CD169-Positive Macrophages Dominate Antitumor Immunity by Crosspresenting Dead Cell-Associated Antigens

Immunity

Volumn 34, Issue 1, 2011, Pages 85-95

  Asano, Kenichi ^a   Nabeyama, Ami ^a   Miyake, Yasunobu ^a   Qiu, Chun Hong ^a   Kurita, Ai ^a   Tomura, Michio ^a   Kanagawa, Osami ^a   Fujii, Shin ichiro ^a   Tanaka, Masato ^a  

^a RIKEN Center for Integrative Medical Sciences   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD169 ANTIGEN; GLYCOPROTEIN P 15095; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; RANTES; TUMOR ANTIGEN; TUMOR CELL VACCINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CANCER IMMUNIZATION; CD169 MACROPHAGE; CD8+ T LYMPHOCYTE; CELL DEATH; CONTROLLED STUDY; CROSS PRESENTATION; CYTOKINE PRODUCTION; LYMPH FLOW; LYMPH FOLLICLE; LYMPH NODE; MACROPHAGE; MACROPHAGE MIGRATION; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TUMOR CELL; TUMOR REJECTION;

ANIMALS; ANTIGENS, CD11C; ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CROSS-PRIMING; IMMUNIZATION; LYMPH NODES; LYMPHOCYTE ACTIVATION; LYMPHOMA, T-CELL; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICE, TRANSGENIC; PHAGOCYTOSIS; RECEPTORS, IMMUNOLOGIC;

EID: 78751704362     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2010.12.011     Document Type: Article

References (47)

