HLA-B44 polymorphisms at position 116 of the heavy chain influence TAP complex binding via an effect on peptide occupancy

Journal of Immunology

Volumn 177, Issue 5, 2006, Pages 3150-3161

  Thammavongsa, Vilasack ^a   Raghuraman, Gayatri ^a   Filzen, Tracy M ^a   Collins, Kathleen L ^a   Raghavan, Malini ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; HLA B ANTIGEN; HLA B44 ANTIGEN; PEPTIDE; PROTEIN TAP; TAPASIN; UNCLASSIFIED DRUG;

ALLOTYPE; ANIMAL CELL; ARTICLE; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; DISSOCIATION; ENDOPLASMIC RETICULUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; THERMOSTABILITY;

EID: 33747766822     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.5.3150     Document Type: Article

References (48)

1. Ortmann, B., J. Copeman, P. J. Lehner, B. Sadasivan, J. A. Herberg, A. G. Grandea, S. R. Riddell, R. Tampe, T. Spies, J. Trowsdale, and P. Cresswell. 1997. A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. Science 277: 1306-1309.
2. Cresswell, P., N. Bangia, T. Dick, and G. Diedrich. 1999. The nature of the MHC class I peptide loading complex. Immunol. Rev. 172: 21-28.
3. Lehner, P. J., M. J. Surman, and P. Cresswell. 1998. Soluble tapasin restores MHC class I expression and function in the tapasin-negative cell line. 220. Immunity 8: 221-231.
4. Garbi, N., N. Tiwari, F. Momburg, and G. J. Hammerling. 2003. A major role for tapasin as a stabilizer of the TAP peptide transporter and consequences for MHC class I expression. Eur. J. Immunol. 33: 264-273.
5. Schoenhals, G. J., R. M. Krishna, A. G. Grandea, III, T. Spies, P. A. Peterson, Y. Yang, and K. Fruh. 1999. Retention of empty MHC class I molecules by tapasin is essential to reconstitute antigen presentation in invertebrate cells. EMBO J. 18: 743-753.
6. Grandea, A. G., III, T. N. Golovina, S. E. Hamilton, V. Sriram, T. Spies, R. R. Brutkiewicz, J. T. Harty, L. C. Eisenlohr, and L. Van Kaer. 2000. Impaired assembly yet normal trafficking of MHC class I molecules in Tapasin mutant mice. Immunity 13: 213-222.
7. Williams, A. P., C. A. Peh, A. W. Purcell, J. McCluskey, and T. Elliott. 2002. Optimization of the MHC class I peptide cargo is dependent on tapasin. Immunity 16: 509-520.
8. Zarling, A. L., C. J. Luckey, J. A. Marto, F. M. White, C. J. Brame, A. M. Evans, P. J. Lehner, P. Cresswell, J. Shabanowitz, D. F. Hunt, and V. H. Engelhard. 2003. Tapasin is a facilitator, not an editor, of class I MHC peptide binding. J. Immunol. 171: 5287-5295.
9. Chun, T., A. G. Grandea, III, L. Lybarger, J. Forman, L. Van Kaer, and C. R. Wang. 2001. Functional roles of TAP and tapasin in the assembly of M3-N-formylated peptide complexes. J. Immunol. 167: 1507-1514.
10. Lybarger, L., Y. Y. Yu, T. Chun, C. R. Wang, A. G. Grandea, III, L. Van Kaer, and T. H. Hansen. 2001. Tapasin enhances peptide-induced expression of H2-M3 molecules, but is not required for the retention of open conformers. J. Immunol. 167: 2097-2105.
11. Peh, C. A., S. R. Burrows, M. Barnden, R. Khanna, P. Cresswell, D. J. Moss, and J. McCluskey. 1998. HLA-B27-restricted antigen presentation in the absence of tapasin reveals polymorphism in mechanisms of HLA class I peptide loading. Immunity 8: 531-542.
12. Park, B., S. Lee, E. Kim, and K. Ahn. 2003. A single polymorphic residue within the peptide-binding cleft of MHC class I molecules determines spectrum of tapasin dependence. J. Immunol. 170: 961-968.
13. Zernich, D., A. W. Purcell, W. A. Macdonald, L. Kjer-Nielsen, L. K. Ely, N. Laham, T. Crockford, N. A. Mifsud, M. Bharadwaj, L. Chang, et al. 2004. Natural HLA class I polymorphism controls the pathway of antigen presentation and susceptibility to viral evasion. J. Exp. Med. 200: 13-24.
