Accessory molecules in the assembly of major histocompatibility complex class I/peptide complexes: How essential are they for CD8+ T-cell immune responses?

Immunological Reviews

Volumn 207, Issue , 2005, Pages 77-88

  Garbi, Natalio ^a   Tanaka, Satoshi ^b   Van Den Broek, Maries ^c   Momburg, Frank ^a   Hämmerling, Günter J ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b SAPPORO CITY GENERAL HOSPITAL   (Japan)

^c INSTITUTE OF EXPERIMENTAL IMMUNOLOGY   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CALRETICULIN; CD8 ANTIGEN; IOXAGLIC ACID; TAPASIN;

ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; HUMAN; IMMUNITY; IN VITRO STUDY; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; REVIEW; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; ANTIPORTERS; ATP-BINDING CASSETTE TRANSPORTERS; CALRETICULIN; CD8-POSITIVE T-LYMPHOCYTES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOGLOBULINS; MEMBRANE TRANSPORT PROTEINS; MICE; MOLECULAR CHAPERONES; PEPTIDES;

EID: 26244443657     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0105-2896.2005.00303.x     Document Type: Review

References (89)

1. Williams DB, Barber BH, Flavell RA, Allen H. Role of beta 2-microglobulin in the intracellular transport and surface expression of murine class I histocompatibility molecules. J Immunol 1989;142:2796-2806.
2. + cytolytic T cells. Nature 1990;344:742-746.
3. + T cells. Cell 1992;71:1205-1214.
4. Pamer E, Cresswell P. Mechanisms of MHC class I-restricted antigen processing. Annu Rev Immunol 1998;16:323-358.
5. Norbury CC, Chambers BJ, Prescott AR, Ljunggren HG, Watts C. Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur J Immunol 1997;27:280-288.
6. Ruedl C, Storn T, Lechner F, Bachi T, Bachmann MF. Cross-presentation of virus-like particles by skin-derived CD8(-) dendritic cells: a dispensable role for TAP. Eur J Immunol 2002;32:818-825.
7. Shen L, Sigal LJ, Boes M, Rock KL. Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo. Immunity 2004;21:155-165.
8. Williams A, Peh CA, Elliott T. The cell biology of MHC class I antigen presentation. Tissue Antigens 2002;59:3-17.
9. Antoniou AN, Powis SJ, Elliott T. Assembly and export of MHC class I peptide ligands. Curr Opin Immunol 2003;15:75-81.
10. Paulsson K, Wang P. Chaperones and folding of MHC class I molecules in the endoplasmic reticulum. Biochim Biophys Acta 2003;1641:1-12.
11. Wright AC, Kozik P, Zacharias M, Springer S. Tapasin and other chaperones: models of the MHC class I loading complex. Biol Chem 2004;385:763-778.
12. Dick TP. Assembly of MHC class I peptide complexes from the perspective of disulfide bond formation. Cell Mol Life Sci 2004;61:547-556.
13. David V, Hochstenbach F, Rajagopalan S, Brenner M. Interaction with newly synthesized and retained proteins in the endoplasmic reticulum suggests a chaperone function for human integral membrane protein IP90 (calnexin). J Biol Chem 1993;268:9585-9592.
14. Degen E, Cohen-Doyle MF, Williams DB. Efficient dissociation of the p88 chaperone from major histocompatibility complex class I molecules requires both b2-microglobulin and peptide. J Exp Med 1994;175:1653-1661.
15. 2- microglobulin complexes associate with TAP transporters before peptide binding. Nature 1994;368:864-867.
16. Nossner E, Parham P. Species-specific differences in chaperone interaction of human and mouse histocompatibility complex class I molecules. J Exp Med 1995;181:327-337.
17. Lindquist JA, Jensen ON, Mann M, Hämmerling GJ. ER-60, a chaperone with thiol-dependent reductase activity involved in MHC class I assembly. EMBO J 1998;17:2186-2195.
18. Morrice NA, Powis SJ. A role for the thiol-dependent reductase ERp57 in the assembly of MHC class I molecules. Curr Biol 1998;8:713-716.
19. Lindquist JA, Hammerling GJ, Trowsdale J. ER60/ERp57 forms disulfide-bonded intermediates with MHC class I heavy chain. FASEB J 2001;15:1448-1450.
