The tumour microenvironment harbours ontogenically distinct dendritic cell populations with opposing effects on tumour immunity

Nature Communications

Volumn 7, Issue , 2016, Pages

  Laoui, Damya ^a,b   Keirsse, Jiri ^a,b   Morias, Yannick ^a,b   Van Overmeire, Eva ^a,b   Geeraerts, Xenia ^a,b   Elkrim, Yvon ^a,b   Kiss, Mate ^a,b   Bolli, Evangelia ^a,b   Lahmar, Qods ^a,b   Sichien, Dorine ^a,c   Serneels, Jens ^a,d   Scott, Charlotte L ^a,c   Boon, Louis ^e   De Baetselier, Patrick ^a,b   Mazzone, Massimiliano ^a,d   Guilliams, Martin ^a,c   Van Ginderachter, Jo A ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e EPIRUS Biopharmaceuticals Netherlands BV   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERFERON REGULATORY FACTOR 4; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR;

ANTIGEN; CELLS AND CELL COMPONENTS; IMMUNE SYSTEM; IMMUNITY; RODENT; TUMOR; VACCINATION;

ADOPTIVE TRANSFER; ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST TUMOR; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL MIGRATION; COLON CARCINOMA; COLORECTAL CANCER; COMPARATIVE STUDY; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; FIBROSARCOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LEWIS CARCINOMA; LUNG CARCINOMA; LYMPH NODE CELL; MALE; MELANOMA B16; MIDDLE AGED; MIXED LYMPHOCYTE REACTION; MONOCYTE; MOUSE; MULTIPLE CANCER; NON SMALL CELL LUNG CANCER; NONHUMAN; NUCLEAR REPROGRAMMING; ONTOGENY; RECTUM CANCER; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TH17 CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; IMMUNOLOGY; IMMUNOTHERAPY; KNOCKOUT MOUSE; MACROPHAGE; NEOPLASM; PATHOLOGY; PROCEDURES; TRANSGENIC MOUSE; TUMOR CELL LINE;

MUS;

ANIMALS; CELL LINE, TUMOR; CELLS, CULTURED; DENDRITIC CELLS; HUMANS; IMMUNOTHERAPY; MACROPHAGES; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MONOCYTES; NEOPLASMS; T-LYMPHOCYTE SUBSETS; TUMOR MICROENVIRONMENT;

EID: 85007174655     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms13720     Document Type: Article

References (57)

