Distinct functions for the glycans of tapasin and heavy chains in the assembly of MHC class I molecules

Journal of Immunology

Volumn 186, Issue 4, 2011, Pages 2309-2320

  Rizvi, Syed Monem ^a   Del Cid, Natasha ^a   Lybarger, Lonnie ^b   Raghavan, Malini ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALRETICULIN; ERP57; GLYCAN; HETERODIMER; IMMUNOGLOBULIN M; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; OXIDOREDUCTASE; PEPTIDE DERIVATIVE; PEPTIDE LOADING COMPLEX; TAPASIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HEAVY CHAIN; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN INTERACTION;

AMINO ACID SUBSTITUTION; ANIMALS; BETA 2-MICROGLOBULIN; CELL LINE; CELL LINE, TUMOR; CONSERVED SEQUENCE; HLA-A2 ANTIGEN; HUMANS; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; POLYSACCHARIDES; PROTEIN FOLDING; SIGNAL TRANSDUCTION;

EID: 79951835547     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002959     Document Type: Article

References (44)

1. Wearsch, P. A., and P. Cresswell. 2008. The quality control of MHC class I peptide loading. Curr. Opin. Cell Biol. 20: 624-631.
2. Schrag, J. D., J. J. Bergeron, Y. Li, S. Borisova, M. Hahn, D. Y. Thomas, and M. Cygler. 2001. The structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol. Cell 8: 633-644. (Pubitemid 32946940)
3. Frickel, E. M., R. Riek, I. Jelesarov, A. Helenius, K. Wuthrich, and L. Ellgaard. 2002. TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain. Proc. Natl. Acad. Sci. USA 99: 1954-1959.
4. Helenius, A., and M. Aebi. 2004. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73: 1019-1049.
5. Sadasivan, B., P. J. Lehner, B. Ortmann, T. Spies, and P. Cresswell. 1996. Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity 5: 103-114. (Pubitemid 26301087)
6. Harris, M. R., Y. Y. Yu, C. S. Kindle, T. H. Hansen, and J. C. Solheim. 1998. Calreticulin and calnexin interact with different protein and glycan determinants during the assembly of MHC class I. J. Immunol. 160: 5404-5409.
7. Harris, M. R., L. Lybarger, N. B. Myers, C. Hilbert, J. C. Solheim, T. H. Hansen, and Y. Y. L. Yu. 2001. Interactions of HLA-B27 with the peptide loading complex as revealed by heavy chain mutations. Int. Immunol. 13: 1275-1282.
8. Sadasivan, B. K., A. Cariappa, G. L. Waneck, and P. Cresswell. 1995. Assembly, peptide loading, and transport of MHC class I molecules in a calnexin-negative cell line. Cold Spring Harb. Symp. Quant. Biol. 60: 267-275.
9. Scott, J. E., and J. R. Dawson. 1995. MHC class I expression and transport in a calnexin-deficient cell line. J. Immunol. 155: 143-148.
10. Gao, B., R. Adhikari, M. Howarth, K. Nakamura, M. C. Gold, A. B. Hill, R. Knee, M. Michalak, and T. Elliott. 2002. Assembly and antigen-presenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin. Immunity 16: 99-109. (Pubitemid 34143220)
11. Ireland, B. S., U. Brockmeier, C. M. Howe, T. Elliott, and D. B. Williams. 2008. Lectin-deficient calreticulin retains full functionality as a chaperone for class I histocompatibility molecules. Mol. Biol. Cell 19: 2413-2423.
12. Del Cid, N., E. Jeffery, S. M. Rizvi, E. Stamper, L. R. Peters, W. C. Brown, C. Provoda, and M. Raghavan. 2010. Modes of calreticulin recruitment to the major histocompatibility complex class I assembly pathway. J. Biol. Chem. 285: 4520-4535.
13. 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. (Pubitemid 34143219)
14. Peaper, D. R., and P. Cresswell. 2008. The redox activity of ERp57 is not essential for its functions in MHC class I peptide loading. Proc. Natl. Acad. Sci. USA 105: 10477-10482.
15. Vigneron, N., D. R. Peaper, R. M. Leonhardt, and P. Cresswell. 2009. Functional significance of tapasin membrane association and disulfide linkage to ERp57 in MHC class I presentation. Eur. J. Immunol. 39: 2371-2376.
16. Rizvi, S. M., and M. Raghavan. 2010. Mechanisms of function of tapasin, a critical major histocompatibility complex class I assembly factor. Traffic 11: 332-347.
17. Belicha-Villanueva, A., S. McEvoy, K. Cycon, S. Ferrone, S. O. Gollnick, and N. Bangia. 2008. Differential contribution of TAP and tapasin to HLA class I antigen expression. Immunology 124: 112-120. (Pubitemid 351537578)
18. Shimizu, Y., D. E. Geraghty, B. H. Koller, H. T. Orr, and R. DeMars. 1988. Transfer and expression of three cloned human non-HLA-A, B, C class I major histocompatibility complex genes in mutant lymphoblastoid cells. Proc. Natl. Acad. Sci. USA 85: 227-231.
19. Pear, W. S., G. P. Nolan, M. L. Scott, and D. Baltimore. 1993. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. USA 90: 8392-8396.