14. Neisig, A., R. Wubbolts, X. Zang, C. Melief, and J. Neefjes. 1996. Allele-specific differences in the interaction of MHC class I molecules with transporters associated with antigen processing. J. Immunol. 156: 3196-3206.
15. Turnquist, H. R., H. J. Thomas, K. R. Prilliman, C. T. Lutz, W. H. Hildebrand, and J. C. Solheim. 2000. HLA-B polymorphism affects interactions with multiple endoplasmic reticulum proteins. Eur. J. Immunol. 30: 3021-3028.
16. Elliott, T. 1997. How does TAP associate with MHC class I molecules? Immunol. Today 18: 375-379.
17. Turnquist, H. R., S. E. Vargas, E. L. Schenk, M. M. McIlhaney, A. J. Reber, and J. C. Solheim. 2002. The interface between tapasin and MHC class I: identification of amino acid residues in both proteins that influence their interaction. Immunol. Res. 25: 261-269.
18. Park, B., Y. Kim, J. Shin, S. Lee, K. Cho, K. Fruh, and K. Ahn. 2004. Human cytomegalovirus inhibits tapasin-dependent peptide loading and optimization of the MHC class I peptide cargo for immune evasion. Immunity 20: 71-85.
19. Suh, W. K., E. K. Mitchell, Y. Yang, P. A. Peterson, G. L. Waneck, and D. B. Williams. 1996. MHC class I molecules form ternary complexes with calnexin and TAP and undergo peptide-regulated interaction with TAP via their extracellular domains. J. Exp. Med. 184: 337-348.
20. Carreno, B. M., J. C. Solheim, M. Harris, I. Stroynowski, J. M. Connolly, and T. H. Hansen. 1995. TAP associates with a unique class I conformation, whereas calnexin associates with multiple class I forms in mouse and man. J. Immunol. 155: 4726-4733.
21. 2-microglobulin complexes associate with TAP transporters before peptide binding. Nature 368: 864-867.
22. Yang, T., B. A. McNally, S. Ferrone, Y. Liu, and P. Zheng. 2003. A single-nucleotide deletion leads to rapid degradation of TAP-1 mRNA in a melanoma cell line. J. Biol. Chem. 278: 15291-15296.
23. low colon cancer reveals the functional significance of the signature domain in antigen processing. Clin. Cancer Res. 11: 3614-3623.
24. Raghuraman, G., P. E. Lapinski, and M. Raghavan. 2002. Tapasin interacts with the membrane-spanning domains of both TAP subunits and enhances the structural stability of TAP1 × TAP2 Complexes. J. Biol. Chem. 277: 41786-41794.
25. Procko, E., G. Raghuraman, D. C. Wiley, M. Raghavan, and R. Gaudet. 2005. Identification of domain boundaries within the N-termini of TAP1 and TAP2 and their importance in tapasin binding and tapasin-mediated increase in peptide loading of MHC class I. Immunol. Cell Biol. 83: 475-482.
26. Roeth, J. F., M. Williams, M. R. Kasper, T. M. Filzen, and K. L. Collins. 2004. HIV-1 Nef disrupts MHC-I trafficking by recruiting AP-1 to the MHC-I cytoplasmic tail. J. Cell Biol. 167: 903-913.
27. Parham, P., C. J. Barnstable, and W. F. Bodmer. 1979. Use of a monoclonal antibody (W6/32) in structural studies of HLA-A,B,C, antigens. J. Immunol. 123: 342-349.
28. Dick, T. P., N. Bangia, D. R. Peaper, and P. Cresswell. 2002. Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity 16: 87-98.
29. Stam, N. J., H. Spits, and H. L. Ploegh. 1986. Monoclonal antibodies raised against denatured HLA-B locus heavy chains permit biochemical characterization of certain HLA-C locus products. J. Immunol. 137: 2299-2306.
30. Blanco-Gelaz, M. A., B. Suárez-Alvarez, S. González, A. López-Vázquez, J. Martínez-Borra, and C. López-Larrea. 2006. The amino acid at position 97 is involved in folding and surface expression of HLA-B27. Int. Immunol. 18: 211-220.
31. Kasper, M. R., J. F. Roeth, M. Williams, T. M. Filzen, R. I. Fleis, and K. L. Collins. 2005. HIV-1 Nef disrupts antigen presentation early in the secretory pathway. J. Biol. Chem. 280: 12840-12848.
