Assembly and export of MHC class I peptide ligands

Current Opinion in Immunology

Volumn 15, Issue 1, 2003, Pages 75-81

  Antoniou, Antony N ^a   Powis, Simon J ^a   Elliott, Tim ^b  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALNEXIN; CALRETICULIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE; TAPASIN; ANTIPORTER; CARRIER PROTEIN; CHAPERONE; HLA ANTIGEN CLASS 1; IMMUNOGLOBULIN;

CELL MEMBRANE TRANSPORT; MOLECULAR BIOLOGY; PROTEIN PROTEIN INTERACTION; REVIEW; ANIMAL; CHEMISTRY; ENDOPLASMIC RETICULUM; HUMAN; IMMUNOLOGY; MACROMOLECULE; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING; PROTEIN TRANSPORT;

ANIMALS; ANTIPORTERS; ENDOPLASMIC RETICULUM; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOGLOBULINS; MACROMOLECULAR SUBSTANCES; MEMBRANE TRANSPORT PROTEINS; MOLECULAR CHAPERONES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT;

EID: 0037290828     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(02)00010-9     Document Type: Review

References (61)

1. Zhang Q., Tector M., Salter R.D. Calnexin recognizes carbohydrate and protein determinants of class I major histocompatibility complex molecules. J. Biol. Chem. 270:1995;3944-3948.
2. Zhang Q., Salter R.D. Distinct patterns of folding and interactions with calnexin and calreticulin in human class I MHC proteins with altered N-glycosylation. J. Immunol. 160:1998;831-837.
3. Helenius A., Aebi M. Intracellular functions of N-linked glycans. Science. 291:2001;2364-2369.
4. Ellgaard L., Molinari M., Helenius A. Setting the standards: quality control in the secretory pathway. Science. 286:1999;1882-1888.
5. Harris M.R., Yu Y.Y., Kindle C.S., Hansen T.H., Solheim J.C. Calreticulin and calnexin interact with different protein and glycan determinants during the assembly of MHC class I. J. Immunol. 160:1998;5404-5409.
6. Harris M.R., Lybarger L., Yu Y.Y., Myers N.B., Hansen T.H. Association of ERp57 with mouse MHC class I molecules is tapasin dependent and mimics that of calreticulin and not calnexin. J. Immunol. 166:2001;6686-6692.
7. Schrag J.D., Bergeron J.J., Li Y., Borisova S., Hahn M., Thomas D.Y., Cygler M. The structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol. Cell. 8:2001;633-644 The three-dimensional structure of the ER lumenal domain of calnexin reveals the lectin binding site and also the elongated P-domain arm composed of proline-rich motifs, interacting in a head-to-tail orientation.
8. Farmery M.R., Allen S., Allen A.J., Bulleid N.J. 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. 275:2000;14933-14938.
9. 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. 166:2001;1703-1709.
10. Cresswell P., Bangia N., Dick T., Diedrich G. The nature of the MHC class I peptide loading complex. Immunol. Rev. 172:1999;21-28.
11. Solheim J.C., Harris M.R., Kindle C.S., Hansen T.H. Prominence of beta 2-microglobulin, class I heavy chain conformation, and tapasin in the interactions of class I heavy chain with calreticulin and the transporter associated with antigen processing. J. Immunol. 158:1997;2236-2241.
12. Sadasivan B., Lehner P.J., 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. 5:1996;103-114.
13. Scott J.E., Dawson J.R. MHC class I expression and transport in a calnexin-deficient cell line. J. Immunol. 155:1995;143-148.
14. Sadasivan B.K., Cariappa A., Waneck G.L., Cresswell P. Assembly, peptide loading, and transport of MHC class I molecules in a calnexin-negative cell line. Cold Spring Harb. Symp. Quant. Biol. 60:1995;267-275.
15. Stronge V.S., Saito Y., Ihara Y., Williams D.B. Relationship between calnexin and BiP in suppressing aggregation and promoting refolding of protein and glycoprotein substrates. J. Biol. Chem. 276:2001;39779-39787.
16. Paulsson K.M., Wang P., Anderson P.O., Chen S., Pettersson R.F., Li S. Distinct differences in association of MHC class I with endoplasmic reticulum proteins in wild-type, and beta 2-microglobulin- and TAP- deficient cell lines. Int. Immunol. 13:2001;1063-1073.
17. Nossner E., Parham P. Species-specific differences in chaperone interaction of human and mouse major histocompatibility complex class I molecules. J. Exp. Med. 181:1995;327-337.
18. Tector M., Salter R.D. Calnexin influences folding of human class I histocompatibility proteins but not their assembly with beta 2-microglobulin. J. Biol. Chem. 270:1995;19638-19642.
19. Zapun A., Darby N.J., Tessier D.C., Michalak M., Bergeron J.J., Thomas D.Y. Enhanced catalysis of ribonuclease B folding by the interaction of calnexin or calreticulin with ERp57. J. Biol. Chem. 273:1998;6009-6012.
