Selection of the MHC class II-associated peptide repertoire by HLA-DM

Immunologic Research

Volumn 16, Issue 3, 1997, Pages 261-272

  Arndt, Sven O ^a   Vogt, Anne B ^a   Hämmerling, Günter J ^a   Kropshofer, Harald ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Antigen presentation; Catalysis of loading; CLIP; Kinetic proofreading; MHC class II; Molecular chaperone; Peptide editing

Indexed keywords

CHAPERONE; HLA D ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANTIGEN PRESENTATION; HLA SYSTEM; MAJOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; REVIEW;

EID: 0030721037     PISSN: 0257277X     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02786394     Document Type: Review

References (75)

1. Germain RN: MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 1994;76:287-299.
2. Roche PA, Marks MS, Cresswell P: Formation of a nine-subunit complex by HLA class II glycoproteins and the invariant chain. Nature 1991;354:392-394.
3. Romagnoli P, Germain RN: The CLIP region of invariant chain plays a critical role in regulating major histocompatibility complex class II folding, transport, and peptide occupancy. J Exp Med 1994;180:1107-1113.
4. Marks MS, Germain RN, Bonifacino JS: Transient aggregation of major histocompatibility complex class II chains during assembly in normal spleen cells. J Biol Chem 1995; 270:10,475-10,481.
5. Roche PA, Cresswell P.: Invariant chain association with HLA-DR molecules inhibits immunogeneic peptide binding. Nature 1990;345: 615-618.
6. Vogt AB, Stern LJ, Amshoff C, Dobberstein B, Hämmerling GJ, Kropshofer H: Interference of distinct invariant chain regions with superantigen contact area and antigenic peptide binding groove of HLA-DR. J Immunol 1995;155: 4757-4765.
7. Busch R, Cloutier I, Sékaly R-P, Hammerling GJ: Invariant chain protects class II histocompatibility antigens from binding intact polypeptides in the endoplasmic reticulum. EMBO J 1996;15:418-428.
8. Bakke O, Dobberstein B: MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 1990;63:707-715.
9. 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 the invariant chain. Nature 1990;348: 600-605.
10. Roche PA, Cresswell P: Proteolysis of the MHC class II-associated invariant chain generates a peptide binding site in intracellular HLA-DR molecules. Proc Natl Acad Sci USA 1991;88:3150-3154.
11. Marie MA, Taylor MD, Blum JS: Endosomal aspartic proteinases are required for invariant chain processing. Proc Natl Acad Sci USA 1994;91:2171-2175.
12. Riberdy JM, Newcomb JR, Surman MJ, Barbosa JA, Cresswell P: HLA-DR molecules from an antigen-processing mutant cell line are associated with invariant chain peptides. Nature 1992;360:474-477.
13. Riese RJ, Wolf PR, Brömme 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. Immunity 1996;4:357-366.
14. Avva R, Cresswell P: In vivo and in vitro formation and dissociation of HLA-DR complexes with invariant chain-derived peptides. Immunity 1994;1:763-774.
15. Kropshofer H, Vogt AB, Hämmerling GJ: Structural features of invariant chain CLIP region controlling rapid release from HLA-DR molecules and inhibition of peptide binding. Proc Natl Acad Sci USA 1995;92:8313-8317.
16. Ghosh P, Amaya M, Mellins E, Wiley DC: The structure of HLA-DR3 complexed with CLIP, an intermediate in peptide loading. Nature 1995;387:457-462.
17. Chicz RM, Urban RG, Lane WS, Gorga JC, Stern LJ, Vignali DAA, Strominger JL: Predominant naturally processed peptides bound to HLA-DR1 are derived from MHC-related molecules and are heterogeneous in size. Nature 1992;358:764-768.
18. Chicz, RM, Urban RG, Gorga JC, Vignali DAA, Lane WS, Strominger JL: Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles. J Exp Med 1993;178:27-47.
19. Sanderson F, Kleijmeer M, Kelly A, Verwoerd D, Tulp A, Neefjes J, Geuze HJ, Trowsdale J: Accumulation of HLA-DM, a regulator of antigen presentation, in MHC class II compartments. Science 1994;266: 1566-1569.
20. Karlsson L, Peleraux A, Lindstedt R, Liljedahl M, Peterson PA: Reconstitution of an operational MHC class II compartment in nonantigen-presenting cells. Science 1994;266:1569-1572.
21. Babbit BP, Allen P, Matsueda G, Haber G, Unanue ER: Binding of immunogenic peptides to Ia histocompatibility moleucles. Nature 1985;317:359-360.
22. Buus S, Sette A, Colon SM, Jenis DM, Grey HM: Isolation and characterization of antigen-Ia complexes involved in T cell recognition. Cell 1986;47:1071-1077.