32. Fahnestock, M. L., I. Tamir, L. Narhi, and P. J. Bjorkman. 1992. Thermal stability comparison of purified empty and peptide-filled forms of a class I MHC molecule. Science 258: 1658-1662.
33. Khanna, R., S. R. Burrows, A. Neisig, J. Neefjes, D. J. Moss, and S. L. Silins. 1997. Hierarchy of Epstein-Barr virus-specific cytotoxic T-cell responses in individuals carrying different subtypes of an HLA allele: implications for epitope-based antiviral vaccines. J. Virol. 71: 7429-7435.
34. Furukawa, H., S. Murata, T. Yabe, N. Shimbara, N. Keicho, K. Kashiwase, K. Watanabe, Y. Ishikawa, T. Akaza, K. Tadokoro, et al. 1999. Splice acceptor site mutation of the transporter associated with antigen processing-1 gene in human bare lymphocyte syndrome. J. Clin. Invest. 103: 755-758.
35. Lauvau, G., B. Gubler, H. Cohen, S. Daniel, S. Caillat-Zucman, and P. M. van Endert. 1999. Tapasin enhances assembly of transporters associated with antigen processing-dependent and -independent peptides with HLA-A2 and HLA-B27 expressed in insect cells. J. Biol. Chem. 274: 31349-31358.
36. Garbi, N., S. Tanaka, F. Momburg, and G. J. Hammerling. 2006. Impaired assembly of the major histocompatibility complex class I peptide-loading complex in mice deficient in the oxidoreductase ERp57. Nat. Immunol. 7: 93-102.
37. Zhang, Y., E. Baig, and D. B. Williams. 2006. Functions of ERp57 in the folding and assembly of MHC Class I molecules. J. Biol. Chem. 281: 14622-14631.
38. Ogino, T., X. Wang, S. Kato, N. Miyokawa, Y. Harabuchi, and S. Ferrone. 2003. Endoplasmic reticulum chaperone-specific monoclonal antibodies for flow cytometry and immunohistochemical staining. Tissue Antigens 62: 385-393.
39. Rouiller, I., S. M. Brookes, A. D. Hyatt, M. Windsor, and T. Wileman. 1998. African swine fever virus is wrapped by the endoplasmic reticulum. J. Virol. 72: 2373-2387.
40. Otsu, M., R. Urade, M. Kito, F. Omura, and M. Kikuchi. 1995. A possible role of ER-60 protease in the degradation of misfolded proteins in the endoplasmic reticulum. J. Biol. Chem. 270: 14958-14961.
41. DiBrino, M., K. C. Parker, D. H. Margulies, J. Shiloach, R. V. Turner, W. E. Biddison, and J. E. Coligan. 1995. Identification of the peptide binding motif for HLA-B44, one of the most common HLA-B alleles in the Caucasian population. Biochemistry 34: 10130-10138.
42. Macdonald, W., D. S. Williams, C. S. Clements, J. J. Gorman, L. Kjer-Nielsen, A. G. Brooks, J. McCluskey, J. Rossjohn, and A. W. Purcell. 2002. Identification of a dominant self-ligand bound to three HLA B44 alleles and the preliminary crystallographic analysis of recombinant forms of each complex. FEBS Lett. 527: 27-32.
43. Sidney, J., S. Southwood, V. Pasquetto, and A. Sette. 2003. Simultaneous prediction of binding capacity for multiple molecules of the HLA B44 supertype. J. Immunol. 171: 5964-5974.
44. Fleischhauer, K., D. Avila, F. Vilbois, C. Traversari, C. Bordignon, and H. J. Wallny. 1994. Characterization of natural peptide ligands for HLA-B*4402 and -B*4403: implications for peptide involvement in allorecognition of a single amino acid change in the HLA-B44 heavy chain. Tissue Antigens 44: 311-317.
45. Lewis, J. W., and T. Elliott. 1998. Evidence for successive peptide binding and quality control stages during MHC class I assembly. Curr. Biol. 8: 717-720.
46. Paquet, M. E., and D. B. Williams. 2002. Mutant MHC class I molecules define interactions between components of the peptide-loading complex. Int. Immunol. 14: 347-358.
47. Tan, P., H. Kropshofer, O. Mandelboim, N. Bulbuc, G. J. Hammerling, and F. Momburg. 2002. 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. 168: 1950-1960.
48. Howarth, M., A. Williams, A. B. Tolstrup, and T. Elliott. 2004. Tapasin enhances MHC class I peptide presentation according to peptide half-life. Proc. Natl. Acad. Sci. USA 101: 11737-11742.