1. Allan R.S., Waithman J., Bedoui S., Jones C.M., Villadangos J.A., Zhan Y., Lew A.M., Shortman K., Heath W.R., Carbone F.R. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 2006, 25:153-162.
2. Allenspach E.J., Lemos M.P., Porrett P.M., Turka L.A., Laufer T.M. Migratory and lymphoid-resident dendritic cells cooperate to efficiently prime naive CD4 T cells. Immunity 2008, 29:795-806.
3. Angeli V., Faveeuw C., Roye O., Fontaine J., Teissier E., Capron A., Wolowczuk I., Capron M., Trottein F. Role of the parasite-derived prostaglandin D2 in the inhibition of epidermal Langerhans cell migration during schistosomiasis infection. J. Exp. Med. 2001, 193:1135-1147.
4. Apetoh L., Ghiringhelli F., Tesniere A., Obeid M., Ortiz C., Criollo A., Mignot G., Maiuri M.C., Ullrich E., Saulnier P., et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med. 2007, 13:1050-1059.
5. Asano K., Miwa M., Miwa K., Hanayama R., Nagase H., Nagata S., Tanaka M. Masking of phosphatidylserine inhibits apoptotic cell engulfment and induces autoantibody production in mice. J. Exp. Med. 2004, 200:459-467.
6. Bozzacco L., Trumpfheller C., Siegal F.P., Mehandru S., Markowitz M., Carrington M., Nussenzweig M.C., Piperno A.G., Steinman R.M. DEC-205 receptor on dendritic cells mediates presentation of HIV gag protein to CD8+ T cells in a spectrum of human MHC I haplotypes. Proc. Natl. Acad. Sci. USA 2007, 104:1289-1294.
7. Bursch L.S., Wang L., Igyarto B., Kissenpfennig A., Malissen B., Kaplan D.H., Hogquist K.A. Identification of a novel population of Langerin+ dendritic cells. J. Exp. Med. 2007, 204:3147-3156.
8. Carrasco Y.R., Batista F.D. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 2007, 27:160-171.
9. Casares N., Pequignot M.O., Tesniere A., Ghiringhelli F., Roux S., Chaput N., Schmitt E., Hamai A., Hervas-Stubbs S., Obeid M., et al. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J. Exp. Med. 2005, 202:1691-1701.
10. Chtanova T., Schaeffer M., Han S.J., van Dooren G.G., Nollmann M., Herzmark P., Chan S.W., Satija H., Camfield K., Aaron H., et al. Dynamics of neutrophil migration in lymph nodes during infection. Immunity 2008, 29:487-496.
11. Chtanova T., Han S.J., Schaeffer M., van Dooren G.G., Herzmark P., Striepen B., Robey E.A. Dynamics of T cell, antigen-presenting cell, and pathogen interactions during recall responses in the lymph node. Immunity 2009, 31:342-355.
12. Gabrilovich D. Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat. Rev. Immunol. 2004, 4:941-952.
13. Ghiringhelli F., Apetoh L., Tesniere A., Aymeric L., Ma Y., Ortiz C., Vermaelen K., Panaretakis T., Mignot G., Ullrich E., et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med. 2009, 15:1170-1178.
14. Gilboa E., Vieweg J. Cancer immunotherapy with mRNA-transfected dendritic cells. Immunol. Rev. 2004, 199:251-263.
15. Green D.R., Ferguson T., Zitvogel L., Kroemer G. Immunogenic and tolerogenic cell death. Nat. Rev. Immunol. 2009, 9:353-363.
16. Grigorova I.L., Schwab S.R., Phan T.G., Pham T.H., Okada T., Cyster J.G. Cortical sinus probing, S1P1-dependent entry and flow-based capture of egressing T cells. Nat. Immunol. 2009, 10:58-65.
17. Hanayama R., Tanaka M., Miwa K., Shinohara A., Iwamatsu A., Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature 2002, 417:182-187.
18. Hanayama R., Tanaka M., Miyasaka K., Aozasa K., Koike M., Uchiyama Y., Nagata S. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 2004, 304:1147-1150.
19. Henson P.M., Bratton D.L., Fadok V.A. Apoptotic cell removal. Curr. Biol. 2001, 11:R795-R805.
20. Junt T., Moseman E.A., Iannacone M., Massberg S., Lang P.A., Boes M., Fink K., Henrickson S.E., Shayakhmetov D.M., Di Paolo N.C., et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 2007, 450:110-114.
21. Kalergis A.M., Ravetch J.V. Inducing tumor immunity through the selective engagement of activating Fcgamma receptors on dendritic cells. J. Exp. Med. 2002, 195:1653-1659.
22. Kissenpfennig A., Henri S., Dubois B., Laplace-Builhe C., Perrin P., Romani N., Tripp C.H., Douillard P., Leserman L., Kaiserlian D., et al. Dynamics and function of Langerhans cells in vivo: Dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 2005, 22:643-654.
23. Lauber K., Blumenthal S.G., Waibel M., Wesselborg S. Clearance of apoptotic cells: Getting rid of the corpses. Mol. Cell 2004, 14:277-287.
