MHC class II restricted antigen presentation

Current Opinion in Immunology

Volumn 9, Issue 1, 1997, Pages 89-96

  Pieters, Jean ^a  

^a BASEL INSTITUTE FOR IMMUNOLOGY   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

HLA D ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; ENDOSOME; HELPER CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; T LYMPHOCYTE;

EID: 0031059765     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(97)80164-1     Document Type: Article

References (84)

1. Pober JS, Collins T, Gimbrone MA Jr, Cotran RS, Gitlin JD, Fiers W, Clayberger C, Krensky AM, Burakoff SJ, Reiss CS. Lymphocytes recognize human vascular endothelial and dermal fibroblast la antigens induced by recombinant immune interferon. Nature. 305:1983;726-729.
2. Kern I, Steimle V, Siegrist CA, Mach B. The two novel MHC class II transactivators RFX5 and CIITA both control expression of HLA-DM genes. Int Immunol. 7:1995;1295-1299 This paper, together with [3], shows that the class II transactivator gene, previously shown to regulate MHC class II gene transcription, also regulates the expression of the Ii and HLA-DM molecules. This suggests that CIITA functions as a 'master control gene' for MHC class II restricted antigen presentation.
3. Chang CH, Flavell RA. Class II transactivator regulates the expression of multiple genes involved in antigen presentation. of special interest J Exp Med. 181:1995;765-767 See annotation [2].
4. Reith W, Steimle V, Mach B. Molecular defects in the bare lymphocyte syndrome and regulation of MHC class II genes. Immunol Today. 16:1995;539-546.
5. Kvist S, Wiman K, Claesson L, Peterson PA, Dobberstein B. Membrane insertion and oligomeric assembly of HLA-DR histocompatibility antigens. Cell. 29:1982;61-69.
6. Hurtley SM, Helenius A. Protein oligomerization in the endoplasmic reticulum. Annu Rev Cell Biol. 5:1989;277-307.
7. Schaiff WT, Hruska KA Jr, McCourt DW, Green M, Schwartz BD. HLA-DR associates with specific stress proteins and is retained in the endoplasmic reticulum in invariant chain negative cells. J Exp Med. 176:1992;657-666.
8. Marks MS, Germain RN, Bonifacino JS. Transient aggregation of major histocompatibility complex class II chains during assembly in normal spleen cells. J Biol Chem. 270:1995;10475-10481.
9. Arunachalam B, Cresswell P. Molecular requirements for the interaction of class II major histocompatibility complex molecules and invariant chain with calnexin. J Biol Chem. 270:1995;2784-2790.
10. Romagnoli P, Germain RN. Inhibition of invariant chain (ii) - calnexin interaction results in enhanced degradation of Ii but does not prevent the assembly of αβ Ii complexes. J Exp Med. 182:1995;2027-2036.
11. Bikoff EK, Germain RN, Robertson EJ. Allelic differences affecting invariant chain dependency of MHC class II subunit assembly. Immunity. 2:1995;301-310.
12. Roche PA, Marks MS, Cresswell P. Formation of a nine-subunit complex by HLA class II glycoproteins and the invariant chain. Nature. 354:1991;392-394.
13. Cresswell P. Invariant chain structure and MHC class II function. Cell. 84:1996;505-507.
14. Bertolino P, Staschewski M, Trescol Biemont MC, Freisewinkel IM, Schenck K, Chretien I, Forquet F, Gerlier D, Rabourdin Combe C, Koch N. Deletion of a C-terminal sequence of the class II-associated invariant chain abrogates invariant chains oligomer formation and class II antigen presentation. J Immunol. 154:1995;5620-5629.
15. Jasanoff A, Park SJ, Wiley DC. Direct observation of disordered regions in the major histocompatibility complex class II-associated invariant chain. Proc Natl Acad Sci USA. 92:1995;9900-9904.
