Monocyte-derived dendritic cells are essential for CD8+ T cell activation and antitumor responses after local immunotherapy

Frontiers in Immunology

Volumn 6, Issue NOV, 2015, Pages

  Kuhn, Sabine ^a,b   Yang, Jianping ^a   Ronchese, Franca ^a  

^a MALAGHAN INSTITUTE OF MEDICAL RESEARCH   (New Zealand)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

CSF1R; Dendritic cells; Monocyte derived dendritic cells; Mouse models; T cells; Tumor immunotherapy

Indexed keywords

ALPHA2 INTEGRIN; CD11B ANTIGEN; CD135 ANTIGEN; CD19 ANTIBODY; CD24 ANTIGEN; CD4 ANTIBODY; CD45 ANTIGEN; CD64 ANTIGEN; CD8ALPHA ANTIGEN; CHEMOKINE RECEPTOR CCR2; DEOXYRIBONUCLEASE I; DIPHTHERIA TOXIN; GLYCOPROTEIN P 15095; INTERLEUKIN 12P40; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE SYNTHASE INHIBITOR; THY 1 ANTIGEN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CELL SIGNALING ASSAY; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; MAJOR HISTOCOMPATIBILITY COMPLEX; MONOCYTE; MOUSE; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; TUMOR CELL LINE;

EID: 84949563642     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00584     Document Type: Article

References (55)