20. Oliver J.D., Roderick H.L., Llewellyn D.H., High S. ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin. Mol. Biol. Cell. 10:1999;2573-2582.
21. Elliott J.G., Oliver J.D., High S. The thiol-dependent reductase ERp57 interacts specifically with N-glycosylated integral membrane proteins. J. Biol. Chem. 272:1997;13849-13855.
22. Frickel E.M., 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. U.S.A. 99:2002;1954-1959 The use of a chemical crosslinker together with NMR indicates the interaction between the tip of recombinant calreticulin P-domain and recombinant ERp57 protein disulfide isomerase (PDI) appears not to form a similar interaction in this system.
23. Brocke P., Garbi N., Momburg F., Hammerling G.J. HLA-DM, HLA-DO and tapasin: functional similarities and differences. Curr. Opin. Immunol. 14:2002;22-29.
24. Lehner P.J., Surman M.J., Cresswell P. Soluble tapasin restores MHC class I expression and function in the tapasin-negative cell line .220. Immunity. 8:1998;221-231.
25. Dick T.P., Bangia N., Peaper D.R., Cresswell P. Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity. 16:2002;87-98 ERp57 is shown to be disulfide bonded to tapasin, a result that significantly alters our view of the PLC. The disulfide association occurs between the TR1 motif of ERp57 and the unpaired Cys95 of tapasin. Mutation of an internal tapasin disulfide pairing between Cys7 and Cys71 results in incomplete disulfide bonding of MHC class I molecules in the PLC.
26. Lindquist J.A., Hammerling G.J., Trowsdale J. ER60/ERp57 forms disulfide-bonded intermediates with MHC class I heavy chain. FASEB J. 15:2001;1448-1450.
27. Antoniou A.N., Ford S., Alphey M., Osborne A., Elliott T., Powis S.J. The oxidoreductase ERp57 efficiently reduces partially folded in preference to fully folded MHC class I molecules. EMBO J. 21:2002;2655-2663 Recombinant ERp57, when added to radiolabelled immunoprecipitates of MHC class I molecules, is able to act as a reductase only on partially folded or unfolded heavy chains, and not on folded MHC class I molecules.
28. Gao B., Adhikari R., Howarth M., Nakamura K., Gold M.C., Hill A.B., Knee R., Michalak M., Elliott T. Assembly and antigen-presenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin. Immunity. 16:2002;99-109 Calreticulin-deficient cells assemble MHC class I molecules with inefficient peptide optimisation. The presence of tapasin permits MHC association with TAP, but cannot compensate fully for the lack of calreticulin.
29. Lewis J.W., Elliott T. Evidence for successive peptide binding and quality control stages during MHC class I assembly. Curr. Biol. 8:1998;717-720.
30. Williams A.P., Peh C.A., Purcell A.W., McCluskey J., Elliott T. Optimization of the MHC class I peptide cargo is dependent on tapasin. Immunity. 16:2002;509-520 Immunoprecipitation of folded MHC class I molecules from heat-treated lysates of tapasin-deficient and tapasin-expressing cell lines indicates a time-dependent acquisition of a stable MHC class I phenotype (equating to the presence of high affinity peptides) in the presence of tapasin.
31. Purcell A.W., Gorman J.J., Garcia-Peydro M., Paradela A., Burrows S.R., Talbo G.H., Laham N., Peh C.A., Reynolds E.C., Lopez De Castro J.A.et al. Quantitative and qualitative influences of tapasin on the class I peptide repertoire. J. Immunol. 166:2001;1016-1027.
32. Lybarger L., Yu Y.Y., Chun T., Wang C.R., Grandea A.G. III, Van Kaer L., Hansen T.H. Tapasin enhances peptide-induced expression of H2-M3 molecules, but is not required for the retention of open conformers. J. Immunol. 167:2001;2097-2105.
33. Chun T., Grandea A.G. III, Lybarger L., Forman J., Van Kaer L., Wang C.R. Functional roles of TAP and tapasin in the assembly of M3-N-formylated peptide complexes. J. Immunol. 167:2001;1507-1514.
34. 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. 156:1996;3196-3206.
35. Yu Y.Y., Turnquist H.R., Myers N.B., Balendiran G.K., Hansen T.H., Solheim J.C. An extensive region of an MHC class I alpha 2 domain loop influences interaction with the assembly complex. J. Immunol. 163:1999;4427-4433.
36. Suh W.K., Derby M.A., Cohen-Doyle M.F., Schoenhals G.J., Fruh K., Berzofsky J.A., Williams D.B. Interaction of murine MHC class I molecules with tapasin and TAP enhances peptide loading and involves the heavy chain alpha3 domain. J. Immunol. 162:1999;1530-1540.
37. Turnquist H.R., Vargas S.E., Reber A.J., McIlhaney M.M., Li S., Wang P., Sanderson S.D., Gubler B., van Endert P., Solheim J.C. A region of tapasin that affects L(d) binding and assembly. J. Immunol. 167:2001;4443-4449.
