Cross-presentation: How to get there - or how to get the ER

Frontiers in Immunology

Volumn 2, Issue JAN, 2012, Pages

  Kreer, Christoph ^a   Rauen, Judith ^a   Zehner, Matthias ^a   Burgdorf, Sven ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

Antigen storage compartments; Cross presentation; Dendritic cells; Endosomes

Indexed keywords

EID: 84874033381     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2011.00087     Document Type: Review

References (102)

1. Ackerman, A. L., Giodini, A., and Cresswell, P. (2006). A role for the endoplasmic reticulum protein retrotranslocation machinery during cross-presentation by dendritic cells. Immunity 25, 607-617.
2. Ackerman, A. L., Kyritsis, C., Tampe, R., and Cresswell, P. (2003). Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc. Natl. Acad. Sci. U.S.A. 100, 12889-12894.
3. Bachem, A., Guttler, S., Hartung, E., Ebstein, F., Schaefer, M., Tannert, A., Salama, A., Movassaghi, K., Opitz, C., Mages, H. W., Henn, V., Kloetzel, P. M., Gurka, S., and Kroczek, R. A. (2010). Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cellsashomologues of mouse CD8+ dendritic cells. J. Exp. Med. 207, 1273-1281.
4. Backer, R., van Leeuwen, F., Kraal, G., and den Haan, J. M. (2008). CD8dendritic cells preferentially cross-present Saccharomyces cerevisiae antigens. Eur. J. Immunol. 38, 370-380.
5. Baker, K., Qiao, S. W., Kuo, T. T., Aveson, V. G., Platzer, B., Andersen, J. T., Sandlie, I., Chen, Z., de Haar, C., Lencer, W. I., Fiebiger, E., and Blumberg, R. S. (2011). Neonatal Fc receptor for IgG (FcRn) regulates cross-presentation of IgG immune complexes by CD8-CD11b+ dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 108, 9927-9932.
6. Bertholet, S., Goldszmid, R., Morrot, A., Debrabant, A., Afrin, F., Collazo Custodio, C., Houde, M., Desjardins, M., Sher, A., and Sacks, D. (2006). Leishmania antigens are presented to CD8+T cells by a transporter associated with antigen processingindependent pathway in vitro and in vivo. J. Immunol. 177, 3525-3533.
7. Bevan, M. J. (1976). Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J. Exp. Med. 143, 1283-1288.
8. Bonifaz, L. C., Bonnyay, D. P., Charalambous, A., Darguste, D. I., Fujii, S., Soares, H., Brimnes, M. K., Moltedo, B., Moran, T. M., and Steinman, R. M. (2004). In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J. Exp. Med. 199, 815-824.
9. Bougneres, L., Helft, J., Tiwari, S., Vargas, P., Chang, B. H., Chan, L., Campisi, L., Lauvau, G., Hugues, S., Kumar, P., Kamphorst, A. O., Dumenil, A. M., Nussenzweig, M., MacMicking, J. D., Amigorena, S., and Guermonprez,P. (2009). A role for lipid bodies in the cross-presentation of phagocytosed antigens by MHC class I in dendritic cells. Immunity 31, 232-244.
10. Burgdorf, S., Kautz, A., Bohnert, V., Knolle, P. A., and Kurts, C. (2007). Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316, 612-616.
11. Burgdorf, S., Scholz, C., Kautz, A., Tampe,R.,and Kurts,C. (2008). Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat. Immunol. 9, 558-566.
12. Cella, M., Engering, A., Pinet, V., Pieters, J., and Lanzavecchia, A. (1997). Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 388, 782-787.
13. Cella, M., Salio, M., Sakakibara, Y., Langen, H., Julkunen, I., and Lanzavecchia, A. (1999). Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J. Exp. Med. 189, 821-829.
