Systemic cancer therapy with a small molecule agonist of toll-like receptor 7 can be improved by circumventing TLR tolerance

Cancer Research

Volumn 71, Issue 15, 2011, Pages 5123-5133

  Bourquin, Carole ^a,b,c   Hotz, Christian ^a,b   Noerenberg, Daniel ^a   Voelkl, Andreas ^a   Heidegger, Simon ^a   Roetzer, Laurin C ^a   Storch, Bettina ^a   Sandholzer, Nadja ^a   Wurzenberger, Cornelia ^a   Anz, David ^a   Endres, Stefan ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF FRIBOURG   (Switzerland)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 6; RESIQUIMOD; TOLL LIKE RECEPTOR 7;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CELL POPULATION; COLON CARCINOMA; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; DRUG ADMINISTRATION ROUTE; DRUG EFFICACY; FEMALE; IMMUNOLOGICAL TOLERANCE; IMMUNOSTIMULATION; MOUSE; MYELOID DENDRITIC CELL; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; SINGLE DRUG DOSE;

ANIMALS; CARCINOMA; CELLS, CULTURED; COLONIC NEOPLASMS; CYTOKINES; DENDRITIC CELLS; DRUG SCREENING ASSAYS, ANTITUMOR; FEMALE; IMIDAZOLES; IMMUNE TOLERANCE; INTERFERON-ALPHA; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; INTERLEUKIN-12; INTERLEUKIN-6; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; TOLL-LIKE RECEPTOR 7; TUMOR ESCAPE;

EID: 79960956913     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-3903     Document Type: Article

References (45)

