ishida K, Tada H, Tezuka H, Ohteki T. Interleukin 15-dependent crosstalk between conventional and plasmacytoid dendritic cells is essential for CpG-induced immune activation. Nat Immunol 2006;7:740-6. (Pubitemid 43905873)
24. Lou Y, Liu C, Kim GJ, Liu YJ, Hwu P, Wang G. Plasmacytoid dendritic cells synergize with myeloid dendritic cells in the induction of antigen-specific antitumor immune responses. J Immunol 2007;178:1534-41. (Pubitemid 46154624)
25. Burnette BC, Liang H, Lee Y, Chlewicki L, Khodarev NN, Weichselbaum RR, et al. The efficacy of radiotherapy relies upon induction of type i interferon-dependent innate and adaptive immunity. Cancer Res 2011;71:2488-96.
26. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007;13:1050-9. (Pubitemid 47517504)
27. Manegold C, Gravenor D, Woytowitz D, Mezger J, Hirsh V, Albert G, et al. Randomized phase II trial of a toll-like receptor 9 agonist oligodeoxynucleotide, PF-3512676, in combination with first-line taxane plus platinum chemotherapy for advanced-stage non-small-cell lung cancer. J Clin Oncol 2008;26:3979-86.
28. Weber J, Thompson JA, Hamid O, Minor D, Amin A, Ron I, et al. A randomized, double-blind, placebo-controlled, phase II study comparing the tolerability and efficacy of ipilimumab administered with or without prophylactic budesonide in patients with unresectable stage III or IV melanoma. Clin Cancer Res 2009;15:5591-8.
29. Leonard JP, Link BK, Emmanouilides C, Gregory SA, Weisdorf D, Andrey J, et al. Phase I trial of toll-like receptor 9 agonist PF-3512676 with and following rituximab in patients with recurrent indolent and aggressive non Hodgkin's lymphoma. Clin Cancer Res 2007;13:6168-74. (Pubitemid 350075077)
30. Link BK, Ballas ZK, Weisdorf D, Wooldridge JE, Bossler AD, Shannon M, et al. Oligodeoxynucleotide CpG 7909 delivered as intravenous infusion demonstrates immunologic modulation in patients with previously treated non-Hodgkin lymphoma. J Immunother 2006;29:558-68. (Pubitemid 44395280)
31. Hoene V, Peiser M, Wanner R. Human monocyte-derived dendritic cells express TLR9 and react directly to the CpG-A oligonucleotide D19. J Leukoc Biol 2006;80:1328-36. (Pubitemid 44904971)
32. Hellman P, Eriksson H. Early activation markers of human peripheral dendritic cells. Hum Immunol 2007;68:324-33. (Pubitemid 46616974)
33. Mao TK, Lian ZX, Selmi C, Ichiki Y, Ashwood P, Ansari AA, et al. Altered monocyte responses to defined TLR ligands in patients with primary biliary cirrhosis. Hepatology 2005;42:802-8. (Pubitemid 41401117)
34. Chen W, Chan AS, Dawson AJ, Liang X, Blazar BR, Miller JS. FLT3 ligand administration after hematopoietic cell transplantation increases circulating dendritic cell precursors that can be activated by CpG oligodeoxynucleotides to enhance T-cell and natural killer cell function. Biol Blood Marrow Transplant 2005;11:23-34. (Pubitemid 40057990)