1. Ataera H, Hyde E, Price KM, Stoitzner P, Ronchese F. Murine melanoma-infiltrating dendritic cells are defective in antigen presenting function regardless of the presence of CD4CD25 regulatory T cells. PLoS One (2011) 6:e17515. doi:10.1371/journal.pone.0017515.
2. Stoitzner P, Green LK, Jung JY, Price KM, Atarea H, Kivell B, et al. Inefficient presentation of tumor-derived antigen by tumor-infiltrating dendritic cells. Cancer Immunol Immunother (2008) 57:1665-73. doi:10.1007/s00262-008-0487-4.
3. Stumbles PA, Himbeck R, Frelinger JA, Collins EJ, Lake RA, Robinson BW. Cutting edge: tumor-specific CTL are constitutively cross-armed in draining lymph nodes and transiently disseminate to mediate tumor regression following systemic CD40 activation. J Immunol (2004) 173:5923-8. doi:10.4049/jimmunol.173.10.5923.
4. Broz ML, Binnewies M, Boldajipour B, Nelson AE, Pollack JL, Erle DJ, et al. Dissecting the tumor myeloid compartment reveals rare activating antigen-presenting cells critical for T cell immunity. Cancer Cell (2014) 26:638-52. doi:10.1016/j.ccell.2014.09.007.
5. Movassagh M, Spatz A, Davoust J, Lebecque S, Romero P, Pittet M, et al. Selective accumulation of mature DC-Lamp+ dendritic cells in tumor sites is associated with efficient T-cell-mediated antitumor response and control of metastatic dissemination in melanoma. Cancer Res (2004) 64:2192-8. doi:10.1158/0008-5472.CAN-03-2969.
6. Aranda F, Vacchelli E, Obrist F, Eggermont A, Galon J, Sautes-Fridman C, et al. Trial watch: toll-like receptor agonists in oncological indications. Oncoimmunology (2014) 3:e29179. doi:10.4161/onci.29179.
7. Broomfield SA, van der Most RG, Prosser AC, Mahendran S, Tovey MG, Smyth MJ, et al. Locally administered TLR7 agonists drive systemic antitumor immune responses that are enhanced by anti-CD40 immunotherapy. J Immunol (2009) 182:5217-24. doi:10.4049/jimmunol.0803826.
8. Kawarada Y, Ganss R, Garbi N, Sacher T, Arnold B, Hammerling GJ. NK-and CD8(+) T cell-mediated eradication of established tumors by peritumoral injection of CpG-containing oligodeoxynucleotides. J Immunol (2001) 167:5247-53. doi:10.4049/jimmunol.167.9.5247.
9. Kuhn S, Hyde EJ, Yang J, Rich FJ, Harper JL, Kirman JR, et al. Increased numbers of monocyte-derived dendritic cells during successful tumor immunotherapy with immune-activating agents. J Immunol (2013) 191:1984-92. doi:10.4049/jimmunol.1301135.
10. Vicari AP, Chiodoni C, Vaure C, Ait-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. doi:10.1084/jem.20020732.
11. Kuhn S, Yang J, Hyde E, Harper JL, Kirman JR, Ronchese F. IL-1βR-dependent priming of anti-tumor CD4 T cells and sustained anti-tumor immunity after peri-tumoral treatment with MSU and mycobacteria. Oncoimmunology (2015) 4:e1042199. doi:10.1080/2162402X.2015.1042199.
12. Rich FJ, Kuhn S, Hyde EJ, Harper JL, Ronchese F, Kirman JR. Induction of T cell responses and recruitment of an inflammatory dendritic cell subset following tumor immunotherapy with Mycobacterium smegmatis. Cancer Immunol Immunother (2012) 61:2333-42. doi:10.1007/s00262-012-1291-8.
13. Serbina NV, Salazar-Mather TP, Biron CA, Kuziel WA, Pamer EG. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity (2003) 19:59-70. doi:10.1016/S1074-7613(03)00171-7.
14. Le Borgne M, Etchart N, Goubier A, Lira SA, Sirard JC, van Rooijen N, et al. Dendritic cells rapidly recruited into epithelial tissues via CCR6/CCL20 are responsible for CD8+ T cell crosspriming in vivo. Immunity (2006) 24:191-201. doi:10.1016/j.immuni.2006.01.005.
15. León B, López-Bravo M, Ardavín C. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity (2007) 26:519-31. doi:10.1016/j.immuni.2007.01.017.
16. Rosas M, Thomas B, Stacey M, Gordon S, Taylor PR. The myeloid 7/4-antigen defines recently generated inflammatory macrophages and is synonymous with Ly-6B. J Leukoc Biol (2010) 88:169-80. doi:10.1189/jlb.0809548.
