CpG promotes cross-presentation of dead cell-associated antigens by pre-CD8α+ dendritic dells

Journal of Immunology

Volumn 186, Issue 3, 2011, Pages 1503-1511

  De Brito, Christelle ^a,b,c   Tomkowiak, Martine ^a,b,c   Ghittoni, Raffaella ^a,b,c   Caux, Christophe ^a   Leverrier, Yann ^a,b,c   Marvel, Jacqueline ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ LYON 1   (France)

^c UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD8ALPHA ANTIGEN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ARTICLE; BIODEGRADATION; CD8+ T LYMPHOCYTE; CELL DEATH; CONTROLLED STUDY; CROSS PRESENTATION; DENDRITIC CELL; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRECURSOR; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGENS; ANTIGENS, CD8; BONE MARROW CELLS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELLS, CULTURED; CPG ISLANDS; CROSS-PRIMING; DENDRITIC CELLS; LIGANDS; MELANOMA, EXPERIMENTAL; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NECROSIS; STEM CELLS; TOLL-LIKE RECEPTORS;

EID: 79251589937     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001022     Document Type: Article

References (53)

1. Heath, W. R., G. T. Belz, G. M. Behrens, C. M. Smith, S. P. Forehan, I. A. Parish, G. M. Davey, N. S. Wilson, F. R. Carbone, and J. A. Villadangos. 2004. Crosspresentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol. Rev. 199: 9-26.
2. Allan, R. S., C. M. Smith, G. T. Belz, A. L. van Lint, L. M. Wakim, W. R. Heath, and F. R. Carbone. 2003. Epidermal viral immunity induced by CD8alpha+ dendritic cells but not by Langerhans cells. Science 301: 1925-1928.
3. Belz, G. T., K. Shortman, M. J. Bevan, and W. R. Heath. 2005. CD8alpha+ dendritic cells selectively present MHC class I-restricted noncytolytic viral and intracellular bacterial antigens in vivo. J. Immunol. 175: 196-200.
4. Belz, G. T., C. M. Smith, D. Eichner, K. Shortman, G. Karupiah, F. R. Carbone, and W. R. Heath. 2004. Cutting edge: conventional CD8 alpha+ dendritic cells are generally involved in priming CTL immunity to viruses. J. Immunol. 172: 1996-2000.
5. Hildner, K., B. T. Edelson, W. E. Purtha, M. Diamond, H. Matsushita, M. Kohyama, B. Calderon, B. U. Schraml, E. R. Unanue, M. S. Diamond, et al. 2008. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322: 1097-1100.
6. den Haan, J. M., S. M. Lehar, and M. J. Bevan. 2000. CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 192: 1685-1696.
7. Iyoda, T., S. Shimoyama, K. Liu, Y. Omatsu, Y. Akiyama, Y. Maeda, K. Takahara, R. M. Steinman, and K. Inaba. 2002. The CD8+ dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J. Exp. Med. 195: 1289-1302.
8. Pooley, J. L., W. R. Heath, and K. Shortman. 2001. Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8- dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J. Immunol. 166: 5327-5330.
9. Schnorrer, P., G. M. Behrens, N. S. Wilson, J. L. Pooley, C. M. Smith, D. El-Sukkari, G. Davey, F. Kupresanin, M. Li, E. Maraskovsky, et al. 2006. The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc. Natl. Acad. Sci. USA 103: 10729-10734.
10. Apetoh, L., F. Ghiringhelli, A. Tesniere, M. Obeid, C. Ortiz, A. Criollo, G. Mignot, M. C. Maiuri, E. Ullrich, P. Saulnier, et al. 2007. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med. 13: 1050-1059.
11. Janeway, C. A., Jr., and R. Medzhitov. 2002. Innate immune recognition. Annu. Rev. Immunol. 20: 197-216.
12. Shi, Y., J. E. Evans, and K. L. Rock. 2003. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425: 516-521.
13. Reis e Sousa, C. 2004. Toll-like receptors and dendritic cells: for whom the bug tolls. Semin. Immunol. 16: 27-34.
14. Wilson, N. S., G. M. Behrens, R. J. Lundie, C. M. Smith, J. Waithman, L. Young, S. P. Forehan, A. Mount, R. J. Steptoe, K. D. Shortman, et al. 2006. Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nat. Immunol. 7: 165-172.
15. Weck, M. M., F. Grünebach, D. Werth, C. Sinzger, A. Bringmann, and P. Brossart. 2007. TLR ligands differentially affect uptake and presentation of cellular antigens. Blood 109: 3890-3894.
