Insights into MHC Class I Peptide Loading from the Structure of the Tapasin-ERp57 Thiol Oxidoreductase Heterodimer

Immunity

Volumn 30, Issue 1, 2009, Pages 21-32

  Dong, Gang ^a   Wearsch, Pamela A ^a   Peaper, David R ^a   Cresswell, Peter ^a   Reinisch, Karin M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

MOLIMMUNO

Indexed keywords

HETERODIMER; ISOMERASE; LINK PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; OXIDOREDUCTASE; TAPASIN; THIOL DERIVATIVE; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; COVALENT BOND; HUMAN; HUMAN CELL; MOLECULAR MODEL; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; RNA EDITING;

ANIMALS; CELL LINE; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; PEPTIDES; PROTEIN DISULFIDE REDUCTASE (GLUTATHIONE); PROTEIN DISULFIDE-ISOMERASES; PROTEIN STRUCTURE, QUATERNARY;

EID: 58149215628     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2008.10.018     Document Type: Article

References (55)

1. Bangia N., Lehner P.J., Hughes E.A., Surman M., and Cresswell P. The N-terminal region of tapasin is required to stabilize the MHC class I loading complex. Eur. J. Immunol. 29 (1999) 1858-1870
2. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
3. Busch R., Rinderknecht C.H., Roh S., Lee A.W., Harding J.J., Burster T., Hornell T.M., and Mellins E.D. Achieving stability through editing and chaperoning: Regulation of MHC class II peptide binding and expression. Immunol. Rev. 207 (2005) 242-260
4. Carreno B.M., Solheim J.C., Harris M., Stroynowski I., Connolly J.M., and Hansen T.H. TAP associates with a unique class I conformation, whereas calnexin associates with multiple class I forms in mouse and man. J. Immunol. 155 (1995) 4726-4733
5. Carson M. Ribbons. Methods Enzymol. 277 (1997) 493-505
6. Chen M., and Bouvier M. Analysis of interactions in a tapasin/class I complex provides a mechanism for peptide selection. EMBO J. 26 (2007) 1681-1690
7. Cresswell P., Ackerman A.L., Giodini A., Peaper D.R., and Wearsch P.A. Mechanisms of MHC class I-restricted antigen processing and cross-presentation. Immunol. Rev. 207 (2005) 145-157
8. de La Fortelle E., and Bricogne G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276 (1997) 472-494
9. DeLano W.L. The PyMOL Molecular Graphics System (computer program) (2002), DeLano Scientific, San Carlos, CA, USA.
10. Dick T.P., Bangia N., Peaper D.R., and Cresswell P. Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity 16 (2002) 87-98
11. Ellgaard L., and Ruddock L.W. The human protein disulphide isomerase family: Substrate interactions and functional properties. EMBO Rep. 6 (2005) 28-32
12. Ellgaard L., Bettendorff P., Braun D., Herrmann T., Fiorito F., Jelesarov I., Güntert P., Helenius A., and Wüthrich K. NMR structures of 36 and 73-residue fragments of the calreticulin P-domain. J. Mol. Biol. 322 (2002) 773-784
13. Elliott T. How does TAP associate with MHC class I molecules?. Immunol. Today 18 (1997) 375-379
14. Elliott T., and Williams A. The optimization of peptide cargo bound to MHC class I molecules by the peptide-loading complex. Immunol. Rev. 207 (2005) 89-99
15. Emsley P., and Cowtan K. Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
16. Fremont D.H., Crawford F., Marrack P., Hendrickson W.A., and Kappler J. Crystal Structure of mouse H2-M. Immunity 9 (1998) 385-393
17. Garbi N., Tiwari N., Momburg F., and Hammerling G.J. A major role for tapasin as a stabilizer of the TAP peptide transporter and consequences for MHC class I expression. Eur. J. Immunol. 33 (2003) 264-273
18. Garbi N., Tanaka S., Momburg F., and Hammerling G.J. Impaired assembly of the Major Histocompatibility Complex class I peptide-loading complex in mice deficient in the oxidoreductase ERp57. Nat. Immunol. 7 (2006) 93-102
19. Hansen T.H., Lybarger L., Yu L., Mitaksov V., and Fremont D.H. Recognition of open conformers of classical MHC by chaperones and monoclonal antibodies. Immunol. Rev. 207 (2005) 100-111
20. Harris M.R., Yu Y.Y., Kindle C.S., Hansen T.H., and 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
21. Helenius A., and Aebi M. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73 (2004) 1019-1049
22. Holm L., and Sander C. Mapping the protein universe. Science 273 (1996) 595-603
23. Kanaseki T., Blanchard N., Hammer G.E., Gonzalez F., and Shastri N. ERAAP synergizes with MHC class I molecules to make the final cut in the antigenic peptide precursors in the endoplasmic reticulum. Immunity 25 (2006) 795-806
24. *201/octameric tax peptide complex with an empty conserved peptide-N-terminal binding site. J. Immunol. 164 (2000) 6398-6405
25. Kienast A., Preuss M., Winkler M., and Dick T.P. Redox regulation of peptide receptivity of Major Histocompatibility Complex class I molecules by ERp57 and tapasin. Nat. Immunol. 8 (2007) 864-872
26. Kozlov G., Maattanen P., Schrag J.D., Pollock S., Cygler M., Nagar B., Thomas D.Y., and Gehring K. Crystal structure of the bb' domains of the protein disulfide isomerase ERp57. Structure 14 (2006) 1331-1339
27. Lewis J.W., and Elliott T. Evidence for successive peptide binding and quality control stages during MHC class I assembly. Curr. Biol. 8 (1998) 717-720