16. Park SJ, Sadegh Nasseri S, Wiley DC. Invariant chain made in Escherichia coli has an exposed N-terminal segment that blocks antigen binding to HLA-DR1 and a trimeric C-terminal segment that binds empty HLA-DR1. Proc Natl Acad Sci USA. 92:1995;11289-11293.
17. Ghosh P, Amaya M, Mellins E, Wiley DC. The structure of an intermediate in class II MHC maturation: CLIP bound to HLA-DR3. of outstanding interest Nature. 378:1995;457-462 Determination of the X-ray crystal structure of the MHC class II-CLIP complex. It is shown that CLIP resides in the MHC class II binding groove in a manner similar to that of antigenic peptides.
18. Wolf PR, Ploegh HL. How MHC class II molecules acquire peptide cargo: biosynthesis and trafficking through the endocytic pathway. Annu Rev Cell Dev Biol. 11:1995;267-306.
19. Amigorena S, Webster P, Drake J, Newcomb J, Cresswell P, Mellman I. Invariant chain cleavage and peptide loading in major histocompatibility complex class II vesicles. J Exp Med. 181:1995;1729-1741.
20. Freisewinkel IM, Schenck K, Koch N. The segment of invariant chain that is critical for association with major histocompatibility complex class II molecules contains the sequence of a peptide eluted from class II polypeptides. Proc Natl Acad Sci USA. 90:1993;9703-9706.
21. Stern LJ, Brown JH, Jardetzky TS, Gorga JC, Urban RG, Strominger JL, Wiley DC. Crystal structure of the human class II MHC protein HLA-DR1 complexed with an influenza virus peptide. Nature. 368:1994;215-221.
22. Sette A, Southwood S, Miller J, Appella E. Binding of major histocompatibility complex class II to the invariant chain-derived peptide, CLIP, is regulated by allelic polymorphism in class II. J Exp Med. 181:1995;677-683.
23. Lotteau V, Teyton L, Peleraux A, Nilsson T, Karlsson L, Schmid SL, Quaranta V, Peterson PA. Intracellular transport of class II MHC molecules directed by invariant chain. Nature. 348:1990;600-605.
24. Bakke O, Dobberstein B. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell. 63:1990;707-716.
25. Pieters J, Bakke O, Dobberstein B. The MHC class II-associated invariant chain contains two endosomal sorting signals within its cytoplasmic tail. J Cell Sci. 106:1993;831-846.
26. Arneson LS, Miller J. Efficient endosomal localization of major histocompatibility complex class II-invariant chain complexes requires multimerization of the invariant chain targeting sequence. of special interest J Cell Biol. 129:1995;1217-1228 An elegant study that reveals the relative contribution of different Ii isoforms within a single Ii trimer in targeting to endocytic compartments. Multimerization of Ii was found to be required for efficient trans-Golgi network to endosome targeting of class II-Ii complexes.
27. Warmerdam PA, Long EO, Roche PA. Isoforms of the invariant chain regulate transport of MHC class II molecules to antigen processing compartments. J Cell Biol. 133:1996;281-291.
28. Kornfeld S, Mellman I. The biogenesis of lysosomes. Annu Rev Cell Biol. 5:1989;483-525.
29. Peters PJ, Neefjes JJ, Oorschot V, Ploegh HL, Geuze HJ. Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments. Nature. 349:1991;669-676.
30. Pieters J, Horstmann H, Bakke O, Griffiths G, Lipp J. Intracellular transport and localization of major histocompatibility complex class II molecules and associated invariant chain. J Cell Biol. 115:1991;1213-1223.
31. Tulp A, Verwoerd D, Dobberstein B, Ploegh HL, Pieters J. Isolation and characterization of the intracellular MHC class II compartment. Nature. 369:1994;120-126.
32. Amigorena S, Drake JR, Webster P, Mellman I. Transient accumulation of new MHC molecules in a novel endocyic compartment in B lymphocytes. Nature. 369:1994;113-120.
33. West MA, Lucocq JM, Watts C. Antigen processing and class II MHC peptide-loading compartments in human B-lymphoblastoid cells. Nature. 369:1994;147-151.