1. Medzhitov R, Janeway CA Jr. Innate immunity:the virtues of a nonclonal system of recognition. Cell 1997;91:295-8. (Pubitemid 27467959)
2. Iwasaki A, Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science 2010;327:291-5.
3. Peris K, Campione E, Micantonio T, Marulli GC, Fargnoli MC, Chimenti S. Imiquimod treatment of superficial and nodular basal cell carcinoma:12-week open-label trial. Dermatol Surg 2005;31:318-23. (Pubitemid 43072987)
4. Fleming CJ, Bryden AM, Evans A, Dawe RS, Ibbotson SH. A pilot study of treatment of lentigo maligna with 5% imiquimod cream. Br J Dermatol 2004;151:485-8. (Pubitemid 39215164)
5. Korman N, Moy R, Ling M, Matheson R, Smith S, McKane S, et al. Dosing with 5% imiquimod cream 3 times per week for the treatment of actinic keratosis:results of two phase 3, randomized, double-blind, parallel-group, vehicle-controlled trials. Arch Dermatol 2005;141:467-73. (Pubitemid 40547405)
6. Hemmi H, Kaisho T, Takeuchi O, Sato S, Sanjo H, Hoshino K, et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 2002;3:196-200. (Pubitemid 34141451)
7. Uematsu S, Sato S, Yamamoto M, Hirotani T, Kato H, Takeshita F, et al. Interleukin-1 receptor-associated kinase-1 plays an essential role for Toll-like receptor (TLR)7-and TLR9-mediated interferon-{alpha} induction. J Exp Med 2005;201:915-23. (Pubitemid 40524461)
8. Dudek AZ, Yunis C, Harrison LI, Kumar S, Hawkinson R, Cooley S, et al. First in human phase I trial of 852A, a novel systemic toll-like receptor 7 agonist, to activate innate immune responses in patients with advanced cancer. Clin Cancer Res 2007;13:7119-25. (Pubitemid 350276897)
9. Dummer R, Hauschild A, Becker JC, Grob JJ, Schadendorf D, Tebbs V, et al. An exploratory study of systemic administration of the toll-like receptor-7 agonist 852A in patients with refractory metastatic melanoma. Clin Cancer Res 2008;14:856-64. (Pubitemid 351231170)
10. Geller MA, Cooley S, Argenta PA, Downs LS, Carson LF, Judson PL, et al. Toll-like receptor-7 agonist administered subcutaneously in a prolonged dosing schedule in heavily pretreated recurrent breast, ovarian, and cervix cancers. Cancer Immunol Immunother 2010;59:1877-84.
11. Greisman SE, Young EJ, Workman JB, Ollodart RM, Hornick RB. Mechanisms of endotoxin tolerance. The role of the spleen. J Clin Invest 1975;56:1597-607.
12. Geisel J, Kahl F, Müller M, Wagner H, Kirschning CJ, Autenrieth IB, et al. IL-6 and maturation govern TLR2 and TLR4 induced TLR agonist tolerance and cross-tolerance in dendritic cells. J Immunol 2007;179:5811-8.
13. Broad A, Kirby JA, Jones DE. Toll-like receptor interactions:tolerance of MyD88-dependent cytokines but enhancement of MyD88-independent interferon-beta production. Immunology 2007;120:103-11.
14. Hayashi E, Kuramitsu Y, Fujimoto M, Zhang X, Tanaka T, Uchida K, et al. Prevention of autoimmune disease by induction of tolerance to Toll-like receptor 7. Proc Natl Acad Sci U S A 2009;106:2764-9.
15. Tsukada K, Kitazawa T, Fukushima A, Okugawa S, Yanagimoto S, Tatsuno K, et al. Macrophage tolerance induced by stimulation with Toll-like receptor 7/8 ligands. Immunol Lett 2007;111:51-6. (Pubitemid 47017477)
16. Vasilakos JP, Smith RM, Gibson SJ, Lindh JM, Pederson LK, Reiter MJ, et al. Adjuvant activities of immune response modifier R-848: comparison with CpG ODN. Cell Immunol 2000;204:64-74.
17. Ito T, Amakawa R, Kaisho T, Hemmi H, Tajima K, Uehira K, et al. Interferon-alpha and interleukin-12 are induced differentially by Toll-like receptor 7 ligands in human blood dendritic cell subsets. J Exp Med 2002;195:1507-12. (Pubitemid 34602828)
18. Lehner MD, Morath S, Michelsen KS, Schumann RR, Hartung T. Induction of cross-tolerance by lipopolysaccharide and highly purified lipoteichoic acid via different Toll-like receptors independent of paracrine mediators. J Immunol 2001;166:5161-7. (Pubitemid 32280731)
19. Sato S, Takeuchi O, Fujita T, Tomizawa H, Takeda K, Akira S. A variety of microbial components induce tolerance to lipopolysaccharide by differentially affecting MyD88-dependent and -independent pathways. Int Immunol 2002;14:783-91. (Pubitemid 34814639)
20. Westin SN, Sun CC, Lu KH, Schmeler KM, Soliman PT, Lacour RA, et al. Treatment failure of a TLR-7 agonist occurs due to self-regulation of acute inflammation and can be overcome by IL-10 blockade. J Immunol 2010;184:5360-7.
21. Vicari AP, Chiodoni C, Vaure C, Aït-Yahia S, Dercamp C, Matsos F, et al. Reversal of tumor-induced dendritic cell paralysis by CpG immunostimulatory oligonucleotide and anti-interleukin 10 receptor antibody. J Exp Med 2002;196:541-9.
22. Phipps-Yonas H, Seto J, Sealfon SC, Moran TM, Fernandez-Sesma A. Interferon-beta pretreatment of conventional and plasmacytoid human dendritic cells enhances their activation by influenza virus. PLoS Pathog 2008;4:e1000193.
