The ins-and-outs of endosomal antigens for cross-presentation

Current Opinion in Immunology

Volumn 26, Issue 1, 2014, Pages 63-68

  Schuette, Verena ^a   Burgdorf, Sven ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; MANNOSE RECEPTOR; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SNARE PROTEIN;

ACIDIFICATION; ANTIGEN DETECTION; ANTIGEN PRESENTATION; ANTIGENICITY; CD8+ T LYMPHOCYTE; CROSS PRESENTATION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; ENDOCYTOSIS; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOSOME; HUMAN; INTERNALIZATION; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN STABILITY; REVIEW;

ANIMALS; ANTIGENS, CD8; CROSS-PRIMING; DENDRITIC CELLS; ENDOCYTOSIS; ENDOSOMES; EXTRACELLULAR SPACE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; LECTINS, C-TYPE; NECROSIS; PROTEIN STABILITY; RECEPTORS, IMMUNOLOGIC; RECEPTORS, MITOGEN;

EID: 84888798052     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2013.11.001     Document Type: Review

References (56)

1. Neefjes J., Jongsma M.L., Paul P., Bakke O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev 2011, 11:823-836.
2. 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., et al. Antigen storage compartments in mature dendritic cells facilitate prolonged cytotoxic T lymphocyte cross-priming capacity. Proc Natl Acad Sci USA 2009, 106:6730-6735.
3. Savina A., Jancic C., Hugues S., Guermonprez P., Vargas P., Moura I.C., Lennon-Dumenil A.M., Seabra M.C., Raposo G., Amigorena S. NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 2006, 126:205-218.
4. Cebrian I., Visentin G., Blanchard N., Jouve M., Bobard A., Moita C., Enninga J., Moita L.F., Amigorena S., Savina A. Sec22b regulates phagosomal maturation and antigen crosspresentation by dendritic cells. Cell 2011, 147:1355-1368.
5. Burgdorf S., Kautz A., Bohnert V., Knolle P.A., Kurts C. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8T cell activation. Science 2007, 316:612-616.
6. Chatterjee B., Smed-Sorensen A., Cohn L., Chalouni C., Vandlen R., Lee B.C., Widger J., Keler T., Delamarre L., Mellman I. Internalization and endosomal degradation of receptor-bound antigens regulate the efficiency of cross presentation by human dendritic cells. Blood 2012, 120:2011-2020.
7. den Haan J.M., Lehar S.M., Bevan M.J. CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med 2000, 192:1685-1696.
8. 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.
9. 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., et al. Differential antigen processing by dendritic cell subsets in vivo. Science 2007, 315:107-111.
10. Savina A., Peres A., Cebrian I., Carmo N., Moita C., Hacohen N., Moita L.F., Amigorena S. The small GTPase Rac2 controls phagosomal alkalinization and antigen crosspresentation selectively in CD8(+) dendritic cells. Immunity 2009, 30:544-555.
11. Delamarre L., Pack M., Chang H., Mellman I., Trombetta E.S. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 2005, 307:1630-1634.
12. den Haan J.M., Bevan M.J. Constitutive versus activation-dependent cross-presentation of immune complexes by CD8(+) and CD8(-) dendritic cells in vivo. J Exp Med 2002, 196:817-827.
13. 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., et al. Neonatal Fc receptor for IgG (FcRn) regulates cross-presentation of IgG immune complexes by CD8-CD11b+ dendritic cells. Proc Natl Acad Sci USA 2011, 108:9927-9932.
14. Backer R., van Leeuwen F., Kraal G., den Haan J.M. CD8-dendritic cells preferentially cross-present Saccharomyces cerevisiae antigens. Eur J Immunol 2008, 38:370-380.
15. Kamphorst A.O., Guermonprez P., Dudziak D., Nussenzweig M.C. Route of antigen uptake differentially impacts presentation by dendritic cells and activated monocytes. J Immunol 2010, 185:3426-3435.
16. Bachem A., Guttler S., Hartung E., Ebstein F., Schaefer M., Tannert A., Salama A., Movassaghi K., Opitz C., Mages H.W., et al. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as homologues of mouse CD8+ dendritic cells. J Exp Med 2010, 207:1273-1281.