34. 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.
35. 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.
36. Peters PJ, Raposo G, Neefjes JJ, Oorschot V, Leijendekker RL, Geuze HJ, Ploegh HL. Major histocompatibility complex class II compartments in human B lymphoblastoid cells are distinct from early endosomes. J Exp Med. 182:1995;325-334.
37. Glickman JN, Morton PA, Slot JW, Kornfeld S, Geuze HJ. The biogenesis of the MHC class II compartment in human I-cell disease B lymphoblasts. J Cell Biol. 132:1996;769-785.
38. Raposo G, Nijman HW, Stoorvogel W, Leijendekker R, Harding CV, Melief CJM, Geuze HJ. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 183:1996;1161-1172.
39. Blum JS, Cresswell P. Role for intracellular proteases in the processing and transport of class II HLA antigens. Proc Natl Acad Sci USA. 85:1988;3975-3979.
40. of outstanding interest Fineschi B, Arneson LS, Naujokas MF, Miller J. Proteolysis of major histocompatibility complex class II-associated invariant chain is regulated by the alternatively spliced gene product, p41. of special interest Proc Natl Acad Sci USA. 92:1995;10257-10261 The alternatively spliced variant of Ii, IiP41, can enhance antigen presentation of a subset of antigens, but the mechanism underlying this enhancement is unknown. Thus far, IiP31 and IiP41 were shown to have similar activities in MHC class II transport. This paper reports the surprising finding that IiP41 is able to alter the proteolysis of IiP31, when expressed within the same cell. See also [47,48].
41. + T cell function in mice lacking the p41 isoform of invariant chain. Immunity. 3:1995;385-396.
42. + T cell development. Immunity. 3:1995;359-372.
43. Shachar I, Elliott EA, Chasnoff B, Grewal IS, Flavell RA. Reconstitution of invariant chain function in transgenic mice in vivo by individual p31 and p41 isoforms. Immunity. 3:1995;373-383.
44. Peterson M, Miller J. Antigen presentation enhanced by the alternatively spliced invariant chain gene product p41. Nature. 357:1992;596-598.
45. Koch N, Lauer W, Habicht J, Dobberstein B. Primary structure of the gene for the murine is antigen-associated invariant chains (Ii). An alternatively spliced exon encodes a cysteine-rich domain highly homologous to a repetitive sequence of thyroglobulin. EMBO J. 6:1987;1677-1683.
46. Herzog S. Regulation of the cellular transport and compactation of thyroglobulin. Exp Clin Endocrinol. 100:1992;12-12.
47. of outstanding interest Bevec T, Stoka V, Pungercic G, Dolenc I, Turk V. Major histocompatibility complex class II-associated p41 invariant chain fragment is a strong inhibitor of lysosomal cathepsin L. of special interest J Exp Med. 183:1996;1331-1338 The alternatively spliced exon that is present in IiP41, but not in IiP31, is shown to be a potent inhibitor for the cysteine protease cathepsin L. This suggest a regulatory role for IiP41 in modulating the activity of endosomal/lysosomal proteases. See also [40,48].
48. of outstanding interest Riese RJ, Wolf PR, Bromme D, Natkin LR, Villadangos JA, Ploegh HL, Chapman HA. Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. of special interest Immunity. 4:1996;357-366 This study provides evidence that the cysteine protease cathepsin S plays an important role in the degradation of MHC class II associated Ii. Cathepsin S mediated digestion of MHC class II-Ii complexes in vitro generates αβ-CLIP complexes, that can be readily loaded with antigenic peptides. See also [40,47].
49. Mellins E, Smith L, Arp B, Cotner T, Celis E, Pious D. Defective processing and presentation of exogenous antigens in mutants with normal HLA class II genes. Nature. 343:1990;71-74.
50. Denzin LK, Robbins NF, Carboy Newcomb C, Cresswell P. Assembly and intracellular transport of HLA-DM and correction of the class II antigen-processing defect in T2 cells. Immunity. 1:1994;595-606.