16. Massberg, S., P. Schaerli, I. Knezevic-Maramica, M. Köllnberger, N. Tubo, E. A. Moseman, I. V. Huff, T. Junt, A. J. Wagers, I. B. Mazo, and U. H. von Andrian. 2007. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131: 994-1008.
17. Nagai, Y., K. P. Garrett, S. Ohta, U. Bahrun, T. Kouro, S. Akira, K. Takatsu, and P. W. Kincade. 2006. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 24: 801-812.
18. Sioud, M., Y. Fløisand, L. Forfang, and F. Lund-Johansen. 2006. Signaling through toll-like receptor 7/8 induces the differentiation of human bone marrow CD34+ progenitor cells along the myeloid lineage. J. Mol. Biol. 364: 945-954.
19. Welner, R. S., R. Pelayo, Y. Nagai, K. P. Garrett, T. R. Wuest, D. J. Carr, L. A. Borghesi, M. A. Farrar, and P. W. Kincade. 2008. Lymphoid precursors are directed to produce dendritic cells as a result of TLR9 ligation during herpes infection. Blood 112: 3753-3761.
20. De Luca, K., V. Frances-Duvert, M. J. Asensio, R. Ihsani, E. Debien, M. Taillardet, E. Verhoeyen, C. Bella, S. Lantheaume, L. Genestier, and T. Defrance. 2009. The TLR1/2 agonist PAM(3)CSK(4) instructs commitment of human hematopoietic stem cells to a myeloid cell fate. Leukemia 23: 2063-2074.
21. Rock, K. L., and H. Kono. 2008. The inflammatory response to cell death. Annu. Rev. Pathol. 3: 99-126.
22. Brasel, K., T. De Smedt, J. L. Smith, and C. R. Maliszewski. 2000. Generation of murine dendritic cells from flt3-ligand-supplemented bone marrow cultures. Blood 96: 3029-3039.
23. Naik, S. H. 2008. Demystifying the development of dendritic cell subtypes, a little. Immunol. Cell Biol. 86: 439-452.
24. Naik, S. H., A. I. Proietto, N. S. Wilson, A. Dakic, P. Schnorrer, M. Fuchsberger, M. H. Lahoud, M. O'Keeffe, Q. X. Shao, W. F. Chen, et al. 2005. Cutting edge: generation of splenic CD8+ and CD8- dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J. Immunol. 174: 6592-6597.
25. Naik, S. H., P. Sathe, H. Y. Park, D. Metcalf, A. I. Proietto, A. Dakic, S. Carotta, M. O'Keeffe, M. Bahlo, A. Papenfuss, et al. 2007. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat. Immunol. 8: 1217-1226.
26. Mamalaki, C., T. Norton, Y. Tanaka, A. R. Townsend, P. Chandler, E. Simpson, and D. Kioussis. 1992. Thymic depletion and peripheral activation of class I major histocompatibility complex-restricted T cells by soluble peptide in T-cell receptor transgenic mice. Proc. Natl. Acad. Sci. USA 89: 11342-11346.
27. Leverrier, Y., J. Thomas, G. R. Perkins, M. Mangeney, M. K. Collins, and J. Marvel. 1997. In bone marrow derived Baf-3 cells, inhibition of apoptosis by IL-3 is mediated by two independent pathways. Oncogene 14: 425-430.
28. Angelov, G. S., M. Tomkowiak, A. Marçais, Y. Leverrier, and J. Marvel. 2005. Flt3 ligand-generated murine plasmacytoid and conventional dendritic cells differ in their capacity to prime naive CD8 T cells and to generate memory cells in vivo. J. Immunol. 175: 189-195.
29. Xu, Y., Y. Zhan, A. M. Lew, S. H. Naik, and M. H. Kershaw. 2007. Differential development of murine dendritic cells by GM-CSF versus Flt3 ligand has implications for inflammation and trafficking. J. Immunol. 179: 7577-7584.
30. Bedoui, S., S. Prato, J. Mintern, T. Gebhardt, Y. Zhan, A. M. Lew, W. R. Heath, J. A. Villadangos, and E. Segura. 2009. Characterization of an immediate splenic precursor of CD8+ dendritic cells capable of inducing antiviral T cell responses. J. Immunol. 182: 4200-4207.
31. Kool, M., T. Soullié, M. van Nimwegen, M. A. Willart, F. Muskens, S. Jung, H. C. Hoogsteden, H. Hammad, and B. N. Lambrecht. 2008. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J. Exp. Med. 205: 869-882.
32. Mouriès, J., G. Moron, G. Schlecht, N. Escriou, G. Dadaglio, and C. Leclerc. 2008. Plasmacytoid dendritic cells efficiently cross-prime naive T cells in vivo after TLR activation. Blood 112: 3713-3722.