17. Plantinga M, Guilliams M, Vanheerswynghels M, Deswarte K, Branco-Madeira F, Toussaint W, et al. Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity (2013) 38:322-35. doi:10.1016/j.immuni.2012.10.016.
18. Goldszmid RS, Caspar P, Rivollier A, White S, Dzutsev A, Hieny S, et al. NK cell-derived interferon-γ orchestrates cellular dynamics and the differentiation of monocytes into dendritic cells at the site of infection. Immunity (2012) 36:1047-59. doi:10.1016/j.immuni.2012.03.026.
19. Nakano H, Lin KL, Yanagita M, Charbonneau C, Cook DN, Kakiuchi T, et al. Blood-derived inflammatory dendritic cells in lymph nodes stimulate acute T helper type 1 immune responses. Nat Immunol (2009) 10:394-402. doi:10.1038/ni.1707.
20. Braumüller H, Wieder T, Brenner E, Aßmann S, Hahn M, Alkhaled M, et al. T-helper-1-cell cytokines drive cancer into senescence. Nature (2013) 494:361-5. doi:10.1038/nature11824.
21. Ruffell B, Chang-Strachan D, Chan V, Rosenbusch A, Ho CMT, Pryer N, et al. Macrophage IL-10 blocks CD8(+) T cell-dependent responses to chemotherapy by suppressing IL-12 expression in intratumoral dendritic cells. Cancer Cell (2014) 26:623-37. doi:10.1016/j.ccell.2014.09.006.
22. Movahedi K, Laoui D, Gysemans C, Baeten M, Stangé G, Van den Bossche J, et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res (2010) 70:5728-39. doi:10.1158/0008-5472.CAN-09-4672.
23. Qian B-Z, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature (2011) 475:222-5. doi:10.1038/nature10138.
24. Franklin RA, Liao W, Sarkar A, Kim MV, Bivona MR, Liu K, et al. The cellular and molecular origin of tumor-associated macrophages. Science (2014) 344:921-5. doi:10.1126/science.1252510.
25. Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity (2014) 41:49-61. doi:10.1016/j.immuni.2014.06.010.
26. Khaled YS, Ammori BJ, Elkord E. Myeloid-derived suppressor cells in cancer: recent progress and prospects. Immunol Cell Biol (2013) 91:493-502. doi:10.1038/icb.2013.29.
27. Pommier A, Audemard A, Durand A, Lengagne R, Delpoux A, Martin B, et al. Inflammatory monocytes are potent antitumor effectors controlled by regulatory CD4+ T cells. Proc Natl Acad Sci U S A (2013) 110:13085-90. doi:10.1073/pnas.1300314110.
28. 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. doi:10.1084/jem.20070021.
29. Ma Y, Adjemian S, Mattarollo SR, Yamazaki T, Aymeric L, Yang H, et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity (2013) 38:729-41. doi:10.1016/j.immuni.2013.03.003.
30. Ma Y, Mattarollo SR, Adjemian S, Yang H, Aymeric L, Hannani D, et al. CCL2/CCR2-dependent recruitment of functional antigen-presenting cells into tumors upon chemotherapy. Cancer Res (2014) 74:436-45. doi:10.1158/0008-5472.CAN-13-1265.
31. Lugade AA, Moran JP, Gerber SA, Rose RC, Frelinger JG, Lord EM. Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J Immunol (2005) 174:7516-23. doi:10.4049/jimmunol.174.12.7516.
32. Ma JZ-I, Lim SN, Qin JS, Yang J, Enomoto N, Ruedl C, et al. Murine CD4+ T cell responses are inhibited by cytotoxic T cell-mediated killing of dendritic cells and are restored by antigen transfer. PLoS One (2012) 7:e37481. doi:10.1371/journal.pone.0037481.
33. Conway JG, McDonald B, Parham J, Keith B, Rusnak DW, Shaw E, et al. Inhibition of colony-stimulating-factor-1 signaling in vivo with the orally bioavailable cFMS kinase inhibitor GW2580. Proc Natl Acad Sci U S A (2005) 102:16078-83. doi:10.1073/pnas.0502000102.
34. Serbina NV, Pamer EG. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol (2006) 7:311-7. doi:10.1038/ni1309.
35. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity (2003) 19:71-82. doi:10.1016/S1074-7613(03)00174-2.
36. Getts DR, Terry RL, Getts MT, Müller M, Rana S, Shrestha B, et al. Ly6c+ "inflammatory monocytes" are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J Exp Med (2008) 205:2319-37. doi:10.1084/jem.20080421.
37. Mitchem JB, Brennan DJ, KnolhoffBL, Belt BA, Zhu Y, Sanford DE, et al. Targeting tumor-infiltrating macrophages decreases tumor-initiating cells, relieves immunosuppression, and improves chemotherapeutic responses. Cancer Res (2013) 73:1128-41. doi:10.1158/0008-5472.CAN-12-2731.