1. Steinman, R. M. & Banchereau, J. Taking dendritic cells into medicine. Nature 449, 419-426 (2007).
2. + T cells. Cancer Res. 74, 705-715 (2014).
3. Fridman, W. H. et al. Prognostic and predictive impact of intra- and peritumoral immune infiltrates. Cancer Res. 71, 5601-5605 (2011).
4. Gabrilovich, D. Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat. Rev. Immunol. 4, 941-952 (2004).
5. Vicari, A. P., Caux, C. & Trinchieri, G. Tumour escape from immune surveillance through dendritic cell inactivation. Semin Cancer Biol. 12, 33-42 (2002).
6. Ma, Y., Shurin, G. V., Gutkin, D. W. & Shurin, M. R. Tumor associated regulatory dendritic cells. Semin. Cancer Biol. 22, 298-306 (2012).
7. Scarlett, U. K. et al. Ovarian cancer progression is controlled by phenotypic changes in dendritic cells. J. Exp. Med. 209, 495-506 (2012).
8. Bennaceur, K. et al. Dendritic cells dysfunction in tumour environment. Cancer Lett. 272, 186-196 (2008).
9. Ma, Y., Aymeric, L., Locher, C., Kroemer, G. & Zitvogel, L. The dendritic cell-tumor cross-talk in cancer. Curr. Opin. Immunol. 23, 146-152 (2011).
10. Ma, Y., Shurin, G. V., Peiyuan, Z. & Shurin, M. R. Dendritic cells in the cancer microenvironment. J. Cancer 4, 36-44 (2013).
11. Helft, J., Ginhoux, F., Bogunovic, M. & Merad, M. Origin and functional heterogeneity of non-lymphoid tissue dendritic cells in mice. Immunol, Rev. 234, 55-75 (2010).
12. Guilliams, M. et al. From skin dendritic cells to a simplified classification of human and mouse dendritic cell subsets. Eur. J. Immunol. 40, 2089-2094 (2010).
13. Plantinga, M. et al. Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 38, 322-335 (2013).
14. Heath, W. R. & Carbone, F. R. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat. Immunol. 10, 1237-1244 (2009).
15. Guilliams, M. et al. Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat. Rev. Immuno. 14, 571-578 (2014).
16. Onai, N. et al. Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat. Immunol. 8, 1207-1216 (2007).
17. Greter, M. et al. GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity 36, 1031-1046 (2012).
18. Serbina, N. V., Jia, T., Hohl, T. M. & Pamer, E. G. Monocyte-mediated defense against microbial pathogens. Ann. Rev. Immunol. 26, 421-452 (2008).
19. Scott, C. L. et al. The transcription factor Zeb2 regulates development of conventional and plasmacytoid DCs by repressing Id2. J. Exp. Med. 213, 897-911 (2016).
20. Merad, M., Sathe, P., Helft, J., Miller, J. & Mortha, A. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 31, 563-604 (2013).
21. Persson, E. K. et al. IRF4 transcription-factor-dependent CD103(+) CD11b(+) dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 38, 958-969 (2013).
22. Gao, Y. et al. Control of T helper 2 responses by transcription factor IRF4-dependent dendritic cells. Immunity 39, 722-732 (2013).
23. + dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38, 970-983 (2013).
24. Broz, M. L. et al. Dissecting the tumor myeloid compartment reveals rare activating antigen-presenting cells critical for T cell immunity. Cancer Cell 26, 638-652 (2014).
25. Movahedi, K. et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 70, 5728-5739 (2010).
26. Laoui, D. et al. Tumor hypoxia does not drive differentiation of tumorassociated macrophages but rather fine-tunes the M2-like macrophage population. Cancer Res 74, 24-30 (2014).
27. Langlet, C. et al. CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J. Immunol. 188, 1751-1760 (2012).
28. Scott, C. L. et al. CCR2(+) CD103(-) intestinal dendritic cells develop from DC-committed precursors and induce interleukin-17 production by T cells. Mucosal Immunol. 8, 327-339 (2015).
29. Kingston, D. et al. The concerted action of GM-CSF and Flt3-ligand on in vivo dendritic cell homeostasis. Blood 114, 835-843 (2009).
30. Tamura, T. et al. IFN regulatory factor-4 and -8 govern dendritic cell subset development and their functional diversity. J. Immunol. 174, 2573-2581 (2005).
31. Gautier, E. L. et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13, 1118-1128 (2012).
32. Remels, L. M. & De Baetselier, P. C. Characterization of 3LL-tumor variants generated by in vitro macrophage-mediated selection. Int. J. Cancer 39, 343-352 (1987).
33. Segura, E. et al. Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity 38, 336-348 (2013).
34. Preynat-Seauve, O. et al. Tumor-infiltrating dendritic cells are potent antigen-presenting cells able to activate T cells and mediate tumor rejection. J. Immunol. 176, 61-67 (2006).
35. Vesely, M. D., Kershaw, M. H., Schreiber, R. D. & Smyth, M. J. Natural innate and adaptive immunity to cancer. Annu. Rev. Immunol. 29, 235-271 (2011).
36. Bronte, V. & Zanovello, P. Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5, 641-654 (2005).
37. + T-cell activation events. Eur. J. Immunol. 43, 2930-2942 (2013).
38. Bosschaerts, T. et al. IL-10 limits production of pathogenic TNF by M1 myeloid cells through induction of nuclear NF-kappaB p50 member in Trypanosoma congolense infection-resistant C57BL/6 mice. Eur. J. Immunol. 41, 3270-3280 (2011).
39. Kissenpfennig, A. et al. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22, 643-654 (2005).
40. Ohl, L. et al. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21, 279-288 (2004).
41. Ghilardi, N. et al. Compromised humoral and delayed-type hypersensitivity responses in IL-23-deficient mice. J. Immunol. 172, 2827-2833 (2004).
42. Van Overmeire, E. et al. M-CSF and GM-CSF receptor signaling differentially regulate monocyte maturation and macrophage polarization in the tumor microenvironment. Cancer Res. 76, 35-42 (2016).
43. Xu, H. et al. Notch-RBP-J signaling regulates the transcription factor IRF8 to promote inflammatory macrophage polarization. Nat. Immunol. 13, 642-650 (2012).
44. Roberts, E. W. et al. Critical role for CD103(+)/CD141(+) dendritic cells bearing CCR7 for tumor antigen trafficking and priming of T cell immunity in melanoma. Cancer Cell 30, 324-336 (2016).
45. Schuler, G., Schuler-Thurner, B. & Steinman, R. M. The use of dendritic cells in cancer immunotherapy. Curr. Opin. Immunol. 15, 138-147 (2003).
46. Palucka, K. & Banchereau, J. Cancer immunotherapy via dendritic cells. Nat. Rev. Cancer 12, 265-277 (2012).
47. Casazza, A. et al. Impeding macrophage entry into hypoxic tumor areas by Sema3A/Nrp1 signaling blockade inhibits angiogenesis and restores antitumor immunity. Cancer Cell 24, 695-709 (2013).
48. Sluijter, M. et al. Inhibition of CSF-1R supports T-cell mediated melanoma therapy. PLoS ONE 9, e104230 (2014).
49. Xu, M. et al. Intratumoral delivery of IL-21 overcomes anti-Her2/Neu resistance through shifting tumor-associated macrophages from M2 to M1 phenotype. J. Immunol. 194, 4997-5006 (2015).
50. Van Overmeire, E. et al. M-CSF and GM-CSF receptor signaling differentially regulate monocyte maturation and macrophage polarization in the tumor microenvironment. Cancer Res. 76, 35-42 (2015).
51. Codarri, L. et al. RORgammat drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 12, 560-567 (2011).
52. El-Behi, M. et al. The encephalitogenicity of T(H)17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF. Nat. Immunol. 12, 568-575 (2011).
53. Salmon, H. et al. Expansion and activation of CD103(+) dendritic cell progenitors at the tumor site enhances tumor responses to therapeutic PD-L1 and BRAF inhibition. Immunity 44, 924-938 (2016).
54. Mac Keon, S., Ruiz, M. S., Gazzaniga, S. & Wainstok, R. Dendritic cell-based vaccination in cancer: therapeutic implications emerging from murine models. Front. Immunol. 6, 243 (2015).
55. Bloy, N. et al. Trial watch: Dendritic cell-based anticancer therapy. Oncoimmunology 3, e963424 (2014).
56. Van Lint, S. et al. Intratumoral delivery of TriMix mRNA results in T-cell activation by cross-presenting dendritic cells. Cancer Immunol. Res. 4, 146-156 (2016).
57. Markov, O. V., Mironova, N. L., Sennikov, S. V., Vlassov, V. V. & Zenkova, M. A. Prophylactic dendritic cell-based vaccines efficiently inhibit metastases in murine metastatic melanoma. PLoS ONE 10, e0136911 (2015).