38. Paquet M.E., Williams D.B. Mutant MHC class I molecules define interactions between components of the peptide-loading complex. Int. Immunol. 14:2002;347-358.
39. Solheim J.C. Class I MHC molecules: assembly and antigen presentation. Immunol. Rev. 172:1999;11-19.
40. Tortorella D., Gewurz B.E., Furman M.H., Schust D.J., Ploegh H.L. Viral subversion of the immune system. Annu. Rev. Immunol. 8:2000;861-926.
41. Tortorella D, Story CM, Huppa JB, Wiertz EJ, Jones TR, Bacik I, Bennink JR, Yewdell JW, Ploegh HL: Dislocation of type I membrane proteins from the ER to the cytosol is sensitive to changes in redox potential. J Cell Biol 1998, 142:365-376. [Published erratum appears in J Cell Biol 1999, 145:642].
42. Wilson C.M., Farmery M.R., Bulleid N.J. Pivotal role of calnexin and mannose trimming in regulating the endoplasmic reticulum-associated degradation of major histocompatibility complex class I heavy chain. J. Biol. Chem. 275:2000;21224-21232.
43. Fiebiger E., Story C., Ploegh H.L., Tortorella D. Visualization of the ER-to-cytosol dislocation reaction of a type I membrane protein. EMBO J. 21:2002;1041-1053.
44. -/- cells, unassembled MHC class I heavy chains fail to accumulate at ER exit sites. After ATP depletion, segregation occurs into a calnexin- and COPII-containing compartment, which may be a distinct site of quality control and/or degradation.
45. Kamhi-Nesher S., Shenkman M., Tolchinsky S., Fromm S.V., Ehrlich R., Lederkremer G.Z. A novel quality control compartment derived from the endoplasmic reticulum. Mol. Biol. Cell. 12:2001;1711-1723.
46. Locher K.P., Lee A.T., Rees D.C. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science. 296:2002;1091-1098.
47. Velarde G., Ford R.C., Rosenberg M.F., Powis S.J. Three-dimensional structure of transporter associated with antigen processing (TAP) obtained by single particle image analysis. J. Biol. Chem. 276:2001;46054-46063.
48. Knittler M.R., Alberts P., Deverson E.V., Howard J.C. Nucleotide binding by TAP mediates association with peptide and release of assembled MHC class I molecules. Curr. Biol. 9:1999;999-1008.
49. Alberts P., Daumke O., Deverson E.V., Howard J.C., Knittler M.R. Distinct functional properties of the TAP subunits coordinate the nucleotide-dependent transport cycle. Curr. Biol. 11:2001;242-251.
50. Rosenberg M.F., Velarde G., Ford R.C., Martin C., Berridge G., Kerr I.D., Callaghan R., Schmidlin A., Wooding C., Linton K.J.et al. Repacking of the transmembrane domains of P-glycoprotein during the transport ATPase cycle. EMBO J. 20:2001;5615-5625.
51. Lacaille V.G., Androlewicz M.J. Herpes simplex virus inhibitor ICP47 destabilizes the transporter associated with antigen processing (TAP) heterodimer. J. Biol. Chem. 273:1998;17386-17390.
52. Hewitt E.W., Gupta S.S., Lehner P.J. The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J. 20:2001;387-396.
53. Antoniou A.N., Ford S., Pilley E.S., Blake N., Powis S.J. Interactions formed by individually expressed TAP1 and TAP2 polypeptide subunits. Immunology. 106:2002;182-189.
54. Li S., Paulsson K.M., Chen S., Sjogren H.O., Wang P. Tapasin is required for efficient peptide binding to transporter associated with antigen processing. J. Biol. Chem. 275:2000;1581-1586.
55. Gaudet R., Wiley D.C. Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing. EMBO J. 20:2001;4964-4972.
56. Gruhler A., Fruh K. Control of MHC class I traffic from the endoplasmic reticulum by cellular chaperones and viral anti-chaperones. Traffic. 1:2000;306-311.
57. Spiliotis E.T., Manley H., Osorio M., Zuniga M.C., Edidin M. Selective export of MHC class I molecules from the ER after their dissociation from TAP. Immunity. 13:2000;841-851.
58. Pentcheva T., Spiliotis E.T., Edidin M. Cutting edge: tapasin is retained in the endoplasmic reticulum by dynamic clustering and exclusion from endoplasmic reticulum exit sites. J. Immunol. 168:2002;1538-1541.
59. Pentcheva T., Edidin M. Clustering of peptide-loaded MHC class I molecules for endoplasmic reticulum export imaged by fluorescence resonance energy transfer. J. Immunol. 166:2001;6625-6632.
60. Adachi T., Schamel W.W., Kim K.M., Watanabe T., Becker B., Nielsen P.J., Reth M. The specificity of association of the IgD molecule with the accessory proteins BAP31/BAP29 lies in the IgD transmembrane sequence. EMBO J. 15:1996;1534-1541.
61. Lewis J.W., Neisig A., Neefjes J., Elliott T. Point mutations in the alpha 2 domain of HLA-A2.1 define a functionally relevant interaction with TAP. Curr. Biol. 6:1996;873-883.