23. Heckelsmiller K, Beck S, Rall K, Sipos B, Schlamp A, Tuma E, et al. Combined dendritic cell-and CpG oligonucleotide-based immune therapy cures large murine tumors that resist chemotherapy. Eur J Immunol 2002;32:3235-45. (Pubitemid 35414881)
24. Wurzenberger C, Koelzer VH, Schreiber S, Anz D, Vollmar AM, Schnurr M, et al. Short-term activation induces multifunctional dendritic cells that generate potent antitumor T-cell responses in vivo. Cancer Immunol Immunother 2009;58:901-13.
25. Palucka K, Ueno H, Zurawski G, Fay J, Banchereau J. Building on dendritic cell subsets to improve cancer vaccines. Curr Opin Immunol 2010;22:258-63.
26. Yanagawa Y, Onoe K. Enhanced IL-10 production by TLR4-and TLR2-primed dendritic cells upon TLR restimulation. J Immunol 2007;178:6173-80. (Pubitemid 46717399)
27. Snijders A, Hilkens CM, van der Pouw Kraan TC, Engel M, Aarden LA, Kapsenberg ML. Regulation of bioactive IL-12 production in lipopolysaccharide- stimulated human monocytes is determined by the expression of the p35 subunit. J Immunol 1996;156:1207-12. (Pubitemid 26048118)
28. Kalinski P, Hilkens CM, Snijders A, Snijdewint FG, Kapsenberg ML. IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells. J Immunol 1997;159:28-35. (Pubitemid 127493681)
29. Kalinski P, Vieira PL, Schuitemaker JH, de Jong EC, Kapsenberg ML. Prostaglandin E(2) is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood 2001;97:3466-9.
30. de Vos AF, Pater JM, van den Pangaart PS, de Kruif MD, van 't Veer C, van der Poll T. In vivo lipopolysaccharide exposure of human blood leukocytes induces cross-tolerance to multiple TLR ligands. J Immunol 2009;183:533-42.
31. Rosenberg SA. Progress in human tumour immunology and immunotherapy. Nature 2001;411:380-4. (Pubitemid 32467048)
32. Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nat Rev Immunol 2006;6:836-48. (Pubitemid 44631652)
33. Stary G, Bangert C, Tauber M, Strohal R, Kopp T, Stingl G. Tumoricidal activity of TLR7/8-activated inflammatory dendritic cells. J Exp Med 2007;204:1441-51. (Pubitemid 46919881)
34. Schön M, Bong AB, Drewniok C, Herz J, Geilen CC, Reifenberger J, et al. Tumor-selective induction of apoptosis and the small-molecule immune response modifier imiquimod. J Natl Cancer Inst 2003;95:1138-49. (Pubitemid 37045392)
35. Smith EB, Schwartz M, Kawamoto H, You X, Hwang D, Liu H, et al. Antitumor effects of imidazoquinolines in urothelial cell carcinoma of the bladder. J Urol 2007;177:2347-51. (Pubitemid 46726385)
36. Wolf IH, Kodama K, Cerroni L, Kerl H. Nature of inflammatory infiltrate in superficial cutaneous malignancies during topical imiquimod treatment. Am J Dermatopathol 2007;29:237-41. (Pubitemid 46801921)
37. Harrison LI, Skinner SL, Marbury TC, Owens ML, Kurup S, McKane S, et al. Pharmacokinetics and safety of imiquimod 5% cream in the treatment of actinic keratoses of the face, scalp, or hands and arms. Arch Dermatol Res 2004;296:6-11. (Pubitemid 38828417)
38. Kulp J, Levy S, Fein MC, Adams M, Furst J, Meng TC. Pharmacokinetics of imiquimod 3.75% cream applied daily for 3 weeks to actinic keratoses on the face and/or balding scalp. Arch Dermatol Res 2010;302:539-44.
39. Urosevic M, Dummer R, Conrad C, Beyeler M, Laine E, Burg G, et al. Disease-independent skin recruitment and activation of plasmacytoid predendritic cells following imiquimod treatment. J Natl Cancer Inst 2005;97:1143-53. (Pubitemid 41511214)
40. Arany I, Tyring SK, Stanley MA, Tomai MA, Miller RL, Smith MH, et al. Enhancement of the innate and cellular immune response in patients with genital warts treated with topical imiquimod cream 5%. Antiviral Res 1999;43:55-63. (Pubitemid 29361501)
41. Bourquin C, Schmidt L, Hornung V, Wurzenberger C, Anz D, Sandholzer N, et al. Immunostimulatory RNA oligonucleotides trigger an antigen-specific cytotoxic T-cell and IgG2a response. Blood 2007;109:2953-60. (Pubitemid 46482093)
42. Bourquin C, Wurzenberger C, Heidegger S, Fuchs S, Anz D, Weigel S, et al. Delivery of immunostimulatory RNA oligonucleotides by gelatin nanoparticles triggers an efficient antitumoral response. J Immunother 2010;33:935-44.
43. Butchar JP, Mehta P, Justiniano SE, Guenterberg KD, Kondadasula SV, Mo X, et al. Reciprocal regulation of activating and inhibitory Fc{gamma} receptors by TLR7/8 activation: implications for tumor immunotherapy. Clin Cancer Res 2010;16:2065-75.
44. Bourquin C, Schmidt L, Lanz AL, Storch B, Wurzenberger C, Anz D, et al. Immunostimulatory RNA oligonucleotides induce an effective antitumoral NK cell response through the TLR7. J Immunol 2009;183:6078-86.
45. Anz D, Koelzer VH, Moder S, Thaler R, Schwerd T, Lahl K, et al. Immunostimulatory RNA blocks suppression by regulatory T cells. J Immunol 2010;184:939-46.