51. Roche PA. HLA-DM: an in vivo facilitator of MHC class II peptide loading. Immunity. 3:1995;259-262.
52. Cho S, Attaya M, Monaco JJ. New class-ii like genes in the murine MHC. Nature. 353:1990;573-576.
53. Kelly AP, Monaco JJ, Cho S, Trowsdale J. A new human HLA class II-related locus, DM. Nature. 353:1990;517-573.
54. 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. of outstanding interest Nature. 375:1995;802-806 These studies, together with [55,56], provide the first insight into the biological activity of HLA-DM molecules. In vitro reconstitution of antigenic peptide loading onto MHC class II molecules was used to demonstrate that at low pH, HLA-DM acts as a catalyst that exchanges the CLIP peptide for antigenic peptides onto MHC class II molecules.
55. Denzin LK, Cresswell P. HLA-DM induces CLIP dissociation from MHC class II αβ dimers and facilitates peptide loading. of outstanding interest Cell. 82:1995;155-165 See annotation [54].
56. Sherman MA, Weber DA, Jensen PE. DM enhances peptide binding to class II MHC by release of invariant chain-derived peptide. of outstanding interest Immunity. 3:1995;197-205 See annotation [54].
57. 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.
58. Pierre P, Denzin LK, Hammond C, Drake JR, Amigorena S, Cresswell P, Mellman I. HLA-DM is localized to conventional and unconventional MHC class II-containing endocytic compartments. Immunity. 4:1996;229-239.
59. Sanderson F, Thomas C, Neefjes J, Trowsdale J. Association between HLA-DM and HLA-DR in vivo. Immunity. 4:1996;87-96.
60. Lindstedt R, Liljedahl M, Peleraux A, Peterson PA, Karlsson L. The MHC class II molecule H2-M is targeted to an endosomal compartment by a tyrosine-based targeting motif. Immunity. 3:1995;561-572.
61. Marks MS, Roche PA, Van Donselaar E, Woodruff L, Peters PJ, Bonifacino JS. A lysosomal targeting signal in the cytoplasmic tail of the β chain directs HLA-DM to MHC class II compartments. J Cell Biol. 131:1995;351-369.
62. Chervonsky AV, Gordon L, Sant A. A segment in the MHC class II β chain plays a critical role in targeting class II molecules to the endocytic pathway. Int Immunol. 6:1994;973-982.
63. Smiley ST, Rudensky AY, Glimcher LH, Grusby MJ. Truncation of the class II beta-chain cytoplasmic domain influences the level of class II-invariant chain-derived peptide complexes. Proc Natl Acad Sci USA. 93:1996;241-244.
64. Vogt AB, Kropshofer H, Moldenhauer G, Hammerling GJ. Kinetic analysis of peptide loading onto HLA-DR molecules mediated by HLA-DM. Proc Natl Acad Sci USA. 93:1996;9724-9729.
65. Liljedahl M, Kuwana T, Fung-Leung W-P, Jackson MR, Peterson PA, Karlsson L. HLA-DO is a lysosomal resident which requires association with HLA-DM for efficient intracellular transport. of special interest EMBO J. 15:1996;4817-4824 This study shows that another MHC encoded molecule of unknown function, HLA-DO, associates and colocalizes with HLA-DM. It is suggested that HLA-DO is involved in regulating HLA-DM activity.
66. Miyazaki T, Wolf P, Tourne S, Waltzinger C, Dierich A, Barois N, Ploegh H, Benoist C, Mathis D. Mice lacking H2-M complexes, enigmatic elements of the MHC class II peptide-loading pathway. of outstanding interest Cell. 84:1996;531-541 Description of mice lacking H2-M, the mouse HLA-DM homologues (together with [67,68]). It is shown that presentation of intact antigens as well as peptides is severely impaired, and the MHC class II molecules at the cell surface are associated almost exclusively with CLIP. Strikingly, positive selection is normal in these mice, suggesting that a single αβ - CLIP complex is sufficient for the selection of a broad repertoire. See also [67,68,71].