14. Crozat, K., Guiton, R., Contreras, V., Feuillet, V., Dutertre, C. A., Ventre, E., Vu Manh, T. P., Baranek, T., Storset, A. K., Marvel, J., Boudinot, P., Hosmalin, A., Schwartz-Cornil, I., and Dalod, M. (2010). The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8alpha+ dendritic cells. J. Exp. Med. 207, 1283-1292.
15. Dasgupta, S., Navarrete, A. M., Bayry, J., Delignat, S., Wootla, B., Andre, S., Christophe, O., Nascimbeni, M., Jacquemin, M., Martinez-Pomares, L., Geijtenbeek, T. B., Moris, A., Saint-Remy, J. M., Kazatchkine, M. D., Kaveri, S. V., and LacroixDesmazes, S. (2007). A role for exposed mannosylations in presentation of human therapeutic selfproteins to CD4+ T lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 104, 8965-8970.
16. Delamarre, L., Pack, M., Chang, H., Mellman, I., and Trombetta, E. S. (2005). Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307, 1630-1634.
17. den Haan,J. M.,and Bevan,M. J. (2001). Antigen presentation to CD8+ T cells: cross-priming in infectious diseases. Curr. Opin. Immunol. 13, 437-441.
18. den Haan, J. M., Lehar, S. M., and Bevan, M. J. (2000). CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 192, 1685-1696.
19. Desjardins, M. (2009). The good fat: a link between lipid bodies and antigen cross-presentation. Immunity 31, 176-178.
20. Dolan, B. P., Gibbs, K. D. Jr., and Ostrand-Rosenberg, S. (2006). Dendritic cells cross-dressed with peptide MHC class I complexes prime CD8+ T cells. J. Immunol. 177, 6018-6024.
21. Dudziak, D., Kamphorst, A. O., Heidkamp, G. F., Buchholz, V. R., Trumpfheller, C., Yamazaki, S., Cheong, C., Liu, K., Lee, H. W., Park, C. G., Steinman, R. M., and Nussenzweig, M. C. (2007). Differential antigen processing by dendritic cell subsets in vivo. Science 315, 107-111.
22. Eberl, G., Widmann, C., and Corradin, G. (1996). The functional half-life of H-2Kd-restricted T cell epitopes on living cells. Eur. J. Immunol. 26, 1993-1999.
23. Ebstein, F., Lange, N., Urban, S., Seifert, U., Kruger, E., and Kloetzel, P. M. (2009). Maturation of human dendritic cells is accompanied by functional remodelling of the ubiquitinproteasome system. Int. J. Biochem. Cell Biol. 41, 1205-1215.
24. Gagnon, E., Duclos, S., Rondeau, C., Chevet, E., Cameron, P. H., Steele Mortimer, O., Paiement, J., Bergeron, J. J., and Desjardins, M. (2002). Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110, 119-131.
25. Georgiadou, D., Hearn, A., Evnouchidou, I., Chroni, A., Leondiadis, L., York, I. A., Rock, K. L., and Stratikos, E. (2010). Placental leucine aminopeptidase efficiently generates mature antigenic peptides in vitro but in patterns distinct from endoplasmic reticulum aminopeptidase 1. J. Immunol. 185, 1584-1592.
26. Gil-Torregrosa, B. C., Lennon-Dumenil, A. M., Kessler, B., Guermonprez, P., Ploegh, H. L., Fruci, D., van Endert, P., and Amigorena,S. (2004). Control of cross-presentation during dendritic cell maturation. Eur. J. Immunol. 34, 398-407.
27. Giodini, A., and Cresswell, P. (2008). Hsp90-mediated cytosolic refolding of exogenous proteins internalized by dendritic cells. EMBO J. 27, 201-211.
28. Giodini,A., Rahner, C., and Cresswell, P. (2009). Receptor-mediated phagocytosis elicits cross-presentation in nonprofessional antigen-presenting cells. Proc. Natl.Acad. Sci. U.S.A. 106, 3324-3329.
29. Goldszmid, R. S., Coppens, I., Lev, A., Caspar, P., Mellman, I., and Sher, A. (2009). Host ER-parasitophorous vacuole interaction provides a route of entry for antigen cross-presentation in Toxoplasma gondii-infected dendritic cells. J. Exp. Med. 206, 399-410.