28. Lindquist J.A., Hammerling G.J., and Trowsdale J. ER60/ERp57 forms disulfide-bonded intermediates with MHC class I heavy chain. FASEB J. 15 (2001) 1448-1450
29. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., and Read R.J. Phaser crystallographic software. Journal of Applied Crystallography 40 (2007) 658-674
30. Mosyak L., Zaller D.M., and Wiley D.C. The structure of HLA-DM, the peptide exchange catalyst that loads antigen onto class II MHC molecules during antigen presentation. Immunity 9 (1998) 377-383
31. Nicholls A., Sharp K.A., and Honig B. Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11 (1991) 281-296
32. Olson R., Huey-Tubman K.E., Dulac C., and Bjorkman P.J. Structure of a pheromone receptor-associated MHC molecule with an open and empty groove. PLoS Biol. 3 (2005) 257
33. Ortmann B., Copeman J., Lehner P.J., Sadasivan B., Herberg J.A., Grandea A.G., Riddell S.R., Tampe R., Spies T., Trowsdale J., and Cresswell P. A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. Science 277 (1997) 1306-1309
34. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
35. *201 results in failure to bind the TAP complex and to present virus-derived peptides to CTL. Immunity 4 (1996) 505-514
36. Peaper D.R., and Cresswell P. The redox activity of ERp57 is not essential for its functions in MHC class I peptide loading. Proc. Natl. Acad. Sci. USA 105 (2008) 10477-10482
37. Peaper D.R., Wearsch P.A., and Cresswell P. Tapasin and ERp57 form a stable disulfide-linked dimer within the MHC class I peptide-loading complex. EMBO J. 24 (2005) 3613-3623
38. Peh C.A., Burrows S.R., Barnden M., Khanna R., Cresswell P., Moss D.J., and McCluskey J. HLA-B27-restricted antigen presentation in the absence of tapasin reveals polymorphism in mechanisms of HLA class I peptide loading. Immunity 8 (1998) 531-542
39. Reichmann D., Rahat O., Cohen M., Neuvirth H., and Schreiber G. The molecular architecture of protein-protein binding sites. Curr. Opin. Struct. Biol. 17 (2007) 67-76
40. Russell S.J., Ruddock L.W., Salo K.E., Oliver J.D., Roebuck Q.P., Llewellyn D.H., Roderick H.L., Koivunen P., Myllyharju J., and High S. The primary substrate binding site in the b' domain of ERp57 is adapted for endoplasmic reticulum lectin association. J. Biol. Chem. 279 (2004) 18861-18869
41. Sadegh-Nasseri S., Chen M., Narayan K., and Bouvier M. The convergent roles of tapasin and HLA-DM in antigen presentation. Trends Immunol. 29 (2008) 141-147
42. Santos S.G., Campbell E.C., Lynch S., Wong V., Antoniou A.N., and Powis S.J. Major Histocompatibility Complex class I-ERp57-tapasin interactions within the peptide-loading complex. J. Biol. Chem. 282 (2007) 17587-17593
43. Schneider T.R., and Sheldrick G.M. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58 (2002) 1772-1779
44. Schrag J.D., Bergeron J.J., Li Y., Borisova S., Hahn M., Thomas D.Y., and Cygler M. The structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol. Cell 8 (2001) 633-644
45. Sharff A.J., Koronakis E., Luisi B., and Koronakis V. Oxidation of selenomethionine: Some MADness in the method!. Acta Crystallogr. D Biol. Crystallogr. 56 (2000) 785-788
46. Tian G., Xiang S., Noiva R., Lennarz W.J., and Schindelin H. The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites. Cell 124 (2006) 61-73
47. Thomson S.P., and Williams D.B. Delineation of the lectin site of the molecular chaperone calreticulin. Cell Stress Chaperones 10 (2005) 242-251
48. Turnquist H.R., Petersen J.L., Vargas S.E., McIlhaney M.M., Bedows E., Mayer W.E., Grandea III A.G., Van Kaer L., and Solheim J.C. The Ig-like domain of tapasin influences intermolecular interactions. J. Immunol. 172 (2004) 2976-2984
49. Walker K.W., and Gilbert H.F. Scanning and escape during protein-disulfide iosmerase-assisted folding. J. Biol. Chem. 272 (1997) 8845-8848
50. Wearsch P.A., and Cresswell P. Selective loading of high-affinity peptides onto major histocompatibility complex class I molecules by the tapasin-ERp57 heterodimer. Nat. Immunol. 8 (2007) 873-881
51. Wearsch P.A., Jakob C.A., Vallin A., Dwek R.A., Rudd P.M., and Cresswell P. Major histocompatibility complex class I molecules expressed with monoglucosylated N-linked glycans bind calreticulin independently of assembly status. J. Biol. Chem. 279 (2004) 25112-25121
52. Wright C.A., Kozik P., Zacharias M., and Springer S. Tapasin and other chaperones: Models of the MHC class I loading complex. Biol. Chem. 385 (2004) 763-768
53. Zacharias M., and Springer S. Conformational flexibility of the MHC class I α1-α2 domain in peptide bound and free states: A molecular dynamics simulation study. Biophys. J. 87 (2004) 2203-2214
54. Yu Y.Y., Turnquist H.R., Myers N.B., Balendiran G.K., Hansen T.H., and Solhein J.C. An extensive region of an MHC class I a2 domain loop influences interaction with the assembly complex. J. Immunol. 163 (1999) 4427-4433
55. Zhang Y., Baig E., and Williams D.B. Functions of ERp57 in the folding and assembly of Major Histocompatibility Complex class I molecules. J. Biol. Chem. 281 (2006) 14622-14631