24. Lee H.K., Zamora M., Linehan M.M., Iijima N., Gonzalez D., Haberman A., Iwasaki A. Differential roles of migratory and resident DCs in T cell priming after mucosal or skin HSV-1 infection. J. Exp. Med. 2009, 206:359-370.
25. Marigo I., Dolcetti L., Serafini P., Zanovello P., Bronte V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol. Rev. 2008, 222:162-179.
26. Melief C.J. Cancer immunotherapy by dendritic cells. Immunity 2008, 29:372-383.
27. Miyake Y., Asano K., Kaise H., Uemura M., Nakayama M., Tanaka M. Critical role of macrophages in the marginal zone in the suppression of immune responses to apoptotic cell-associated antigens. J. Clin. Invest. 2007, 117:2268-2278.
28. Miyanishi M., Tada K., Koike M., Uchiyama Y., Kitamura T., Nagata S. Identification of Tim4 as a phosphatidylserine receptor. Nature 2007, 450:435-439.
29. Obeid M., Tesniere A., Ghiringhelli F., Fimia G.M., Apetoh L., Perfettini J.L., Castedo M., Mignot G., Panaretakis T., Casares N., et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 2007, 13:54-61.
30. Phan T.G., Grigorova I., Okada T., Cyster J.G. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol. 2007, 8:992-1000.
31. Phan T.G., Green J.A., Gray E.E., Xu Y., Cyster J.G. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat. Immunol. 2009, 10:786-793.
32. Poulin L.F., Henri S., de Bovis B., Devilard E., Kissenpfennig A., Malissen B. The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells. J. Exp. Med. 2007, 204:3119-3131.
33. Qiu C.H., Miyake Y., Kaise H., Kitamura H., Ohara O., Tanaka M. Novel subset of CD8{alpha}+ dendritic cells localized in the marginal zone is responsible for tolerance to cell-associated antigens. J. Immunol. 2009, 182:4127-4136.
34. Ravichandran K.S., Lorenz U. Engulfment of apoptotic cells: Signals for a good meal. Nat. Rev. Immunol. 2007, 7:964-974.
35. Roozendaal R., Mebius R.E., Kraal G. The conduit system of the lymph node. Int. Immunol. 2008, 20:1483-1487.
36. Sancho D., Mourao-Sa D., Joffre O.P., Schulz O., Rogers N.C., Pennington D.J., Carlyle J.R., Reis e Sousa C. Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J. Clin. Invest. 2008, 118:2098-2110.
37. Sancho D., Joffre O.P., Keller A.M., Rogers N.C., Martinez D., Hernanz-Falcon P., Rosewell I., Reis e Sousa C. Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 2009, 458:899-903.
38. Savill J., Fadok V. Corpse clearance defines the meaning of cell death. Nature 2000, 407:784-788.
39. Schnorrer P., Behrens G.M., Wilson N.S., Pooley J.L., Smith C.M., El-Sukkari D., Davey G., Kupresanin F., Li M., Maraskovsky E., et al. The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc. Natl. Acad. Sci. USA 2006, 103:10729-10734.
40. Schuurhuis D.H., van Montfoort N., Ioan-Facsinay A., Jiawan R., Camps M., Nouta J., Melief C.J., Verbeek J.S., Ossendorp F. Immune complex-loaded dendritic cells are superior to soluble immune complexes as antitumor vaccine. J. Immunol. 2006, 176:4573-4580.
41. Sica A., Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J. Clin. Invest. 2007, 117:1155-1166.
42. Sixt M., Kanazawa N., Selg M., Samson T., Roos G., Reinhardt D.P., Pabst R., Lutz M.B., Sorokin L. The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity 2005, 22:19-29.
43. Su Z., Dannull J., Yang B.K., Dahm P., Coleman D., Yancey D., Sichi S., Niedzwiecki D., Boczkowski D., Gilboa E., Vieweg J. Telomerase mRNA-transfected dendritic cells stimulate antigen-specific CD8+ and CD4+ T cell responses in patients with metastatic prostate cancer. J. Immunol. 2005, 174:3798-3807.
44. Tesniere A., Panaretakis T., Kepp O., Apetoh L., Ghiringhelli F., Zitvogel L., Kroemer G. Molecular characteristics of immunogenic cancer cell death. Cell Death Differ. 2008, 15:3-12.
45. Tomura M., Yoshida N., Tanaka J., Karasawa S., Miwa Y., Miyawaki A., Kanagawa O. Monitoring cellular movement in vivo with photoconvertible fluorescence protein "Kaede" transgenic mice. Proc. Natl. Acad. Sci. USA 2008, 105:10871-10876.
46. Trumpfheller C., Finke J.S., Lopez C.B., Moran T.M., Moltedo B., Soares H., Huang Y., Schlesinger S.J., Park C.G., Nussenzweig M.C., et al. Intensified and protective CD4+ T cell immunity in mice with anti-dendritic cell HIV gag fusion antibody vaccine. J. Exp. Med. 2006, 203:607-617.
47. Waithman J., Allan R.S., Kosaka H., Azukizawa H., Shortman K., Lutz M.B., Heath W.R., Carbone F.R., Belz G.T. Skin-derived dendritic cells can mediate deletional tolerance of class I-restricted self-reactive T cells. J. Immunol. 2007, 179:4535-4541.