33. Robbins, S. H., T. Walzer, D. Dembélé, C. Thibault, A. Defays, G. Bessou, H. Xu, E. Vivier, M. Sellars, P. Pierre, et al. 2008. Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol. 9: R17.
34. Serbina, N. V., T. P. Salazar-Mather, C. A. Biron, W. A. Kuziel, and E. G. Pamer. 2003. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19: 59-70.
35. Fields, R. C., K. Shimizu, and J. J. Mulé. 1998. Murine dendritic cells pulsed with whole tumor lysates mediate potent antitumor immune responses in vitro and in vivo. Proc. Natl. Acad. Sci. USA 95: 9482-9487.
36. Gil-Torregrosa, B. C., A. M. Lennon-Duménil, B. Kessler, P. Guermonprez, H. L. Ploegh, D. Fruci, P. van Endert, and S. Amigorena. 2004. Control of cross-presentation during dendritic cell maturation. Eur. J. Immunol. 34: 398-407.
37. Mercier, B. C., A. Cottalorda, C. A. Coupet, J. Marvel, and N. Bonnefoy-Bérard. 2009. TLR2 engagement on CD8 T cells enables generation of functional memory cells in response to a suboptimal TCR signal. J. Immunol. 182: 1860-1867.
38. West, M. A., R. P. Wallin, S. P. Matthews, H. G. Svensson, R. Zaru, H. G. Ljunggren, A. R. Prescott, and C. Watts. 2004. Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 305: 1153-1157.
39. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18: 767-811.
40. Norbury, C. C. 2006. Drinking a lot is good for dendritic cells. Immunology 117: 443-451.
41. Burgdorf, S., C. Schölz, A. Kautz, R. Tampé, and C. Kurts. 2008. Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat. Immunol. 9: 558-566.
42. Kingston, D., M. A. Schmid, N. Onai, A. Obata-Onai, D. Baumjohann, and M. G. Manz. 2009. The concerted action of GM-CSF and Flt3-ligand on in vivo dendritic cell homeostasis. Blood 114: 835-843.
43. Hamilton, J. A. 2008. Colony-stimulating factors in inflammation and autoimmunity. Nat. Rev. Immunol. 8: 533-544.
44. Wilson, N. S., D. El-Sukkari, G. T. Belz, C. M. Smith, R. J. Steptoe, W. R. Heath, K. Shortman, and J. A. Villadangos. 2003. Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood 102: 2187-2194.
45. Gallucci, S., M. Lolkema, and P. Matzinger. 1999. Natural adjuvants: endogenous activators of dendritic cells. Nat. Med. 5: 1249-1255.
46. Obeid, M., A. Tesniere, F. Ghiringhelli, G. M. Fimia, L. Apetoh, J. L. Perfettini, M. Castedo, G. Mignot, T. Panaretakis, N. Casares, et al. 2007. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 13: 54-61.
47. Russell, D. G. 2007. New ways to arrest phagosome maturation. Nat. Cell Biol. 9: 357-359.
48. Lin, M. L., Y. Zhan, A. I. Proietto, S. Prato, L. Wu, W. R. Heath, J. A. Villadangos, and A. M. Lew. 2008. Selective suicide of cross-presenting CD8+ dendritic cells by cytochrome c injection shows functional heterogeneity within this subset. Proc. Natl. Acad. Sci. USA 105: 3029-3034.
49. Alvarez, D., E. H. Vollmann, and U. H. von Andrian. 2008. Mechanisms and consequences of dendritic cell migration. Immunity 29: 325-342.
50. Shi, Y., C. H. Liu, A. I. Roberts, J. Das, G. Xu, G. Ren, Y. Zhang, L. Zhang, Z. R. Yuan, H. S. Tan, et al. 2006. Granulocyte-macrophage colony-stimulating factor (GM-CSF) and T-cell responses: what we do and don't know. Cell Res. 16: 126-133.
51. Janssen, E., K. Tabeta, M. J. Barnes, S. Rutschmann, S. McBride, K. S. Bahjat, S. P. Schoenberger, A. N. Theofilopoulos, B. Beutler, and K. Hoebe. 2006. Efficient T cell activation via a Toll-Interleukin 1 Receptor-independent pathway. Immunity 24: 787-799.
52. Nayak, J. V., D. A. Hokey, A. Larregina, Y. He, R. D. Salter, S. C. Watkins, and L. D. Falo, Jr. 2006. Phagocytosis induces lysosome remodeling and regulated presentation of particulate antigens by activated dendritic cells. J. Immunol. 177: 8493-8503.
53. Mach, N., S. Gillessen, S. B. Wilson, C. Sheehan, M. Mihm, and G. Dranoff. 2000. Differences in dendritic cells stimulated in vivo by tumors engineered to secrete granulocyte-macrophage colony-stimulating factor or Flt3-ligand. Cancer Res. 60: 3239-3246. (Pubitemid 30407923)