30. Guermonprez, P., Saveanu, L., Kleijmeer, M., Davoust, J., Van Endert, P., and Amigorena, S. (2003). ERphagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 425, 397-402.
31. Guillaume, B., Chapiro, J., Stroobant, V., Colau, D., Van Holle, B., Parvizi, G., Bousquet-Dubouch, M. P., Theate, I., Parmentier, N., and Van den Eynde, B. J. (2010). Two abundant proteasome subtypes that uniquely process some antigens presented by HLA class I molecules. Proc. Natl. Acad. Sci. U.S.A. 107, 18599-18604.
32. Hamman, B. D., Chen, J. C., Johnson, E. E., and Johnson, A. E. (1997). The aqueous pore through the translocon has a diameter of 40-60 A during cotranslational protein translocation at the ER membrane. Cell 89, 535-544.
33. He, L. Z., Crocker, A., Lee, J., Mendoza Ramirez, J., Wang, X. T., Vitale, L. A., O'Neill, T., Petromilli, C., Zhang, H. F., Lopez, J., Rohrer, D., Keler, T., and Clynes, R. (2007). Antigenic targeting of the human mannose receptor induces tumor immunity. J. Immunol. 178, 6259-6267.
34. Heath, W. R., and Carbone, F. R. (2001). Cross-presentation in viral immunity and self-tolerance. Nat. Rev. Immunol. 1, 126-134.
35. Herre, J., Marshall, A. S., Caron, E., Edwards, A. D., Williams, D. L., Schweighoffer, E., Tybulewicz, V., Reis e Sousa, C., Gordon, S., and Brown, G. D. (2004). Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages. Blood 104, 4038-4045.
36. Hildner, K., Edelson, B. T., Purtha, W. E., Diamond, M., Matsushita, H., Kohyama, M., Calderon, B., Schraml, B. U., Unanue, E. R., Diamond, M. S., Schreiber, R. D., Murphy, T. L., and Murphy, K. M. (2008). Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322, 1097-1100.
37. Hotta, C., Fujimaki, H., Yoshinari, M., Nakazawa, M., and Minami, M. (2006). The delivery of an antigen from the endocytic compartment into the cytosol for crosspresentation is restricted to early immature dendritic cells. Immunology 117, 97-107.
38. Hou, J. C., Suzuki, N., Pessin, J. E., and Watson, R. T. (2006). A specific dileucine motif is required for the GGA-dependent entry of newly synthesized insulin-responsive aminopeptidase into the insulinresponsive compartment. J. Biol. Chem. 281, 33457-33466.
39. Houde, M., Bertholet, S., Gagnon, E., Brunet, S., Goyette, G., Laplante, A., Princiotta, M. F., Thibault, P., Sacks, D., and Desjardins, M. (2003). Phagosomes are competent organelles for antigen crosspresentation. Nature 425, 402-406.
40. Huang,A.Y., Bruce,A. T., Pardoll, D. M., and Levitsky, H. I. (1996). In vivo cross-priming of MHC class Irestricted antigens requires the TAP transporter. Immunity 4, 349-355.
41. Huang, A. Y., Golumbek, P., Ahmadzadeh, M., Jaffee, E., Pardoll, D., and Levitsky, H. (1994). Role of bone marrow-derived cells in presenting MHC class I-restricted tumor antigens. Science 264, 961-965.
42. Imai, J., Hasegawa, H., Maruya, M., Koyasu, S., and Yahara, I. (2005). Exogenous antigens are processed through the endoplasmic reticulumassociated degradation (ERAD) in cross-presentation by dendritic cells. Int. Immunol. 17, 45-53.
43. Jongbloed, S. L., Kassianos, A. J., McDonald, K. J., Clark, G. J., Ju, X., Angel, C. E., Chen, C. J., Dunbar, P. R., Wadley, R. B., Jeet, V., Vulink, A. J., Hart, D. N., and Radford, K. J. (2010). Human CD141+ (BDCA3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J. Exp. Med. 207, 1247-1260.