23. Rammensee H-G, Friede T, Stefanovic S: MHC ligands and peptide motifs: first listing. Immunogenetics 1995;41:178-228.
24. Hammer J, Takacs B, Sinigaglia F: Identification of a motif for HLA-DR1 binding peptides using M13 display libraries. J Exp Med 1992;176:1007-1013.
25. Vogt AB, Kropshofer H, Kalbacher H, Kalbus M, Rammensee H-G, Coligan JE, Martin R: Ligand motifs of HLA-DRB5*0101 and DRB1*1501 molecules delineated from self-peptides. J Immunol 1994;153:1665-1673.
26. Hammer J, Valsasnini P, Tolba K, Bolin D, Higelin J, Takacs A, Sinigaglia F: Promiscuous and allele-specific anchors in HLA-DR binding peptides. Cell 1993;74:197-203.
27. Hammer J, Belunis C, Bolin D, Papadopoulos J, Walsky R, Higelin J, Danho W, Sinigaglia F, Nagy Z: High-affinity binding of short peptides to major histocompatibility complex class II molecules by anchor combinations. Proc Natl Acad Sci USA 1994;91:4456-4460.
28. Neefjes JJ, Ploegh HL: Intracellular transport of MHC class II molecules. Immunol Today 1992; 13:179-184
29. 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 1990;343:71-74.
30. Mellins E, Kempin S, Smith L, Monji T, Pious D: A gene required for class II-restricted antigen presentation maps to the major histocompatibility complex. J Exp Med 1991;174:1607-1615.
31. Riberdy JM, Cresswell P: The antigen processing mutant T2 suggests a role for MHC-linked genes in class II antigen presentation. J Immunol 1992;148:2586-2590.
32. Sette A, Ceman S, Kubo RT, Sakaguchi K, Appella E, Hunt DF, Davis TA, Michel H, Shabanowitz J, Rudersdorf R, Grey HM, DeMars R: Invariant chain peptides in most HLA-DR molecules of an antigen processing mutant. Science 1992; 258:1801-1804.
33. Morris P, Shaman J, Attaya M, Amaya M, Goodman S, Bergman C, Monaco JJ, Mellins E;. An essential role for HLA-DM in antigen presentation by class II major histocompatibility molecules. Nature 1994; 368:551-554.
34. Fling SP, Arp B, Pious D: The HLA-DMA gene is required for the formation of stable class II/peptide complexes. Nature 1994;368:554-558.
35. Denzin LK, Robbins NF, Carboy-Newcomb C, Cresswell P: Assembly and intracellular transport of HLADM and correction of the class II antigen-processing defect in T2 cells. Immunity 1994;1:595-606.
36. DeMars R, Chang CC, Shaw S, Reitnauer PJ, Sondel PM: Homozygous deletions that simultaneously eliminate expression of class I and class II antigens of EBV-transformed B-lymphoblastoid cells: reduced proliferative responses of autologous and allogeneic T cells to mutant cells that have decreased expression of class II antigens. Hum Immunol 1984;11:77-99.
37. Ehrlich H, Lee JS, Petersen JW, Bugawan T, DeMars: Molecular analysis of HLA class I and class II antigen loss mutants reveals a homozygous deletion of the DR, DQ and part of the DP regions: implications for class II gene order. Hum Immunol 1986;16:205-219.
38. Monji T, McCormack AL, Yates III JR, Pious D: Invariant-cognate peptide exchange restores class II dimer stability in HLA-DM- mutants. J Immunol 1994;153: 4468-4477.
39. Vogt AB, Kropshofer H, Moldenhauer G, Hämmerling GJ: Kinetic analysis of peptide loading onto HLA-DR molecules mediated by HLA-DM. Proc Natl Acad Sci USA 1996;93:9724-9729.
40. Kropshofer H, Arndt SO, Moldenhauer G, Hämmerling GJ, Vogt AB: HLA-DM acts as a molecular chaperone and rescues empty HLA-DR molecules at lysosomal pH. Immunity 1997; 6:293-302.
41. Kropshofer H, Vogt AB, Stern LJ, Hämmerling GJ: Self-release of CLIP in peptide loading of HLA- DR molecules. Science 1995; 270:1357-1359.
42. Brooks AG, Campbell PL, Reynolds P, Gautam AM, McCluskey J: Antigen presentation and assembly by mouse I-Ak class II molecules in human APC containing deleted or mutated HLA-DM genes. J Immunol 1994;153:5382-5392.
43. Albert LJ, Ghumman B, Watts TH: Effect of HLA-DM transfection of hen egg lysozyme presentation by T2.Ak cells. J Immunol 1996; 157:2247-2255.
44. Ma C, Blum JS: Receptor-mediated endocytosis of antigens overcomes the requirement for HLA-DM in class II-restricted antigen presentation. J Immunol 1997;158:1-4.
45. Malcharek G, Gnau V, Jung, G, Rammensee H-G, Melms A: Supermotifs enable natural invariant chain-derived peptide to interact with many major histocompatibility complex-class II molecules. J Exp Med 1995;181:527-536.