17. Crozat K., Guiton R., Contreras V., Feuillet V., Dutertre C.A., Ventre E., Vu Manh T.P., Baranek T., Storset A.K., Marvel J., et al. The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8alpha+ dendritic cells. J Exp Med 2010, 207:1283-1292.
18. 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., et al. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 2010, 207:1247-1260.
19. Poulin L.F., Salio M., Griessinger E., Anjos-Afonso F., Craciun L., Chen J.L., Keller A.M., Joffre O., Zelenay S., Nye E., et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J Exp Med 2010, 207:1261-1271.
20. Segura E., Durand M., Amigorena S. Similar antigen cross-presentation capacity and phagocytic functions in all freshly isolated human lymphoid organ-resident dendritic cells. J Exp Med 2013, 210:1035-1047.
21. Cohn L., Chatterjee B., Esselborn F., Smed-Sorensen A., Nakamura N., Chalouni C., Lee B.C., Vandlen R., Keler T., Lauer P., et al. Antigen delivery to early endosomes eliminates the superiority of human blood BDCA3+ dendritic cells at cross presentation. J Exp Med 2013, 210:1049-1063.
22. Segura E., Villadangos J.A., Modular A. Combinatorial view of the antigen cross-presentation pathway in dendritic cells. Traffic 2011, 12:1677-1685.
23. Schreibelt G., Klinkenberg L.J., Cruz L.J., Tacken P.J., Tel J., Kreutz M., Adema G.J., Brown G.D., Figdor C.G., de Vries I.J. The C-type lectin receptor CLEC9A mediates antigen uptake and (cross-)presentation by human blood BDCA3+ myeloid dendritic cells. Blood 2012, 119:2284-2292.
24. Zelenay S., Keller A.M., Whitney P.G., Schraml B.U., Deddouche S., Rogers N.C., Schulz O., Sancho D., Reis e Sousa C. The dendritic cell receptor DNGR-1 controls endocytic handling of necrotic cell antigens to favor cross-priming of CTLs in virus-infected mice. J Clin Invest 2012, 122:1615-1627.
25. Iborra S., Izquierdo H.M., Martinez-Lopez M., Blanco-Menendez N., Reis e Sousa C., Sancho D. The DC receptor DNGR-1 mediates cross-priming of CTLs during vaccinia virus infection in mice. J Clin Invest 2012, 122:1628-1643.
26. Tacken P.J., Ginter W., Berod L., Cruz L.J., Joosten B., Sparwasser T., Figdor C.G., Cambi A. Targeting DC-SIGN via its neck region leads to prolonged antigen residence in early endosomes, delayed lysosomal degradation, and cross-presentation. Blood 2011, 118:4111-4119.
27. Kutomi G., Tamura Y., Okuya K., Yamamoto T., Hirohashi Y., Kamiguchi K., Oura J., Saito K., Torigoe T., Ogawa S., et al. Targeting to static endosome is required for efficient cross-presentation of endoplasmic reticulum-resident oxygen-regulated protein 150-peptide complexes. J Immunol 2009, 183:5861-5869.
28. Bertholet S., Goldszmid R., Morrot A., Debrabant A., Afrin F., Collazo-Custodio C., Houde M., Desjardins M., Sher A., Sacks D. Leishmania antigens are presented to CD8+ T cells by a transporter associated with antigen processing-independent pathway in vitro and in vivo. J Immunol 2006, 177:3525-3533.
29. Shen L., Sigal L.J., Boes M., Rock K.L. Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo. Immunity 2004, 21:155-165.
30. Rock K.L., Shen L. Cross-presentation: underlying mechanisms and role in immune surveillance. Immunol Rev 2005, 207:166-183.
31. Kovacsovics-Bankowski M., Rock K.L. A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science 1995, 267:243-246.
32. Ackerman A.L., Kyritsis C., Tampe R., Cresswell P. Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc Natl Acad Sci USA 2003, 100:12889-12894.
33. Singh R., Cresswell P. Defective cross-presentation of viral antigens in GILT-free mice. Science 2010, 328:1394-1398.
34. West L.C., Cresswell P. Expanding roles for GILT in immunity. Curr Opin Immunol 2013, 25:103-108.
35. Neefjes J., Sadaka C. Into the intracellular logistics of cross-presentation. Front Immunol 2012, 3:31.
36. Ackerman A.L., Giodini A., Cresswell P. A role for the endoplasmic reticulum protein retrotranslocation machinery during crosspresentation by dendritic cells. Immunity 2006, 25:607-617.
37. Zehner M., Chasan A.I., Schuette V., Embgenbroich M., Quast T., Kolanus W., Burgdorf S. Mannose receptor polyubiquitination regulates endosomal recruitment of p97 and cytosolic antigen translocation for cross-presentation. Proc Natl Acad Sci USA 2011, 108:9933-9938.
