Mechanisms of antigen uptake for presentation

Current Opinion in Immunology

Volumn 8, Issue 3, 1996, Pages 348-354

  Lanzavecchia, Antonio ^a  

^a BASEL INSTITUTE FOR IMMUNOLOGY   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MANNOSE RECEPTOR;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; DENDRITIC CELL; INTRACELLULAR TRANSPORT; PINOCYTOSIS; REVIEW;

EID: 0030175501     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(96)80124-5     Document Type: Article

References (93)

1. Lanzavecchia A, Reid PA, Watts C. Irreversible association of peptides with class II MHC molecules in living cells. Nature. 357:1992;249-252. [see comments].
2. Nelson CA, Petzold SJ, Unanue ER. Peptides determine the lifespan of MHC class II molecules in the antigen-presenting cell. Nature. 371:1994;250-252.
3. Lanzavecchia A. Antigen uptake and accumulation in antigen-specific B cells. Immunol Rev. 99:1987;39-51.
4. Demotz S, Grey HM, Sette A. The minimal number of class II MHC-antigen complexes needed for T cell activation. Science. 249:1990;1028-1030.
5. Harding CV, Unanue ER. Quantitation of antigen-presenting cell MHC class II-peptide complexes necessary for T-cell stimulation. Nature. 346:1990;574-576.
6. Valitutti S, Muller S, Cella M, Padovan E, Lanzavecchia A. Serial triggering of many T-cell receptors by a few peptide - MHC complexes. [see comments] Nature. 375:1995;148-151 Demonstration that few peptide - MHC complexes can trigger many TCRs during the prolonged interaction between T cells and APCs.
7. of outstanding interest Steinman RM. The dendritic cell system and its role in immunogenicity. Annu Rev Immunol. 9:1991;271-296.
8. Steinman RM, Swanson J. The endocytic activity of dendritic cells [comment]. J Exp Med. 182:1995;283-288.
9. Stossel H, Koch F, Kampgen E, Stoger P, Lenz A, Heufler C, Romani N, Schuler G. Disappearance of certain acidic organelles (endosomes and Langerhans cell granules) accompanies loss of antigen processing capacity upon culture of epidermal Langerhans cells. J Exp Med. 172:1990;1471-1482.
10. Romani N, Koide S, Crowley M, Witmer-Pack M, Livingstone AM, Fathman CG, Inaba K, Steinman RM. Presentation of exogenous protein antigens by dendritic cells to T cell clones. Intact protein is presented best by immature, epidermal Langerhans cells. J Exp Med. 169:1989;1169-1178.
11. Inaba K, Metlay JP, Crowley MT, Steinman RM. Dendritic cells pulsed with protein antigens in vitro can prime antigen-specific, MHC-restricted T cells in situ. [Published erratum appears in J Exp Med 1990, 172: 1275.] J Exp Med. 172:1990;631-640.
12. Pure E, Inaba K, Crowley MT, Tardelli L, Witmer-Pack MD, Ruberti G, Fathman G, Steinman RM. Antigen processing by epidermal Langerhans cells correlates with the level of biosynthesis of major histocompatibility complex class II molecules and expression of invariant chain. J Exp Med. 172:1990;1459-1469.
13. Sallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med. 179:1994;1109-1118 Describes the generation of DCs from human monocytes using GM-CSF and IL-4. These cells are very efficient at presenting soluble antigens.
14. of outstanding interest Sallusto F, Cella M, Danieli C, Lanzavecchia A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. [see comments] J Exp Med. 182:1995;389-400 Demonstration that DCs can use macropinocytosis to concentrate macrosolutes and the mannose receptor to capture a variety of glycosylated molecules. TNF-α, IL-1 and LPS induce downregulation of endocytic capacity and upregulation of adhesion and costimulatory molecules.
15. of outstanding interest Swanson JA, Watts C. Macropinocytosis. of special interest Trends Cell Biol. 5:1995;424-426 A recent review on macropinocytosis in different cell types.
16. Racoosin EL, Swanson JA. Macropinosome maturation and fusion with tubular lysosomes in macrophages. J Cell Biol. 121:1993;1011-1020.