67. Martin WD, Hicks GG, Mendiratta SK, Leva HI, Ruley HE, Vankaer L. H2-M mutant mice are defective in the peptide loading of class II molecules, antigen presentation, and T cell repertoire selection. of outstanding interest Cell. 84:1996;543-550 See annotation [66].
68. Fung-Leung W-P, Surh CD, Liljedahl M, Pang J, Leturcq D, Peterson PA, Webb SR, Karlsson L. Antigen presentation and T cell development in H2-M-deficient mice. of outstanding interest Science. 271:1996;1278-1281 See annotation [66].
69. Von Boehmer H. Positive selection of lymphocytes. Cell. 76:1994;219-228.
70. Lucas B, Germain RN. T-cell repertoire: political correctness in the immune system. Curr Biol. 6:1996;783-787.
71. + T cells are positively selected quite efficiently. Thus, a single MHC/peptide ligand is sufficient for selection of a broad repertoire. See also [66].
72. Long EO, Roche PA, Malnati MS, LaVaute T, Pinet V. Multiple pathways of antigen processing for MHC class II restricted presentation. Humphreys RE, Pierce SK. Antigen Processing and Presentation. 1994;Academic Press.
73. Stebbins CC, Loss GE Jr, Elias CG, Chervonsky A, Sant AJ. The requirement for DM in class II-restricted antigen presentation and SDS-stable dimer formation is allele and species dependent. J Exp Med. 181:1995;223-234.
74. Kropshofer H, Vogt AB, Stern LJ, Hammerling GJ. Self-release of CLIP in peptide loading of HLA-DR molecules. of special interest Science. 270:1995;1357-1359 This study reveals the presence of a sequence in CLIP that has the ability to induce release of the CLIP peptide from MHC class II molecules at low pH. This might explain peptide loading events that occur in the absence of HLA-DM.
75. Pinet V, Vergelli M, Martin R, Bakke O, Long EO. Antigen presentation mediated by recycling of surface HLA-DR molecules. of special interest Nature. 375:1995;603-606 MHC class II heterodimers that lack cytoplasmic tails are unable to recycle after internalization from the plasma membrane. These truncated class II molecules cannot present peptides from internalized antigens anymore, suggesting that this peptide loading occurs in early endosomes.
76. 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. J Exp Med. 182:1995;389-400.
77. 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. Nature. 375:1995;151-155.
78. Berthiaume EP, Medina C, Swanson JA. Molecular size-fractionation during endocytosis in macrophages. J Cell Biol. 129:1995;989-998.
79. Bonnerot C, Lankar D, Hanau D, Spehner D, Davoust J, Salamero J, Fridman WH. Role of B cell receptor Ig α and Ig β subunits in MHC class II-restricted antigen presentation. of special interest Immunity. 3:1995;335-347 This study shows that Igα and Igβ association with the membrane immunoglobulin receptor determines the intracellular site to which these complexes are targeted. Igα is shown to be responsible for targeting antigen to MIICs, whereas Igβ directs the antigen to early endosomes.
80. Mitchell RN, Barnes KA, Grupp SA, Sanchez M, Misulovin Z, Nussenzweig MC, Abbas AK. Intracellular targeting of antigens internalized by membrane immunoglobulin in B lymphocytes. J Exp Med. 181:1995;1705-1714.
81. Viner NJ, Nelson CA, Deck B, Unanue ER. Complexes generated by the binding of free peptides to class II MHC molecules are antigenically diverse compared with those generated by intracellular processing. J Immunol. 156:1996;2365-2368.
82. Lanzavecchia A. Mechanisms of antigen uptake for presentation. Curr Opin Immunol. 8:1996;348-354.
83. Pierce SK. Molecular chaperones in the processing and presentation of antigen to helper T cells. Experientia. 50:1994;1026-1030.
84. Rammensee HG. Chemistry of peptides associated with MHC class I and class II molecules. Curr Opin Immunol. 7:1995;85-96.