Tumor promotion by intratumoral plasmacytoid dendritic cells is reversed by TLR7 ligand treatment

Cancer Research

Volumn 73, Issue 15, 2013, Pages 4629-4640

  Le Mercier, Isabelle ^a,b   Poujol, Dominique ^a,b,c   Sanlaville, Amelien ^a,b   Sisirak, Vanja ^a,b   Gobert, Michael ^a,b   Durand, Isabelle ^a,b,c   Dubois, Bertrand ^b,d   Treilleux, Isabelle ^c   Marvel, Jacqueline ^b,d   Vlach, Jaromir ^f   Blay, Jean Yves ^a,b,c,e   Bendriss, Nathalie Vermare ^a,b   Caux, Christophe ^a,b,c,e   Puisieux, Isabelle ^a,b,c   Goutagny, Nadege ^a,b,c,e  

^a CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

^c CENTRE LÉON BÉRARD   (France)

^d INSERM   (France)

^e LabEx DEVweCAN   (France)

^f Serono International SA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR 2; INTERFERON; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 7 LIGAND; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DEPLETION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT;

ANIMALS; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; LIGANDS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE TEST, MIXED; LYMPHOCYTES, TUMOR-INFILTRATING; MAMMARY NEOPLASMS, EXPERIMENTAL; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; T-LYMPHOCYTES, REGULATORY; TOLL-LIKE RECEPTOR 7;

EID: 84881401720     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-3058     Document Type: Article

References (47)

1. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 2006; 6:24-37.
2. Fricke I, Gabrilovich DI. Dendritic cells and tumor microenvironment: a dangerous liaison. Immunol Invest 2006;35:459-83.
3. Drobits B, Holcmann M, Amberg N, Swiecki M, Grundtner R, Hammer M, et al. Imiquimod clears tumors in mice independent of adaptive immunity by converting pDCs into tumor-killing effector cells. J Clin Invest 2012;122:575-85.
4. Liu C, Lou Y, Lizee G, Qin H, Liu S, Rabinovich B, et al. Plasmacytoid dendritic cells induce NK cell-dependent, tumor antigen-specific T cell cross-priming and tumor regression in mice. J Clin Invest 2008;118: 1165-75.
5. Kadowaki N, Antonenko S, Lau JY, Liu YJ. Natural interferon alpha/ beta-producing cells link innate and adaptive immunity. J Exp Med 2000;192:219-26.
6. Colonna M, Trinchieri G, Liu YJ. Plasmacytoid dendritic cells in immunity. Nat Immunol 2004;5:1219-26.
7. Gilliet M, Cao W, Liu YJ. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol 2008;8:594-606.
8. Kawai T, Sato S, Ishii KJ, Coban C, Hemmi H, Yamamoto M, et al. Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat Immunol 2004;5:1061-8.
9. Fonteneau JF, Gilliet M, Larsson M, Dasilva I, Munz C, Liu YJ, et al. Activation of influenza virus-specific CD4+ and CD8+ T cells: a new role for plasmacytoid dendritic cells in adaptive immunity. Blood 2003;101:3520-6.
10. Blanco P, Palucka AK, Gill M, Pascual V, Banchereau J. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science 2001;294:1540-3.
11. de Heer HJ, Hammad H, Soullie T, Hijdra D, Vos N, Willart MA, et al. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J Exp Med 2004;200: 89-98.
12. Goubier A, Dubois B, Gheit H, Joubert G, Villard-Truc F, Asselin- Paturel C, et al. Plasmacytoid dendritic cells mediate oral tolerance. Immunity 2008;29:464-75.
13. Fugier-Vivier IJ, Rezzoug F, Huang Y, Graul-Layman AJ, Schanie CL, Xu H, et al. Plasmacytoid precursor dendritic cells facilitate allogeneic hematopoietic stem cell engraftment. J Exp Med 2005;201: 373-83.
14. Wei S, Kryczek I, Zou L, Daniel B, Cheng P, Mottram P, et al. Plasmacytoid dendritic cells induce CD8+ regulatory T cells in human ovarian carcinoma. Cancer Res 2005;65:5020-6.
15. Treilleux I, Blay JY, Bendriss-Vermare N, Ray-Coquard I, Bachelot T, Guastalla JP, et al. Dendritic cell infiltration and prognosis of early stage breast cancer. Clin Cancer Res 2004;10:7466-74.
16. Vermi W, Bonecchi R, Facchetti F, Bianchi D, Sozzani S, Festa S, et al. Recruitment of immature plasmacytoid dendritic cells (plasmacytoid monocytes) and myeloid dendritic cells in primary cutaneous melanomas. J Pathol 2003;200:255-68.
17. Hartmann E, Wollenberg B, Rothenfusser S, Wagner M, Wellisch D, Mack B, et al. Identification and functional analysis of tumor-infiltrating plasmacytoid dendritic cells in head and neck cancer. Cancer Res 2003;63:6478-87.
18. Zou W, Machelon V, Coulomb-L'Hermin A, Borvak J,NomeF, Isaeva T, et al. Stromal-derived factor-1 in human tumors recruits and alters the function of plasmacytoid precursor dendritic cells. Nat Med 2001;7: 1339-46.
19. Labidi-Galy SI, Sisirak V, Meeus P, Gobert M, Treilleux I, Bajard A, et al. Quantitative and functional alterations of plasmacytoid dendritic cells contribute to immune tolerance in ovarian cancer. Cancer Res 2011; 71:5423-34.
20. Sisirak V, Faget J, Gobert M, Goutagny N, Vey N, Treilleux I, et al. Impaired IFN-alpha production by plasmacytoid dendritic cells favors regulatory T-cell expansion that may contribute to breast cancer progression. Cancer Res 2012;72:5188-97.
21. 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.
22. Guy CT, Webster MA, Schaller M, Parsons TJ, Cardiff RD, Muller WJ. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc Natl Acad Sci U S A 1992;89:10578-82.
23. Dharmapuri S, Aurisicchio L, Neuner P, Verdirame M, Ciliberto G, La MN. An oral TLR7 agonist is a potent adjuvant of DNA vaccination in transgenic mouse tumor models. Cancer Gene Ther 2009;16:462-72.
24. Blasius AL, Giurisato E, Cella M, Schreiber RD, Shaw AS, Colonna M. Bone marrow stromal cell antigen 2 is a specific marker of type I IFNproducing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J Immunol 2006;177:3260-5.
25. Asselin-Paturel C, BrizardG, Pin JJ, Briere F, TrinchieriG. Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal antibody. J Immunol 2003;171: 6466-77.
26. Gobert M, Treilleux I, Bendriss-Vermare N, Bachelot T, Goddard-Leon S, Arfi V, et al. Regulatory T cells recruited through CCL22/CCR4 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome. Cancer Res 2009;69: 2000-9.
27. Faget J, Bendriss-Vermare N, Gobert M, Durand I, Olive D, Biota C, et al. ICOS-ligand expression on plasmacytoid dendritic cells supports breast cancer progression by promoting the accumulation of immunosuppressive CD4+ T cells. Cancer Res 2012;72:6130-41.
28. Hirsch I,CauxC, Hasan U, Bendriss-VermareN,OliveD. Impaired Tolllike receptor 7 and 9 signaling: from chronic viral infections to cancer. Trends Immunol 2010;31:391-7.
29. Sisirak V, Vey N, Goutagny N, Renaudineau S, Malfroy M, Thys S, et al. Breast cancer-derived TGF-beta and TNF-alpha compromise IFNalpha production by tumor-associated plasmacytoid dendritic cells. Int J Cancer 2013;133:771-8.
30. Barrat FJ, Meeker T, Gregorio J, Chan JH, Uematsu S, Akira S, et al. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J Exp Med 2005;202:1131-9.
31. Vollmer J, Tluk S, Schmitz C, Hamm S, Jurk M, Forsbach A, et al. Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. J Exp Med 2005;202:1575-85.
32. Ganguly D, Chamilos G, Lande R, Gregorio J, Meller S, Facchinetti V, et al. Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J Exp Med 2009;206: 1983-94.
33. Cisse B, Caton ML, Lehner M, Maeda T, Scheu S, Locksley R, et al. Transcription factor E2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell 2008;135:37-48.
34. Chauhan D, Singh AV, Brahmandam M, Carrasco R, Bandi M, Hideshima T, et al. Functional interaction of plasmacytoid dendritic cells with multiple myeloma cells: a therapeutic target. Cancer Cell 2009;16: 309-23.
35. Sawant A, Hensel JA, Chanda D, Harris BA, Siegal GP, Maheshwari A, et al. Depletion of plasmacytoid dendritic cells inhibits tumor growth and prevents bone metastasis of breast cancer cells. J Immunol 2012;189:4258-65.
36. Wang RF. Regulatory T cells and Toll-like receptors in cancer therapy. Cancer Res 2006;66:4987-90.
37. Kuwana M. Induction of anergic and regulatory T cells by plasmacytoid dendritic cells and other dendritic cell subsets. Hum Immunol 2002;63: 1156-63.
38. Bilsborough J, George TC, Norment A, Viney JL. Mucosal CD8alpha+ DC, with a plasmacytoid phenotype, induce differentiation and support function of T cells with regulatory properties. Immunology 2003;108: 481-92.
39. Ito T, Yang M, Wang YH, Lande R, Gregorio J, Perng OA, et al. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J Exp Med 2007;204:105-15.
40. Gilliet M, Liu YJ. Human plasmacytoid-derived dendritic cells and the induction of T-regulatory cells. Hum Immunol 2002;63:1149-55.
41. Moseman EA, Liang X, Dawson AJ, Panoskaltsis-Mortari A, Krieg AM, Liu YJ, et al. Human plasmacytoid dendritic cells activated by CpG oligodeoxynucleotides induce the generation of CD4+CD25+ regulatory T cells. J Immunol 2004;173:4433-42.
42. Kang HK, Liu M, Datta SK. Low-dose peptide tolerance therapy of lupus generates plasmacytoid dendritic cells that cause expansion of autoantigen-specific regulatory T cells and contraction of inflammatory Th17 cells. J Immunol 2007;178:7849-58.
43. Ouabed A, Hubert FX, Chabannes D, Gautreau L, Heslan M, Josien R. Differential control of T regulatory cell proliferation and suppressive activity by mature plasmacytoid versus conventional spleen dendritic cells. J Immunol 2008;180:5862-70.
44. Sharma MD, Baban B, Chandler P, Hou DY, Singh N, Yagita H, et al. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J Clin Invest 2007;117:2570-82.
45. Guiducci C, Vicari AP, Sangaletti S, Trinchieri G, Colombo MP. Redirecting in vivo elicited tumor infiltrating macrophages and dendritic cells towards tumor rejection. Cancer Res 2005;65: 3437-46.
46. Colombo MP, Mantovani A. Targeting myelomonocytic cells to revert inflammation-dependent cancer promotion. Cancer Res 2005;65: 9113-6.
47. Goutagny N, Estornes Y, Hasan U, Lebecque S, Caux C. Targeting pattern recognition receptors in cancer immunotherapy. Target Oncol 2012;7:29-54.