44. Kagan, J. C., Su, T., Horng, T., Chow, A., Akira, S., and Medzhitov, R. (2008). TRAM couples endocytosis of Tolllike receptor 4 to the induction of interferon-beta. Nat. Immunol. 9, 361-368.
45. Kamphorst, A. O., Guermonprez, P., Dudziak,D.,and Nussenzweig,M. C. (2010). Route of antigen uptake differentially impacts presentation by dendritic cells and activated monocytes. J. Immunol. 185, 3426-3435.
46. Kim, Y. M., Brinkmann, M. M., Paquet, M. E., and Ploegh, H. L. (2008). UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature 452, 234-238.
47. Kloetzel, P. M., and Ossendorp, F. (2004). Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr. Opin. Immunol. 16, 76-81.
48. Koopmann, J. O., Albring, J., Huter, E., Bulbuc, N., Spee, P., Neefjes, J., Hammerling, G. J., and Momburg, F. (2000). Export of antigenic peptides from the endoplasmic reticulum intersects with retrograde protein translocation through the Sec61p channel. Immunity 13, 117-127.
49. Kovacsovics-Bankowski, M., and Rock, K. L. (1995). A phagosome-tocytosol pathway for exogenous antigens presented on MHC class I molecules. Science 267, 243-246.
50. Kukutsch, N. A., Rossner, S., Austyn, J. M., Schuler, G., and Ltz, M. B. (2000). Formation and kinetics of MHC class I-ovalbumin peptide complexes on immature and mature dendritic cells. J. Invest. Dermatol. 115, 449-453.
51. Kurts, C., Heath, W. R., Carbone, F. R., Allison, J., Miller, J. F., and Kosaka, H. (1996). Constitutive class I-restricted exogenous presentation of self antigens in vivo. J. Exp. Med. 184, 923-930.
52. Latz, E., Schoenemeyer, A., Visintin, A., Fitzgerald, K. A., Monks, B. G., Knetter, C. F., Lien, E., Nilsen, N. J., Espevik, T., and Golenbock, D. T. (2004). TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 5, 190-198.
53. Lev, A., Princiotta, M. F., Zanker, D., Takeda, K., Gibbs, J. S., Kumagai, C., Waffarn, E., Dolan, B. P., Burgevin, A., Van Endert, P., Chen, W., Bennink, J. R., and Yewdell, J. W. (2010). Compartmentalized MHC class I antigen processing enhances immunosurveillance by circumventing the law of mass action. Proc. Natl. Acad. Sci. U.S.A. 107, 6964-6969.
54. Lilley, B. N., and Ploegh, H. L. (2004). A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429, 834-840.
55. Lin, M. L., Zhan, Y., Villadangos, J. A., and Lew, A. M. (2008). The cell biology of cross-presentation and the role of dendritic cell subsets. Immunol. Cell Biol. 86, 353-362.
56. Macagno, A., Gilliet, M., Sallusto, F., Lanzavecchia, A., Nestle, F. O., and Groettrup, M. (1999). Dendritic cells up-regulate immunoproteasomes and the proteasome regulator PA28 during maturation. Eur. J. Immunol. 29, 4037-4042.
57. Mantegazza, A. R., Savina, A., Vermeulen, M., Perez, L., Geffner, J., Hermine, O., Rosenzweig, S. D., Faure, F., and Amigorena, S. (2008). NADPH oxidase controls phagosomal pH and antigen crosspresentation in human dendritic cells. Blood 112, 4712-4722.
58. Martin-Fontecha, A., Sebastiani, S., Hopken, U. E., Uguccioni, M., Lipp, M., Lanzavecchia, A., and Sallusto, F. (2003). Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J. Exp. Med. 198, 615-621.