20. Scott JE, Dawson JR. MHC class I expression and transport in a calnexin-deficient cell line. J Immunol 1995;155:143-148.
21. Prasad SA, Yewdell JW, Porgador A, Sadasivan B, Cresswell P, Bennink JR. Calnexin expression does not enhance the generation of MHC class I-peptide complexes. Eur J Immunol 1998;28:907-913.
22. Molinari M, et al. Contrasting functions calreticulin calnexin glycoprotein folding ER quality control. Mol Cell 2004;13:125-135.
23. Farmery MR, Allen S, Allen AJ, Bulleid NJ. The role of ERp57 in disulfide bond formation during the assembly of major histocompatibility complex class I in a synchronized semipermeabilized cell translation system. J Biol Chem 2000;275:14933-14938.
24. Neefjes J, Hämmerling GJ, Momburg F. Folding and assembly of major histocompatibility complex class I heterodimers in the endoplasmic reticulum of intact cells precedes the binding of peptide. J Exp Med 1993;178:1971-1980.
25. Tector M, Zhang Q, Salter RD. Beta 2-microglobulin and calnexin can independently promote folding and disulfide bond formation in class I histocompatibility proteins. Mol Immunol 1997;34:401-408.
26. Smith JD, Solheim JC, Carreno BM, Hansen TH. Characterization of class I MHC folding intermediates and their disparate interactions with peptide and beta 2-microglobulin. Mol Immunol 1995;32:531-540.
27. Pedersen LO, et al. Efficient assembly of recombinant major histocompatibility complex class I molecules with preformed disulfide bonds. Eur J Immunol 2001;31:2986-2996.
28. Wearsch PA, Jakob CA, Vallin A, Dwek RA, Rudd PM, Cresswell P. Major histocompatibility complex class I molecules expressed with monoglucosylated N-linked glycans bind calreticulin independently of their assembly status. J Biol Chem 2004;279:25112-25121.
29. Culina S, Lauvau G, Gubler B, van Endert PM. Calreticulin promotes folding of functional human leukocyte antigen class I molecules in vitro. J Biol Chem 2004;279:54210-54215.
30. Suh WK, Cohen-Doyle MF, Fruh K, Wang K, Peterson PA, Williams DB. Interaction of MHC class I molecules with the transporter associated with antigen processing. Science 1994;264:1322-1326.
31. Li S, Paulsson KM, Sjogren H-O, Wang P. Peptide-bound major histocompatibility complex class I molecules associate with tapasin before dissociation from transporter associated with antigen processing. J Biol Chem 1999;274:8649-8654.
32. Androlewicz MJ, Anderson KS, Cresswell P. Evidence that transporters associated with antigen processing translocate a major histocompatibility complex class I-binding peptide into the endoplasmic reticulum in an ATP-dependent manner. Proc Natl Acad Sci USA 1993;90:9130-9134.
33. Neefjes JJ, Momburg F, Hämmerling GJ. Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter. Science 1993;261:769-771.
34. Sadasivan B, Lehner PJ, Ortmann B, Spies T, Cresswell P. Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity 1996;5:103-114.
35. Hughes EA, Cresswell P. The thiol oxidoreductase ERp57 is a component of the MHC dass I peptide-loading complex. Curr Biol 1998;8:709-712.
36. Bangia N, Cresswell P. Stoichiometric tapasin interactions in the catalysis of major histocompatibility complex class I molecule assembly. Immunology 2005;114:346-353.
37. Ortmann B, et al. A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. Science 1997;277:1306-1309.
38. Dick TP, Bangia N, Peaper DR, Cresswell P. Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity 2002;16:87-98.
39. Lewis JW, Elliott T. Evidence for successive peptide binding and quality control stages during MHC class I assembly. Curr Biol 1998;8:717-720.
40. Tan P, Kropshofer H, Mandelboim O, Bulbuc N, Hämmerling GJ, Momburg F. Recruitment of MHC class I molecules by tapasin into the transporter associated with antigen processing-associated complex is essential for optimal peptide loading. J Immunol 2002;168:1950-1960.