38. Segura E, Albiston AL, Wicks IP, Chai SY, Villadangos JA. Different cross-presentation pathways in steady-state and inflammatory dendritic cells. Proc Natl Acad Sci U S A (2009) 106:20377-81. doi:10.1073/pnas.0910295106.
39. Cheong C, Matos I, Choi JH, Dandamudi DB, Shrestha E, Longhi MP, et al. Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell (2010) 143:416-29. doi:10.1016/j.cell.2010.09.039.
40. Greter M, Helft J, Chow A, Hashimoto D, Mortha A, Agudo-Cantero J, et al. GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity (2012) 36:1031-46. doi:10.1016/j.immuni.2012.03.027.
41. Shime H, Matsumoto M, Oshiumi H, Tanaka S, Nakane A, Iwakura Y, et al. Toll-like receptor 3 signaling converts tumor-supporting myeloid cells to tumoricidal effectors. Proc Natl Acad Sci U S A (2012) 109:2066-71. doi:10.1073/pnas.1113099109.
42. Singer K, Gottfried E, Kreutz M, Mackensen A. Suppression of T-cell responses by tumor metabolites. Cancer Immunol Immunother (2011) 60:425-31. doi:10.1007/s00262-010-0967-1.
43. Chang CI, Liao JC, Kuo L. Macrophage arginase promotes tumor cell growth and suppresses nitric oxide-mediated tumor cytotoxicity. Cancer Res (2001) 61:1100-6.
44. Brantley EC, Guo L, Zhang C, Lin Q, Yokoi K, Langley RR, et al. Nitric oxide-mediated tumoricidal activity of murine microglial cells. Transl Oncol (2010) 3:380-8. doi:10.1593/tlo.10208.
45. Miguel RDV, Cherpes TL, Watson LJ, McKenna KC. CTL induction of tumoricidal nitric oxide production by intratumoral macrophages is critical for tumor elimination. J Immunol (2010) 185:6706-18. doi:10.4049/jimmunol.0903411.
46. Priceman SJ, Sung JL, Shaposhnik Z, Burton JB, Torres-Collado AX, Moughon DL, et al. Targeting distinct tumor-infiltrating myeloid cells by inhibiting CSF-1 receptor: combating tumor evasion of antiangiogenic therapy. Blood (2010) 115:1461-71. doi:10.1182/blood-2009-08-237412.
47. Ries CH, Cannarile MA, Hoves S, Benz J, Wartha K, Runza V, et al. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell (2014) 25:846-59. doi:10.1016/j.ccr.2014.05.016.
48. Xu J, Escamilla J, Mok S, David J, Priceman S, West B, et al. CSF1R signaling blockade stanches tumor-infiltrating myeloid cells and improves the efficacy of radiotherapy in prostate cancer. Cancer Res (2013) 73:2782-94. doi:10.1158/0008-5472.CAN-12-3981.
49. MacDonald KPA, Palmer JS, Cronau S, Seppanen E, Olver S, Raffelt NC, et al. An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue-and tumor-associated macrophages but does not inhibit inflammation. Blood (2010) 116:3955-63. doi:10.1182/blood-2010-02-266296.
50. Li M, Knight DA, A Snyder L. A role for CCL2 in both tumor progression and immunosurveillance. Oncoimmunology (2013) 2:e25474. doi:10.4161/onci.25474.
51. van der Sluis TC, Sluijter M, van Duikeren S, West BL, Melief CJ, Arens R, et al. Therapeutic peptide vaccine-induced CD8 T cells strongly modulate intratumoral macrophages required for tumor regression. Cancer Immunol Res (2015) 3:1042-51. doi:10.1158/2326-6066.CIR-15-0052.
52. Beck AH, Espinosa I, Edris B, Li R, Montgomery K, Zhu S, et al. The macrophage colony-stimulating factor 1 response signature in breast carcinoma. Clin Cancer Res (2009) 15:778-87. doi:10.1158/1078-0432.CCR-08-1283.
53. Ohri CM, Shikotra A, Green RH, Waller DA, Bradding P. Macrophages within NSCLC tumour islets are predominantly of a cytotoxic M1 phenotype associated with extended survival. Eur Respir J (2009) 33:118-26. doi:10.1183/09031936.00065708.
54. Qian B-Z, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell (2010) 141:39-51. doi:10.1016/j.cell.2010.03.014.
55. Kerkar SP, Goldszmid RS, Muranski P, Chinnasamy D, Yu Z, Reger RN, et al. IL-12 triggers a programmatic change in dysfunctional myeloid-derived cells within mouse tumors. J Clin Invest (2011) 121:4746-57. doi:10.1172/JCI58814