TLR7-based cancer immunotherapy decreases intratumoral myeloid-derived suppressor cells and blocks their immunosuppressive function

OncoImmunology

Volumn 5, Issue 11, 2016, Pages

  Spinetti, Thibaud ^a   Spagnuolo, Lorenzo ^a   Mottas, Inès ^a,b   Secondini, Chiara ^a   Treinies, Marina ^a   Rüegg, Curzio ^a   Hotz, Christian ^a   Bourquin, Carole ^a,b  

^a University of Fribourg   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Immunotherapy; MDSC; myeloid derived suppressor cells; R848; TLR7

Indexed keywords

B7 ANTIGEN; GLYCOPROTEIN P 15095; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RESIQUIMOD; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE MARROW CELL; CANCER IMMUNOTHERAPY; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; IMMUNE RESPONSE; IN VITRO STUDY; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NEOPLASM; NONHUMAN; PROTEIN EXPRESSION; SUPPRESSOR CELL;

EID: 84994115593     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1230578     Document Type: Article

References (37)

1. Hanahan D, Weinberg RA. Hallmarks of cancer:the next generation. Cell 2011; 144:646-74; PMID:21376230; doi:10.1016/j.cell.2011.02.013
2. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012; 12:253-68; PMID:22437938; doi:10.1038/nri3175
3. Idorn M, Kollgaard T, Kongsted P, Sengelov L, Thor Straten P. Correlation between frequencies of blood monocytic myeloid-derived suppressor cells, regulatory T cells and negative prognostic markers in patients with castration-resistant metastatic prostate cancer. Cancer Immunol Immunother 2014; 63:1177-87; PMID:25085000; doi:10.1007/s00262-014-1591-2
4. Gabrilovich DI, Bronte V, Chen SH, Colombo MP, Ochoa A, Ostrand-Rosenberg S, Schreiber H. The terminology issue for myeloid-derived suppressor cells. Cancer Res 2007; 67:425; PMID:17210725; doi:10.1158/0008-5472.CAN-06-3037
5. Sica A, Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 2007; 117:1155-66; PMID:17476345; doi:10.1172/JCI31422
6. Najjar YG, Finke JH. Clinical perspectives on targeting of myeloid derived suppressor cells in the treatment of cancer. Front Oncol 2013; 3:49; PMID:23508517; doi:10.3389/fonc.2013.00049
7. Hemmi H, Kaisho T, Takeuchi O, Sato S, Sanjo H, Hoshino K, Horiuchi T, Tomizawa H, Takeda K, Akira S. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 2002; 3:196-200; PMID:11812998; doi:10.1038/ni758
8. Kobold S, Wiedemann G, Rothenfusser S, Endres S. Modes of action of TLR7 agonists in cancer therapy. Immunother 2014; 6:1085-95; PMID:25428647; doi:10.2217/imt.14.75
9. Sidky YA, Borden EC, Weeks CE, Reiter MJ, Hatcher JF, Bryan GT. Inhibition of murine tumor growth by an interferon-inducing imidazoquinolinamine. Cancer Res 1992; 52:3528-33; PMID:1377595
10. Bourquin C, Schmidt L, Lanz AL, Storch B, Wurzenberger C, Anz D, Sandholzer N, Mocikat R, Berger M, Poeck H, et al. Immunostimulatory RNA oligonucleotides induce an effective antitumoral NK cell response through the TLR7. J Immunol 2009; 183:6078-86; PMID:19890064; doi:10.4049/jimmunol.0901594
11. Lee M, Park CS, Lee YR, Im SA, Song S, Lee CK. Resiquimod, a TLR7/8 agonist, promotes differentiation of myeloid-derived suppressor cells into macrophages and dendritic cells. Arch Pharm Res 2014; 37:1234-40; PMID:24748512; doi:10.1007/s12272-014-0379-4
12. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008; 181:5791-802; PMID:18832739; doi:10.4049/jimmunol.181.8.5791
13. Dolcetti L, Peranzoni E, Ugel S, Marigo I, Fernandez Gomez A, Mesa C, Geilich M, Winkels G, Traggiai E, Casati A, et al. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur J Immunol 2010; 40:22-35; PMID:19941314; doi:10.1002/eji.200939903
14. Zoglmeier C, Bauer H, Norenberg D, Wedekind G, Bittner P, Sandholzer N, Rapp M, Anz D, Endres S, Bourquin C. CpG blocks immunosuppression by myeloid-derived suppressor cells in tumor-bearing mice. Clin Cancer Res 2011; 17:1765-75; PMID:21233400; doi:10.1158/1078-0432.CCR-10-2672
15. Marigo I, Bosio E, Solito S, Mesa C, Fernandez A, Dolcetti L, Ugel S, Sonda N, Bicciato S, Falisi E, et al. Tumor-induced tolerance and immune suppression depend on the C/EBPbeta transcription factor. Immunity 2010; 32:790-802; PMID:20605485; doi:10.1016/j.immuni.2010.05.010
16. Movahedi K, Guilliams M, Van den Bossche J, Van den Bergh R, Gysemans C, Beschin A, De Baetselier P, Van Ginderachter JA. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008; 111:4233-44; PMID:18272812; doi:10.1182/blood-2007-07-099226
17. Qu P, Yan C, Du H. Matrix metalloproteinase 12 overexpression in myeloid lineage cells plays a key role in modulating myelopoiesis, immune suppression, and lung tumorigenesis. Blood 2011; 117:4476-89; PMID:21378275; doi:10.1182/blood-2010-07-298380