59. McKenzie, E. J., Taylor, P. R., Stillion, R. J., Lucas, A. D., Harris, J., Gordon, S.,and Martinez-Pomares,L. (2007). Mannose receptor expression and function define a new population of murine dendritic cells. J. Immunol. 178, 4975-4983.
60. Mellman, I., and Steinman, R. M. (2001). Dendritic cells: specialized and regulated antigen processing machines. Cell 106, 255-258.
61. Mendoza-Naranjo, A., Saez, P. J., Johansson, C. C., Ramirez, M., Mandakovic, D., Pereda, C., Lopez, M. N., Kiessling, R., Saez, J. C., and Salazar Onfray, F. (2007). Functional gap junctions facilitate melanoma antigen transfer and cross-presentation between human dendritic cells. J. Immunol. 178, 6949-6957.
62. Neijssen, J., Herberts, C., Drijfhout, J. W., Reits, E., Janssen, L., and Neefjes, J. (2005). Cross-presentation by intercellular peptide transfer through gap junctions. Nature 434, 83-88.
63. Nishi, T., and Forgac, M. (2002). The vacuolar (H+)-ATPases - nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 3, 94-103.
64. Norbury, C. C., Basta, S., Donohue, K. B., Tscharke, D. C., Princiotta, M. F., Berglund, P., Gibbs, J., Bennink, J. R., and Yewdell, J. W. (2004). CD8+ T cell cross-priming via transfer of proteasome substrates. Science 304, 1318-1321.
65. Norbury, C. C., Chambers, B. J., Prescott, A. R., Ljunggren, H. G., and Watts, C. (1997). Constitutive macropinocytosis allows TAPdependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur. J. Immunol. 27, 280-288.
66. Palmowski, M. J., Gileadi, U., Salio, M., Gallimore, A., Millrain, M., James, E., Addey, C., Scott, D., Dyson, J., Simpson, E., and Cerundolo, V. (2006). Role of immunoproteasomes in cross-presentation. J. Immunol. 177, 983-990.
67. Pooley, J. L., Heath, W. R., and Shortman, K. (2001). Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J. Immunol. 166, 5327-5330.
68. Poulin, L. F., Salio, M., Griessinger, E., Anjos-Afonso, F., Craciun, L., Chen, J. L., Keller, A. M., Joffre, O., Zelenay, S., Nye, E., Le Moine, A., Faure, F., Donckier, V., Sancho, D., Cerundolo, V., Bonnet, D., and Reise Sousa, C. (2010). Characterization of human DNGR1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J. Exp. Med. 207, 1261-1271.
69. Purcell, A. W., and Elliott, T. (2008). Molecular machinations of the MHC-I peptide loading complex. Curr. Opin. Immunol. 20, 75-81.
70. Reits, E., Griekspoor, A., Neijssen, J., Groothuis, T., Jalink, K., van Veelen, P., Janssen, H., Calafat, J., Drijfhout, J. W., and Neefjes, J. (2003). Peptide diffusion,protection,and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity 18, 97-108.
71. Rescigno, M., Citterio, S., Thery, C., Rittig, M., Medaglini, D., Pozzi, G., Amigorena, S., and RicciardiCastagnoli, P. (1998). Bacteriainduced neo-biosynthesis, stabilization, and surface expression of functional class I molecules in mouse dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 95, 5229-5234.
72. Rock, K. L., and Shen, L. (2005). Crosspresentation: underlying mechanisms and role in immune surveillance. Immunol. Rev. 207, 166-183.
73. Rodriguez, A., Regnault, A., Kleijmeer, M., Ricciardi-Castagnoli, P., and Amigorena, S. (1999). Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells. Nat. Cell Biol. 1, 362-368.
74. Saccheri, F., Pozzi, C., Avogadri, F., Barozzi, S., Faretta, M., Fusi, P., and Rescigno, M. (2010). Bacteriainduced gap junctions in tumors favor antigen cross-presentation and antitumor immunity. Sci. Transl. Med. 2, 44-57.