17. Hewlett LJ, Prescott AR, Watts C. The coated pit and macropinocytic pathways serve distinct endosome populations. J Cell Biol. 124:1994;689-703.
18. Manca F, Fenoglio D, Li-Pira G, Kunkl A, Celada F. Effect of antigen/antibody ratio on macrophage uptake, processing, and presentation to T cells of antigen complexed with polyclonal antibodies. J Exp Med. 173:1991;37-48.
19. Ezekowitz RA, Sastry K, Bailly P, Warner A. Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells. J Exp Med. 172:1990;1785-1794.
20. Stahl PD. The mannose receptor and other macrophage lectins. Curr Opin Immunol. 4:1992;49-52.
21. Jiang W, Swiggard WJ, Heufler C, Peng M, Mirza A, Steinman RM, Nussenzweig MC. The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing. of outstanding interest Nature. 375:1995;151-155 Identification of a novel C-type lectin that may be involved in antigen capture in mouse dendritic cells.
22. Maurer D, Ebner C, Reininger B, Fiebiger E, Kraft D, Kinet JP, Stingl G. The high affinity IgE receptor (Fc εRI) mediates IgE-dependent allergen presentation. [Published erratum appears in Curr Opin Immunol 1993, 5:566.] J Immunol. 154:1995;6285-6290.
23. Sastry K, Ezekowitz RA. Collectins: pattern recognition molecules involved in first line host defense. Curr Opin Immunol. 5:1993;59-66.
24. Inaba K, Inaba M, Naito M, Steinman RM. Dendritic cell progenitors phagocytose particulates, including bacillus Calmette - Guerin organisms, and sensitize mice to mycobacterial antigens in vivo. J Exp Med. 178:1993;479-488.
25. Reis-e-Sousa C, Stahl PD, Austyn JM. Phagocytosis of antigen by Langerhans cells in vitro. J Exp Med. 178:1993;509-519.
26. Nijman HW, Kleijmeer MJ, Ossevoort MA, Oorschot VM, Vierboom MP, Van-de-Keur M, Kenemans P, Kast WM, Geuze HJ, Melief CJ. Antigen capture and major histocompatibility class II compartments of freshly isolated and cultured human blood dendritic cells. J Exp Med. 182:1995;163-174.
27. Kleijmeer MJ, Ossevoort MA, Van-Veen CJ, Van-Hellemond JJ, Neefjes JJ, Kast WM, Melief CJ, Geuze HJ. MHC class II compartments and the kinetics of antigen presentation in activated mouse spleen dendritic cells. J Immunol. 154:1995;5715-5724.
28. Roake JA, Rao AS, Morris PJ, Larsen CP, Hankins DF, Austyn JM. Dendritic cell loss from nonlymphoid tissues after systemic administration of lipopolysaccharide, tumor necrosis factor, and interleukin 1. J Exp Med. 181:1995;2237-2247 Demonstration that inflammatory stimuli can induce dendritic cell migration out of nonlymphoid tissues.
29. [Published erratum appears in Curr Opin Immunol 1993, 5:566.] Patel KJ, Neuberger MS. Antigen presentation by the B cell antigen receptor is driven by the alpha/beta sheath and occurs independently of its cytoplasmic tyrosines. Cell. 74:1993;939-946.
30. Mitchell RN, Barnes KA, Grupp SA, Sanchez M, Misulovin Z, Nussenzweig MC, Abbas AK. Intracellular targeting of antigen internalized by membrane immunoglobulin in B lymphocytes. J Exp Med. 181:1995;1705-1714.
31. Watts C, Davidson HW. Endocytosis and recycling of specific antigen by human B cell lines. EMBO J. 7:1988;1937-1945.
32. West MA, Lucocq JM, Watts C. Antigen processing and class II MHC peptide-loading compartments in human B-lymphoblastoid cells. [see comments] Nature. 369:1994;147-151.
33. Amigorena S, Salamero J, Davoust J, Fridman WH, Bonnerot C. Tyrosine-containing motif that transduces cell activation signals also determines internalization and antigen presentation via type III receptors for IgG. Nature. 358:1992;337-341.