18. Peris K, Campione E, Micantonio T, Clare Marulli G, Concetta Fargnoli M, Chimenti S. Imiquimod treatment of superficial and nodular basal cell carcinoma:12-week open-label trial. Dermatol Surg 2006; 31:318-23; PMID:15841634; doi:10.1111/j.1524-4725.2005.31081
19. Anz D, Koelzer VH, Moder S, Thaler R, Schwerd T, Lahl K, Sparwasser T, Besch R, Poeck H, Hornung V, et al. Immunostimulatory RNA blocks suppression by regulatory T cells. J Immunol 2010; 184:939-46; PMID:19966212; doi:10.4049/jimmunol.0901245
20. Jia W, Jackson-Cook C, Graf MR. Tumor-infiltrating, myeloid-derived suppressor cells inhibit T cell activity by nitric oxide production in an intracranial rat glioma + vaccination model. J Neuroimmunol 2010; 223:20-30; PMID:20452681; doi:10.1016/j.jneuroim.2010.03.011
21. Maenhout SK, Van Lint S, Emeagi PU, Thielemans K, Aerts JL. Enhanced suppressive capacity of tumor-infiltrating myeloid-derived suppressor cells compared with their peripheral counterparts. Int J Cancer 2014; 134:1077-90; PMID:23983191; doi:10.1002/ijc.28449
22. Corzo CA, Condamine T, Lu L, Cotter MJ, Youn JI, Cheng P, Cho HI, Celis E, Quiceno DG, Padhya T, et al. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med 2010; 207:2439-53; PMID:20876310; doi:10.1084/jem.20100587
23. Serafini P, Mgebroff S, Noonan K, Borrello I. Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res 2008; 68:5439-49; PMID:18593947; doi:10.1158/0008-5472.CAN-07-6621
24. Gallina G, Dolcetti L, Serafini P, De Santo C, Marigo I, Colombo MP, Basso G, Brombacher F, Borrello I, Zanovello P, et al. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J Clin Invest 2006; 116:2777-90; PMID:17016559; doi:10.1172/JCI28828
25. Vincent J, Mignot G, Chalmin F, Ladoire S, Bruchard M, Chevriaux A, Martin F, Apetoh L, Rebe C, Ghiringhelli F. 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res 2010; 70:3052-61; PMID:20388795; doi:10.1158/0008-5472.CAN-09-3690
26. Le HK, Graham L, Cha E, Morales JK, Manjili MH, Bear HD. Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice. Int Immunopharmacol 2009; 9:900-9; PMID:19336265; doi:10.1016/j.intimp.2009.03.015
27. Ko JS, Rayman P, Ireland J, Swaidani S, Li G, Bunting KD, Rini B, Finke JH, Cohen PA. Direct and differential suppression of myeloid-derived suppressor cell subsets by sunitinib is compartmentally constrained. Cancer Res 2010; 70:3526-36; PMID:20406969; doi:10.1158/0008-5472.CAN-09-3278
28. Serafini P, Meckel K, Kelso M, Noonan K, Califano J, Koch W, Dolcetti L, Bronte V, Borrello I. Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function. J Exp Med 2006; 203:2691-702; PMID:17101732; doi:10.1084/jem.20061104
29. Fujita M, Kohanbash G, Fellows-Mayle W, Hamilton RL, Komohara Y, Decker SA, Ohlfest JR, Okada H. COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res 2011; 71:2664-74; PMID:21324923; doi:10.1158/0008-5472.CAN-10-3055
30. Nefedova Y, Fishman M, Sherman S, Wang X, Beg AA, Gabrilovich DI. Mechanism of all-trans retinoic acid effect on tumor-associated myeloid-derived suppressor cells. Cancer Res 2007; 67:11021-8; PMID:18006848; doi:10.1158/0008-5472.CAN-07-2593
31. Wang J, Shirota Y, Bayik D, Shirota H, Tross D, Gulley JL, Wood LV, Berzofsky JA, Klinman DM. Effect of TLR agonists on the differentiation and function of human monocytic myeloid-derived suppressor cells. J Immunol 2015; 194:4215-21; PMID:25825448; doi:10.4049/jimmunol.1402004
32. Kumar V, Cheng P, Condamine T, Mony S, Languino LR, McCaffrey JC, Hockstein N, Guarino M, Masters G, Penman E, et al. CD45 phosphatase inhibits STAT3 transcription factor activity in myeloid cells and promotes tumor-associated macrophage differentiation. Immunity 2016; 44:303-15; PMID:26885857; doi:10.1016/j.immuni.2016.01.014
33. Bonizzi G, Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 2004; 25:280-8; PMID:15145317; doi:10.1016/j.it.2004.03.008
34. Larangé A, Antonios D, Pallardy M, Kerdine-Römer S. TLR7 and TLR8 agonists trigger different signaling pathways for human dendritic cell maturation. J Leukoc Biol 2009; 85:673-83; PMID:19164127; doi:10.1189/jlb.0808504
35. Bonapace L, Coissieux MM, Wyckoff J, Mertz KD, Varga Z, Junt T, Bentires-Alj M. Cessation of CCL2 inhibition accelerates breast cancer metastasis by promoting angiogenesis. Nature 2014; 515:130-3; PMID:25337873; doi:10.1038/nature13862
36. Kuonen F, Laurent J, Secondini C, Lorusso G, Stehle JC, Rausch T, Hull EF-vt, Bieler G, Alghisi GC, Schwendener R, et al. Inhibition of the kit ligand/c-kit axis attenuates metastasis in a mouse model mimicking local breast cancer relapse after radiotherapy. Clin Cancer Res 2012; 18:4365-74; PMID:22711708; doi:10.1158/1078-0432.CCR-11-3028
37. Lyons AB, Parish CR. Determination of lymphocyte division by flow cytometry. J Immunol Meth 1994; 171:131-7; PMID:8176234; doi:10.1016/0022-1759(94)90236-4