20. 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.
21. Androlewicz, M. J., B. Ortmann, P. M. van Endert, T. Spies, and P. Cresswell. 1994. Characteristics of peptide and major histocompatibility complex class I/beta 2-microglobulin binding to the transporters associated with antigen processing (TAP1 and TAP2). Proc. Natl. Acad. Sci. USA 91: 12716-12720.
22. Brodsky, F. M., W. F. Bodmer, and P. Parham. 1979. Characterization of a monoclonal anti-beta 2-microglobulin antibody and its use in the genetic and biochemical analysis of major histocompatibility antigens. Eur. J. Immunol. 9: 536-545.
23. 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. (Pubitemid 37338878)
24. 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.
25. Simone, L. C., X. Wang, A. Tuli, and J. C. Solheim. 2010. Effect of a tapasin mutant on the assembly of the mouse MHC class I molecule H2-K(d). Immunol. Cell Biol. 88: 57-62.
26. Diedrich, G., N. Bangia, M. Pan, and P. Cresswell. 2001. A role for calnexin in the assembly of the MHC class I loading complex in the endoplasmic reticulum. J. Immunol. 166: 1703-1709. (Pubitemid 32114653)
27. Ortmann, B., M. J. Androlewicz, and P. Cresswell. 1994. MHC class I/beta 2-microglobulin complexes associate with TAP transporters before peptide binding. Nature 368: 864-867. (Pubitemid 24137752)
28. Suh, W. K., M. F. Cohen-Doyle, K. Fruh, K. Wang, P. A. Peterson, and D. B. Williams. 1994. Interaction of MHC class I molecules with the transporter associated with antigen processing. Science 264: 1322-1326.
29. Peaper, D. R., P. A. Wearsch, and P. Cresswell. 2005. Tapasin and ERp57 form a stable disulfide-linked dimer within the MHC class I peptide-loading complex. EMBO J. 24: 3613-3623. (Pubitemid 41509368)
30. Lindquist, J. A., G. J. Hämmerling, and J. Trowsdale. 2001. ER60/ERp57 forms disulfide-bonded intermediates with MHC class I heavy chain. FASEB J. 15: 1448-1450.
31. Kienast, A., M. Preuss, M. Winkler, and T. P. Dick. 2007. Redox regulation of peptide receptivity of major histocompatibility complex class I molecules by ERp57 and tapasin. Nat. Immunol. 8: 864-872.
32. Martayan, A., L. Sibilio, A. Setini, E. Lo Monaco, E. Tremante, D. Fruci, M. Colonna, and P. Giacomini. 2008. N-linked glycosylation selectively regulates the generic folding of HLA-Cw1. J. Biol. Chem. 283: 16469-16476.
33. Zhang, Q., M. Tector, and R. D. Salter. 1995. Calnexin recognizes carbohydrate and protein determinants of class I major histocompatibility complex molecules. J. Biol. Chem. 270: 3944-3948.
34. Radcliffe, C. M., G. Diedrich, D. J. Harvey, R. A. Dwek, P. Cresswell, and P. M. Rudd. 2002. Identification of specific glycoforms of major histocompatibility complex class I heavy chains suggests that class I peptide loading is an adaptation of the quality control pathway involving calreticulin and ERp57. J. Biol. Chem. 277: 46415-46423.
35. Wearsch, P. A., C. A. Jakob, A. Vallin, R. A. Dwek, P. M. Rudd, and P. Cresswell. 2004. Major histocompatibility complex class I molecules expressed with monoglucosylated N-linked glycans bind calreticulin independently of their assembly status. J. Biol. Chem. 279: 25112-25121.
36. Dong, G., P. A. Wearsch, D. R. Peaper, P. Cresswell, and K. M. Reinisch. 2009. Insights into MHC class I peptide loading from the structure of the tapasin-ERp57 thiol oxidoreductase heterodimer. Immunity 30: 21-32.
37. 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.
38. Solheim, J. C., M. R. Harris, C. S. Kindle, and T. H. Hansen. 1997. 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: 2236-2241.
39. Shimizu, Y., and R. DeMars. 1989. Production of human cells expressing individual transferred HLA-A,-B,-C genes using an HLA-A,-B,-C null human cell line. J. Immunol. 142: 3320-3328. (Pubitemid 19129961)
40. Pedersen, L. O., A. S. Hansen, A. C. Olsen, J. Gerwien, M. H. Nissen, and S. Buus. 1994. The interaction between beta 2-microglobulin (beta 2m) and purified class-I major histocompatibility (MHC) antigen. Scand. J. Immunol. 39: 64-72.
41. Rizvi, S. M., and M. Raghavan. 2006. Direct peptide-regulatable interactions between MHC class I molecules and tapasin. Proc. Natl. Acad. Sci. USA 103: 18220-18225.
42. Bangia, N., P. J. Lehner, E. A. Hughes, M. Surman, and P. Cresswell. 1999. The N-terminal region of tapasin is required to stabilize the MHC class I loading complex. Eur. J. Immunol. 29: 1858-1870.
43. 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. (Pubitemid 28123749)
44. Garbi, N., N. Tiwari, F. Momburg, and G. J. Hämmerling. 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.