34. Ukkonen P, Lewis V, Marsh M, Helenius A, Mellman I. Transport of macrophage Fc receptors and Fc receptor-bound ligands to lysosomes. J Exp Med. 163:1986;952-971.
35. Fearon DT, Carter RH. The CD19/CR2/TAPA-1 complex of B lymphocytes: linking natural to acquired immunity. Annu Rev Immunol. 13:1995;127-149.
36. Dempsey PW, Allison MED, Akkaraju S, Goodnow CC, Fearon DT. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science. 271:1996;348-350 This work shows that an antigen can be made 10 000×more immunogenic by engineering it to be expressed with three copies of C3d.
37. of outstanding interest Miettinen HM, Rose JK, Mellman I. Fc receptor isoforms exhibit distinct abilities for coated pit localization as a result of cytoplasmic domain heterogeneity. Cell. 58:1989;317-327.
38. Muta T, Kurosaki T, Misulovin Z, Sanchez M, Nussenzweig MC, Ravetch JV. A 13-amino-acid motif in the cytoplasmic domain of Fc γRIIB modulates B-cell receptor signalling. Nature. 368:1994;70-73.
39. D'Ambrosio D, Hippen KL, Minskoff SA, Mellman I, Pani G, Siminovitch KA, Cambier JC. Recruitment and activation of PTP1C in negative regulation of antigen receptor signaling by FcγRIIB1. of outstanding interest Science. 268:1995;293-297.
40. Takai T, Ono M, Hikida M, Ohmori H, Ravetch JV. Augmented humoral and anaphylactic responses in FcgRII-deficient mice. Nature. 379:1996;346-349.
41. Nemazee DA. Immune complexes can trigger specific, T cell-dependent autoanti-IgG antibody production in mice. J Exp Med. 161:1985;242-252.
42. Roosnek E, Lanzavecchia A. Efficient and selective presentation of antigen-antibody complexes by rheumatoid factor B cells. J Exp Med. 173:1991;487-489.
43. Tulp A, Verwoerd D, Dobberstein B, Ploegh HL, Pieters J. Isolation and characterization of the intracellular MHC class II compartment. [see comments] Nature. 369:1994;120-126.
44. Amigorena S, Drake JR, Webster P, Mellman I. Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. [see comments] Nature. 369:1994;113-120.
45. Qiu Y, Xu X, Wandinger-Ness A, Dalke DP, Pierce SK. Separation of subcellular compartments containing distinct functional forms of MHC class II. J Cell Biol. 125:1994;595-605.
46. Castellino F, Germain RN. Extensive trafficking of MHC class II-invariant chain complexes in the endocytic pathway and appearance of peptide-loaded class II in multiple compartments. Immunity. 2:1995;73-88.
47. Sloan VS, Cameron P, Porter G, Gammon M, Amaya M, Mellins E, Zaller DM. Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature. 375:1995;802-806.
48. Denzin LK, Cresswell P. HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers and facilitates peptide loading. Cell. 82:1995;155-165.
49. Reid PA, Watts C. Cycling of cell-surface MHC glycoproteins through primaquine-sensitive intracellular compartments. Nature. 346:1990;655-657.
50. Harding CV, Unanue ER. Antigen processing and intracellular Ia. Possible roles of endocytosis and protein synthesis in Ia function. J Immunol. 142:1989;12-19.
51. Davidson HW, Reid PA, Lanzavecchia A, Watts C. Processed antigen binds to newly synthesized MHC class II molecules in antigen-specific B lymphocytes. Cell. 67:1991;105-116.
52. Pinet V, Malnati MS, Long EO. Two processing pathways for the MHC class II-restricted presentation of exogenous influenza virus antigen. J Immunol. 152:1994;4852-4860.
53. Pinet V, Vergelli M, Martin R, Bakke O, Long EO. Antigen presentation mediated by recycling of surface HLA-DR molecules. Nature. 375:1995;603-606 Demonstration that recycling class II molecules can bind peptides generated in an early recycling compartment. Evidence for an alternative pathway.