41. Momburg F, Tan P. Tapasin - the keystone of the loading complex optimizing peptide binding by MHC class I molecules in the endoplasmic reticulum. Mol Immunol 2002;39:217-233.
42. Grandea AG III, Van Kaer L. Tapasin: an ER chaperone that controls MHC class I assembly with peptide. Trends Immunol 2001;22:194-199.
43. Brocke P, Garbi N, Momburg F, Hämmerling GJ. HLA-DM, HLA-DO and tapasin: functional similarities and differences. Curr Opin Immunol 2002;14:22-29.
44. Garbi N, et al. Impaired immune responses and altered peptide repertoire in tapasin-deficient mice. Nat Immunol 2000;1:234-238.
45. Grandea AG III, et al. Impaired assembly yet normal trafficking of MHC class I molecules in tapasin mutant mice. Immunity 2000;13:213-222.
46. Greenwood R, Shimizu Y, Sekhon GS, DeMars R. Novel allele-specific, post-translational reduction in HLA class I surface expression in a mutant human B cell line. J Immunol 1994;153:5525-5536.
47. Barnden MJ, Purcell AW, Gorman JJ, McCluskey J. Tapasin-mediated retention and optimization of peptide ligands during the assembly of class I molecules. J Immunol 2000;165:322-330.
48. Purcell AW, et al. Quantitative and qualitative influences of tapasin on the class I peptide repertoire. J Immunol 2001;166:1016-1027.
49. Williams AP, Peh CA, Purcell AW, McCluskey J, Elliott T. Optimization of the MHC class I peptide cargo is dependent on tapasin. Immunity 2002;16:509-520.
50. Peh CA, et al. HLA-B27-restricted antigen presentation in the absence of tapasin reveals polymorphism in mechanisms of HLA class I peptide loading. Immunity 1998;8:531-542.
51. Park B, Lee S, Kim E, Ahn K. A single polymorphic residue within the peptide-binding cleft of MHC class I molecules determines spectrum of tapasin dependence. J Immunol 2003;170:961-968.
52. Lehner PJ, Surman MJ, Cresswell P. Soluble tapasin restores MHC class I expression and function in the tapasin-negative cell line. 220. Immunity 1998;8:221-231.
53. Yabe T, et al. A subject with a novel type I bare lymphocyte syndrome has tapasin deficiency due to deletion of 4 exons by Alu-mediated recombination. Blood 2002;100:1496-1498.
54. Garbi N, Tiwari N, Momburg F, Hämmerling GJ. A major role for tapasin as a stabilizer of the TAP peptide transporter and consequences for MHC class I expression. Eur J Immunol 2003;33:264-273.
55. Petersen JL, et al. A charged amino acid residue in the transmembrane/cytoplasmic region of tapasin influences MHC class I assembly and maturation. J Immunol 2005;174:962-969.
56. Gao B, et al. Assembly and antigen-presenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin. Immunity 2002;16:99-109.
57. Diedrich G, Bangia N, Pan M, Cresswell P. A role for calnexin in the assembly of the MHC class I loading complex in the endoplasmic reticulum. J Immunol 2001;166:1703-1709.
58. Bangia N, Lehner PJ, Hughes EA, Surman M, Cresswell P. The N-terminal region of tapasin is required to stabilize the MHC class I loading complex. Eur J Immunol 1999;29:1858-1870.
59. Zarling AL, et al. Tapasin is a facilitator, not an editor of class I MHC peptide binding. J Immunol 2003;171:5287-5295.
60. Howarth M, Williams AP, Tolstrup AB, Elliott T. Tapasin enhances MHC class I peptide presentation according to peptide half-life. Proc Natl Acad Sci USA 2004;101:11737-11742.
61. Frickel EM, Riek R, Jelesarov I, Helenius A, Wuthrich K, Ellgaard L. TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain. Proc Natl Acad Sci USA 2002;99:1954-1959.
62. Turnquist HR, et al. The Ig-like domain of tapasin influences intermolecular interactions. J Immunol 2004;172:2976-2984.
63. Mesaeli N, et al. Calreticulin is essential for heart development. J Cell Biol 1999;1444:857-868.