38. Imai J., Hasegawa H., Maruya M., Koyasu S., Yahara I. Exogenous antigens are processed through the endoplasmic reticulum-associated degradation (ERAD) in cross-presentation by dendritic cells. Int Immunol 2005, 17:45-53.
39. Lin M.L., Zhan Y., Villadangos J.A., Lew A.M. The cell biology of cross-presentation and the role of dendritic cell subsets. Immunol Cell Biol 2008, 86:353-362.
40. Koopmann J.O., Albring J., Huter E., Bulbuc N., Spee P., Neefjes J., Hammerling G.J., Momburg F. Export of antigenic peptides from the endoplasmic reticulum intersects with retrograde protein translocation through the Sec61p channel. Immunity 2000, 13:117-127.
41. Imai T., Kato Y., Kajiwara C., Mizukami S., Ishige I., Ichiyanagi T., Hikida M., Wang J.Y., Udono H. Heat shock protein 90 (HSP90) contributes to cytosolic translocation of extracellular antigen for cross-presentation by dendritic cells. Proc Natl Acad Sci USA 2011, 108:16363-16368.
42. Oura J., Tamura Y., Kamiguchi K., Kutomi G., Sahara H., Torigoe T., Himi T., Sato N. Extracellular heat shock protein 90 plays a role in translocating chaperoned antigen from endosome to proteasome for generating antigenic peptide to be cross-presented by dendritic cells. Int Immunol 2011, 23:223-237.
43. Houde M., Bertholet S., Gagnon E., Brunet S., Goyette G., Laplante A., Princiotta M.F., Thibault P., Sacks D., Desjardins M. Phagosomes are competent organelles for antigen cross-presentation. Nature 2003, 425:402-406.
44. Guermonprez P., Saveanu L., Kleijmeer M., Davoust J., Van Endert P., Amigorena S. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 2003, 425:397-402.
45. Burgdorf S., Scholz C., Kautz A., Tampe R., Kurts C. Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat Immunol 2008, 9:558-566.
46. Fiegl D., Kagebein D., Liebler-Tenorio E.M., Weisser T., Sens M., Gutjahr M., Knittler M.R. Amphisomal route of MHC class I cross-presentation in bacteria-infected dendritic cells. J Immunol 2013, 190:2791-2806.
47. Saveanu L., Carroll O., Weimershaus M., Guermonprez P., Firat E., Lindo V., Greer F., Davoust J., Kratzer R., Keller S.R., et al. IRAP identifies an endosomal compartment required for MHC class I cross-presentation. Science 2009, 325:213-217.
48. Weimershaus M., Maschalidi S., Sepulveda F., Manoury B., van Endert P., Saveanu L. Conventional dendritic cells require IRAP-Rab14 endosomes for efficient cross-presentation. J Immunol 2012, 188:1840-1846.
49. Firat E., Saveanu L., Aichele P., Staeheli P., Huai J., Gaedicke S., Nil A., Besin G., Kanzler B., van Endert P., et al. The role of endoplasmic reticulum-associated aminopeptidase 1 in immunity to infection and in cross-presentation. J Immunol 2007, 178:2241-2248.
50. Burgdorf S., Lukacs-Kornek V., Kurts C. The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J Immunol 2006, 176:6770-6776.
51. Gagnon E., Duclos S., Rondeau C., Chevet E., Cameron P.H., Steele-Mortimer O., Paiement J., Bergeron J.J., Desjardins M. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 2002, 110:119-131.
52. Goldszmid R.S., Coppens I., Lev A., Caspar P., Mellman I., Sher A. Host ER-parasitophorous vacuole interaction provides a route of entry for antigen cross-presentation in Toxoplasma gondii-infected dendritic cells. J Exp Med 2009, 206:399-410.
53. Grotzke J.E., Lu Q., Cresswell P. Deglycosylation-dependent fluorescent proteins provide unique tools for the study of ER-associated degradation. Proc Natl Acad Sci USA 2013, 110:3393-3398.
54. Savina A., Vargas P., Guermonprez P., Lennon A.M., Amigorena S. Measuring pH, ROS production, maturation, and degradation in dendritic cell phagosomes using cytofluorometry-based assays. Methods Mol Biol 2010, 595:383-402.
55. Zehner M., Rauen J., Chasan A.I., Embgenbroich M., Camps M.G., Kaden S., Haas A., Kurts C., Endl E., Beyer M., et al. Intraendosomal flow cytometry: a novel approach to analyze the protein composition of antigen-loaded endosomes. Eur J Immunol 2012, 42:2187-2190.
56. Chasan A.I., Beyer M., Kurts C., Burgdorf S. Isolation of a specialized, antigen-loaded early endosomal subpopulation by flow cytometry. Methods Mol Biol 2013, 960:379-388.