75. Saveanu, L., Carroll, O., Weimershaus, M., Guermonprez, P., Firat, E., Lindo, V., Greer, F., Davoust, J., Kratzer, R., Keller, S. R., Niedermann, G., and van Endert, P. (2009). IRAP identifies an endosomal compartment required for MHC class I cross-presentation. Science 325, 213-217.
76. Savina, A., Jancic, C., Hugues, S., Guermonprez, P., Vargas, P., Moura, I. C., Lennon-Dumenil, A. M., Seabra, M. C., Raposo, G., and Amigorena, S. (2006). NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126, 205-218.
77. Savina, A., Peres, A., Cebrian, I., Carmo, N., Moita, C., Hacohen, N., Moita, L. F., and Amigorena, S. (2009). The small GTPase Rac2 controls phagosomal alkalinization and antigen crosspresentation selectively in CD8(+) dendritic cells. Immunity 30, 544-555.
78. Schnorrer, P., Behrens, G. M., Wilson, N. S., Pooley, J. L., Smith, C. M., Elsukkari, D., Davey, G., Kupresanin, F., Li, M., Maraskovsky, E., Belz, G. T., Carbone, F. R., Shortman, K., Heath, W. R., and Villadangos, J. A. (2006). The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc. Natl. Acad. Sci. U.S.A. 103, 10729-10734.
79. Segura, E., and Villadangos, J. A. (2011). A modular and combinatorial view of the antigen cross-presentation pathway in dendritic cells. Traffic 12, 1677-1685.
80. Seifert, U., Bialy, L. P., Ebstein, F., Bech-Otschir, D., Voigt, A., Schroter, F., Prozorovski, T., Lange, N., Steffen, J., Rieger, M., Kuckelkorn, U., Aktas, O., Kloetzel, P. M., and Krüger, E. (2010). Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell 142, 613-624.
81. Shen, L., Sigal, L. J., Boes, M., and Rock, K. L. (2004). Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo. Immunity 21, 155-165.
82. Shimada, K., Takimoto, H., Yano, I., and Kumazawa, Y. (2006). Involvement of mannose receptor in glycopeptidolipid-mediated inhibition of phagosome-lysosome fusion. Microbiol. Immunol. 50, 243-251.
83. Sigal, L. J., Crotty, S., Andino, R., and Rock, K. L. (1999). Cytotoxic T-cell immunity to virus-infected non-haematopoietic cells requires presentation of exogenous antigen. Nature 398, 77-80.
84. Smyth, L. A., Harker, N., Turnbull, W., El-Doueik, H., Klavinskis, L., Kioussis, D., Lombardi, G., and Lechler, R. (2008). The relative efficiency of acquisition of MHC: peptide complexes and cross-presentation depends on dendritic cell type. J. Immunol. 181, 3212-3220.
85. Song, R., and Harding, C. V. (1996). Roles of proteasomes, transporter for antigen presentation (TAP), and beta 2-microglobulin in the processing of bacterial or particulate antigens via an alternate class I MHC processing pathway. J. Immunol. 156, 4182-4190.
86. Sweet, L., Singh, P. P., Azad, A. K., Rajaram, M. V., Schlesinger, L. S., and Schorey, J. S. (2010). Mannose receptor-dependent delay in phagosome maturation by Mycobacterium avium glycopeptidolipids. Infect. Immun. 78, 518-526.
87. Tabeta, K., Hoebe, K., Janssen, E. M., Du,X.,Georgel,P.,Crozat,K.,Mudd, S., Mann, N., Sovath, S., Goode, J., Shamel, L., Herskovits, A. A., Portnoy, D. A., Cooke, M., Tarantino, L. M., Wiltshire, T., Steinberg, B. E., Grinstein, S., and Beutler, B. (2006). The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3,7 and 9. Nat. Immunol. 7, 156-164.