54. of outstanding interest Bonnerot C, Lankar D, Hanau D, Spehner D, Davoust J, Salamero J, Fridman WH. Role of B cell receptor Ig alpha and Ig beta subunits in MHC class II-restricted antigen presentation. Immunity. 3:1995;335-347 Demonstrates that the Igα and Igβ cytoplasmic tails contain targeting signals for the MIIC and recycling class II compartment respectively.
55. of outstanding interest Watts C, Lanzavecchia A. Suppressive effect of antibody on processing of T cell epitopes. J Exp Med. 178:1993;1459-1483.
56. Simitsek PD, Campbell DG, Lanzavecchia A, Fairweather N, Watts C. Modulation of antigen processing by bound antibodies can boost or suppress class II major histocompatibility complex presentation of different T cell determinants. [see comments] J Exp Med. 181:1995;1957-1963 Describes enhancing and inhibitory effects of antibody on antigen processing.
57. of outstanding interest Lanzavecchia A. How can cryptic epitopes trigger autoimmunity? [comment]. J Exp Med. 181:1995;1945-1948.
58. Lanzavecchia A, Abrignani S, Scheidegger D, Obrist R, Dorken B, Moldenhauer G. Antibodies as antigens. The use of mouse monoclonal antibodies to focus human T cells against selected targets. J Exp Med. 167:1988;345-352.
59. Lanzavecchia A, Roosnek E, Gregory T, Berman P, Abrignani S. T cells can present antigens such as HIV gp120 targeted to their own surface molecules. Nature. 334:1988;530-532.
60. Gerlier D, Trescol-Biemont MC, Varior-Krishnan G, Naniche D, Fugier-Vivier I, Rabourdin-Combe C. Major histocompatibility complex class II-restricted presentation of measles virus relies on hemagglutin mediated targeting to its cellular receptor human CD46 expressed by murine B cells. J Exp Med. 179:1994;353-358.
61. Salemi S, Caporossi AP, Boffa L, Longobardi MG, Barnaba V. HIVgp120 activates autoreactive CD4-specific T cell responses by unveiling of hidden CD4 peptides during processing. [see comments] J Exp Med. 181:1995;2253-2257 Downregulation of membrane-bound CD4 in activated T cells results in generation of otherwise cryptic epitopes that are recognized by autoreactive T cells.
62. of outstanding interest Unanue ER. Antigen-presenting function of the macrophage. Annu Rev Immunol. 2:1984;395-428.
63. Francis CL, Ryan TA, Jones BD, Smith SJ, Falkow S. Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature. 364:1993;639-642.
64. Ginocchio CC, Olmsted SB, Wells CL, Galan JE. Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell. 76:1994;717-724.
65. Alpuche-Aranda CM, Racoosin EL, Swanson JA, Miller SI. Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes. J Exp Med. 179:1994;601-608.
66. Sibley LD, Weidner E, Krahenbuhl JL. Phagosome acidification blocked by intracellular Toxoplasma gondii. Nature. 315:1985;416-419.
67. Russel DG. Mycobacterium and Leishmania: stowaways in the endosomal network. Trends Cell Biol. 5:1995;125-128.
68. Pancholi P, Mirza A, Bhardwaj N, Steinman RM. Sequestration from immune CD4+ T cells of mycobacteria growing in human macrophages. Science. 260:1993;984-986.
69. Joiner KA, Fuhrman SA, Miettinen HM, Kasper LH, Mellman I. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science. 249:1990;641-646.
70. Bevan MJ. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in cytotoxic assay. J Exp Med. 144:1976;1283-1288.
71. Bevan MJ. Class discrimination in the world of immunology. Nature. 325:1987;192-194.
72. Huang AY, Golumbek P, Ahmadzadeh M, Jaffee E, Pardoll D, Levitsky H. Role of bone marrow-derived cells in presenting MHC class I-restricted tumor antigens. Science. 264:1994;961-965.
73. Barnaba V, Franco A, Alberti A, Benvenuto R, Balsano F. Selective killing of hepatitis B envelope antigen-specific B cells by class I-restricted, exogenous antigen-specific T lymphocytes. Nature. 345:1990;258-260.