46. Urban RG, Chicz RM, Strominger JL: Selective release of some invariant chain-derived peptides from HLA-DR1 molecules at endosomal pH. J Exp Med 1994;180:751-755.
47. Sadegh-Nasseri S, Stern LJ, Wiley DC, Germain RN: MHC class II function preserved by low-affinity peptide interactions preceding stable binding. Nature 1994; 370:647-650.
48. Stebbins CS, Loss Jr GE, 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 1995;181:223-234.
49. Sette A, Southwood S, Miller J, Apella 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 1995;181:677-683.
50. Tulp A, Verwoerd D, Dobberstein B, Ploegh HL, Pieters J: Isolation and characterization of the intracellular MHC class II compartment. Nature 1994;369:120-126.
51. West MA, Lucocq JM, Watts C: Antigen processing and class II MHC peptide-loading compartments in human lymphoblastoid cells. Nature 1994;369:147-150.
52. 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 1996;4:229-239.
53. Lindstedt R, Liljedahl M, Péléraux 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 1995;3:561-572.
54. 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 1995;131: 351-369.
55. Schafer PH, Green JM, Malapati S, Gu L, Pierce SK: HLA-DM is present in one-fifth the amount of HLA.DR in the class II peptide loading compartment where it associates with leupeptin-induced peptide (LIP)-HLA-DR complexes. J Immunol 1996;157: 5487-5495.
56. Denzin LK, Cresswell P: HLA- DM induces CLIP dissociation from MHC class II αβ dimers and facilitates peptide loading. Cell 1995;82:155-165.
57. Kelly AP, Monaco JJ, Cho S, Trowsdale J: A new human HLA class II-related locus. Nature 1991;353:571-573.
58. Cho S, Attaya M, Monaco JJ: New class II-like genes in the murine MHC. Nature 1991;353:573-576.
59. 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 1995; 375:802-806.
60. Sherman MA, Weber DA, Jensen P: DM enhances peptide binding to class II MHC by release of invariant chain-derived peptides. Immunity 1995;3:197-205.
61. Ellis RJ, van der Vies SM: Molecular chaperones. Annu Rev Biochem 1991;60:321-347.
62. Mellins E, Cameron P, Amaya M, Goodman S, Pious D, Smith L, Arp B: A mutant human histocompatibility leukocyte antigen DR molecule associated with invariant chain peptides. J Exp Med 1994; 179:541-549.
63. Sanderson F, Thomas C, Neefjes J, Trowsdale J: Association between HLA-DM and HLA-DR in vivo. Immunity 1996;4:87-96.
64. Kropshofer H, Vogt AB, Moldenhauer G, Hammer J, Blum JS, Hämmerling GJ: Editing of the HLA-DR peptide repertoire by HLA-DM. EMBO J 1996;15: 6144-6154.
65. Denzin LK, Hammond C, Cresswell P: HLA-DM interactions with intermediates in HLA-DR maturation and a role for HLA-DM in stabilizing empty HLA-DR molecules. J Exp Med 1996;184: 2153-2165.
66. Stern LJ, Wiley DC: The human MHC class II protein HLA-DR1 assembles as empty αβ-heterodimers in the absence of antigenic peptide. Cell 1992;68:465-477.
67. Sadegh-Nasseri S, Germain RN: A role for peptide in determining MHC class II structure. Nature 1991;353:167-170.
68. Devaux B, Wilson KJ, Aguilar B, Jorgensen B, Rothbard JB: Differential stability of HLA-DR alleles independent of endogenous peptides. J Immunol 1995;155:1921-1928.
69. Germain R, Hendrix, LR: MHC class II structure, occupancy and surface expression determined by post-endoplasmic reticulum antigen binding. Nature 1991;353:134-139.
70. Germain R, Rinker Jr. AG: Peptide binding inhibits protein aggregation of invariant-chain free class II dimers and promotes selective cell surface expression of occupied molecules. Nature 1993;363:725-728.
71. Katz JF, Stebbins C, Appella E Sant AJ: Invariant chain and DM edit self-peptide presentation by major histocompatibility complex (MHC) class II molecules. J Exp Med 1996;184:1747-1753.
72. Kropshofer H, Hämmerling GJ, Vogt AB: How HLA-DM edits the MHC class II peptide repertoire: survival of the fittest? Immunol Today 1997;18:77-82.
73. Weber DA, Evavold BD, Jensen PE: Enhanced dissociation of HLA-DR- bound peptides in the presence of HLA- DM. Science 1996;274:618-620.
74. van Ham SM, Grüneberg U, Malcharek G, Broker I, Melms A, Trowsdale J: Human histocompatibility leukocyte antigen (HLA)- DM edits peptides presented by HLA-DR according to their ligand binding motifs. J Exp Med 1996; 184:2019-2024.
75. 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 1994;368:215-221.