64. + T cell repertoire that displays both diversity and peptide specificity. Eur J Immunol 1996;26:288-293.
65. + T cells in vivo. J Immunol 2001;166:4355-4362.
66. Sigal LJ, Crotty S, Andino R, Rock KL. Cytotoxic T-cell immunity to virus-infected non-haematopoietic cells requires presentation of exogenous antigen. Nature 1999;398:77-80.
67. Neisig A, Wubbolts R, Zang X, Melief C, Neefjes J. Allele-specific differences in the interaction of MHC class I molecules with transporters associated with antigen processing. J Immunol 1996;156:3196-3206.
68. Turnquist HR, Thomas HJ, Prilliman KR, Lutz CT, Hildebrand WH, Solheim JC. HLA-B polymorphism affects interactions with multiple endoplasmic reticulum proteins. Eur J Immunol 2000;30:3021-3028.
69. Zernich D, et al. Natural HLA class I polymorphism controls the pathway of antigen presentation and susceptibility to viral evasion. J Exp Med 2004;200:13-24.
70. Henderson RA, et al. HLA-A2.1-associated peptides from a mutant cell line: a second pathway of antigen presentation. Science 1992;255:1264-1266.
71. Wei ML, Cresswell P. HLA-A2 molecules in an antigen-processing mutant cell contain signal sequence-derived peptides. Nature 1992;356:443-446.
72. Rock KL. A new foreign policy: MHC class I molecules monitor the outside world. Immunol Today 1996;17:131-137.
73. Jondal M, Schirmbeck R, Reimann J. MHC class I-restricted CTL responses to exogenous antigens. Immunity 1996;5:295-302.
74. Ackerman AL, Cresswell P. Cellular mechanisms governing cross-presentation of exogenous antigens. Nat Immunol 2004;5:678-684.
75. Sijts AJ, Neisig A, Neefjes J, Pamer EG. Two Listeria monocytogenes CTL epitopes are processed from the same antigen with different efficiencies. J Immunol 1996;156:685-692.
76. Villanueva MS, Sijts AJ, Pamer EG. Listeriolysin is processed efficiently into an MHC class I-associated epitope in Listeria monocytogenes-infected cells. J Immunol 1995;155:5227-5233.
77. Villanueva MS, Fischer P, Feen K, Pamer EG. Efficiency of MHC class I antigen processing: a quantitative analysis. Immunity 1994;1:479-489.
78. Princiotta MF, et al. Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 2003;18:343-354.
79. Yewdell JW. Not such a dismal science: the economics of protein synthesis, folding, degradation and antigen processing. Trends Cell Biol 2001;11:294-297.
80. Delamarre L, Pack M, Chang H, Mellman I, Trombetta ES. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 2005;307:1630-1634.
81. Trombetta ES, Mellman I. Cell biology of antigen processing in vitro and in vivo. Annu Rev Immunol 2005;23:975-1028.
82. Sykulev Y, Joo M, Vturina I, Tsomides TJ, Eisen HN. Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity 1996;4:565-571.
83. Christinck ER, Luscher MA, Barber BH, Williams DB. Peptide binding to class I MHC on living cells and quantisation of complexes required for CTL lysis. Nature 1991;352:67-70.
84. + CTL. Mol Immunol 1994;31:1285-1293.
85. Reay PA, Matsui K, Haase KW, Wulfing C, Chien YH, Davis MM. Determination of the relationship between T cell responsiveness and the number of MHC-peptide complexes using specific monoclonal antibodies. J Immunol 2000;164:5626-5634.
86. Purbhoo MA, Irvine DJ, Huppa JB, Davis MM. T cell killing does not require the formation of a stable mature immunological synapse. Nat Immunol 2004;5:524-530.
87. Stoll S, Delon J, Brotz TM, Germain RN. Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science 2002;296:1873-1876.
88. Hugues S, Fetler L, Bonifaz L, Helft J, Amblard F, Amigorena S. Distinct T cell dynamics in lymph nodes during the induction of tolerance and immunity. Nat Immunol 2004;5:1235-1242.
89. Garbi N, Tanaka S, Momburg F, Hämmerling GJ. Severely impaired assembly of the MHC class I peptide loading complex in mice deficient for the oxidoreductase ER p 57. Nat Immunol 2005 (in press).