88. Tacken, P. J., de Vries, I. J., Gijzen, K., Joosten, B., Wu, D., Rother, R. P., Faas, S. J., Punt, C. J., Torensma, R., Adema, G. J., and Figdor, C. G. (2005). Effective induction of naive and recall T-cell responses by targeting antigen to human dendritic cells via a humanized anti-DC-SIGN antibody. Blood 106, 1278-1285.
89. Tacken, P. J., Ginter, W., Berod, L., Cruz, L. J., Joosten, B., Sparwasser, T., Figdor, C. G., and Cambi, A. (2011). Targeting DC-SIGN via its neck region leads to prolonged antigen residence in early endosomes, delayed lysosomal degradation, and cross-presentation. Blood 118, 4111-4119.
90. Touret, N., Paroutis, P., Terebiznik, M., Harrison, R. E., Trombetta, S., Pypaert, M., Chow, A., Jiang, A., Shaw, J., Yip, C., Moore, H. P., van der Wel, N., Houben, D., Peters, P. J., de Chastellier, C., Mellman, I., and Grinstein, S. (2005). Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 123, 157-170.
91. Trombetta, E. S., Ebersold, M., Garrett, W., Pypaert, M., and Mellman, I. (2003). Activation of lysosomal function during dendritic cell maturation. Science 299, 1400-1403.
92. Tucker, S. C., and Casadevall, A. (2002). Replication of Cryptococcus neoformans in macrophages is accompanied by phagosomal permeabilization and accumulation of vesicles containing polysaccharide in the cytoplasm. Proc. Natl. Acad. Sci. U.S.A. 99, 3165-3170.
93. Van den Berg, B., Clemons, W. M. Jr., Collinson, I., Modis, Y., Hartmann, E., Harrison, S. C., and Rapoport, T. A. (2004). X-ray structure of a protein-conducting channel. Nature 427, 36-44.
94. van Montfoort,N.,Camps,M. G.,Khan, S., Filippov, D. V., Weterings, J. J., Griffith, J. M., Geuze, H. J., van Hall, T., Verbeek, J. S., Melief, C. J., and Ossendorp, F. (2009). Antigen storage compartments in mature dendritic cells facilitate prolonged cytotoxic T lymphocyte cross-priming capacity. Proc. Natl. Acad. Sci. U.S.A. 106, 6730-6735.
95. Wakim, L. M., and Bevan, M. J. (2011). Cross-dressed dendritic cells drive memory CD8+ T-cell activation after viral infection. Nature 471, 629-632.
96. Weck, M. M., Appel, S., Werth, D., Sinzger, C., Bringmann, A., Grunebach, F., and Brossart, P. (2008). hDectin-1 is involved in uptake and cross-presentation of cellular antigens. Blood 111, 4264-4272.
97. Werneburg, N. W., Guicciardi, M. E., Bronk, S. F., and Gores, G. J. (2002). Tumor necrosis factoralpha-associated lysosomal permeabilization is cathepsin B dependent. Am. J. Physiol. Gastrointest. Liver Physiol. 283, G947-G956.
98. Wiertz, E. J., Tortorella, D., Bogyo, M., Yu, J., Mothes, W., Jones, T. R., Rapoport, T. A., and Ploegh, H. L. (1996). Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384, 432-438.
99. Wolkers, M. C., Brouwenstijn, N., Bakker, A. H., Toebes, M., and Schumacher, T. N. (2004). Antigen bias in T cell cross-priming. Science 304, 1314-1317.
100. Ye, Y., Meyer, H. H., and Rapoport, T. A. (2003). Function of the p97-Ufd1Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J. Cell Biol. 162, 71-84.
101. Ye, Y., Shibata, Y., Yun, C., Ron, D., and Rapoport, T. A. (2004). A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429, 841-847.
102. Zehner, M., Chasan, A. I., Schuette, V., Embgenbroich, M., Quast, T., Kolanus, W., and Burgdorf, S. (2011). Mannose receptor polyubiquitination regulates endosomal recruitment of p97 and cytosolic antigen translocation for crosspresentation. Proc. Natl. Acad. Sci. U.S.A. 108, 9933-9938.