74. Rock KL, Gamble S, Rothstein L. Presentation of exogenous antigen with class I major histocompatibility complex molecules. Science. 249:1990;918-921.
75. Rock KL, Rothstein L, Gamble S, Fleischacker C. Characterization of antigen-presenting cells that present exogenous antigens in association with class I MHC molecules. J Immunol. 150:1993;438-446.
76. Moore MW, Carbone FR, Bevan MJ. Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell. 54:1988;777-785.
77. Brunt LM, Portnoy DA, Unanue ER. Presentation of Listeria monocytogenes to CD8+ T cells requires secretion of hemolysin and intracellular bacterial growth. J Immunol. 145:1990;3540-3546.
78. Yewdell JW, Bennink JR, Hosaka Y. Cells process exogenous proteins for recognition by cytotoxic T lymphocytes. Science. 239:1988;637-640.
79. Bevan MJ. Antigen presentation to cytotoxic T lymphocytes in vivo. J Exp Med. 182:1995;639-641.
80. Kovacsovics-Bankowski M, Rock KL. A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science. 267:1995;243-246 Together with [81,82] this work shows that antigens taken up by phagocytosis can be presented on class I molecules via the classical cytosolic pathway.
81. of outstanding interest Norbury CC, Hewlett LJ, Prescot AR, Shastri N, Watts C. Class I MHC presentation of exogenous soluble antigen via macropinocytosis in bone marrow macrophages. Immunity. 3:1995;783-791 See annotation [80].
82. of outstanding interest Reis-e-Sousa C, Germain RN. Major histocompatibility complex class I presentation of peptides derived from soluble exogenous antigen by a subset of cells engaged in phagocytosis. J Exp Med. 182:1995;841-851 See annotation [80].
83. of outstanding interest Kovacsovics-Bankowski M, Clark K, Benacerraf B, Rock KL. Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc Natl Acad Sci USA. 90:1993;4942-4946.
84. Pfeifer JD, Wick MJ, Roberts RL, Findlay K, Normark SJ, Harding CV. Phagocytic processing of bacterial antigens for class I MHC presentation to T cells. Nature. 361:1993;359-362.
85. De-Bruijn ML, Jackson MR, Peterson PA. Phagocyte-induced antigen-specific activation of unprimed CD8+ T cells in vitro. Eur J Immunol. 25:1995;1274-1285.
86. Sugita M, Brenner MB. Association of the invariant chain with major histocompatibility complex class I molecules directs trafficking to endocytic compartments. J Biol Chem. 270:1995;1443-1448.
87. Bachmann MF, Oxenius A, Pircher H, Hengartner H, Ashton-Richardt PA, Tonegawa S, Zinkernagel RM. TAP1-independent loading of class I molecules by exogenous viral proteins. Eur J Immunol. 25:1995;1739-1743.
88. Srivastava PK, Udono H, Blachere NE, Li Z. Heat shock proteins transfer peptides during antigen processing and CTL priming. Immunogenetics. 39:1994;93-98.
89. Suto R, Srivastava PK. A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. of outstanding interest Science. 269:1995;1585-1588 Demonstrates that peptides associated with hsp96 can be efficiently presented by macrophages on class I molecules and induce class-I-restricted responses. See also [90].
90. Arnold D, Faath S, Rammensee H, Schild H. Cross-priming of minor histocompatibility antigen-specific cytotoxic T cells upon immunization with the heat shock protein gp96. of outstanding interest J Exp Med. 182:1995;885-889 See annotation [89].
91. Pelham HRB, Roberts LM, Lord JM. Toxin entry: how reversible is the secretory pathway? Trends Cell Biol. 2:1992;183-185.
92. Miesenbock G, Rothman JE. The capacity to retrieve escaped ER proteins extends to the trans-most cisterna of the Golgi stack. J Cell Biol. 129:1995;309-319.
93. Cella M, Scheidegger D, Palmer-Lehmann K, Lane P, Lanzavecchia A, Alber G. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. in press J Exp Med. 1996.