Differential requirement for tapasin in the presentation of leader- and insulin-derived peptide antigens to Qa-1b-restricted CTLs

Journal of Immunology

Volumn 173, Issue 6, 2004, Pages 3707-3715

  Li, LiQi ^a,f   Sullivan, Barbara A ^b,g   Aldrich, Carla J ^c   Soloski, Mark J ^d   Forman, James ^e   Grandea III, Andres G ^a,h   Jensen, Peter E ^b   Van Kaer, Luc ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Indiana University School of Medicine Evansville   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^f EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^g LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^h Celltech R and D Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD8 ANTIGEN; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 1B; INSULIN; INSULIN DERIVED PEPTIDE ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE; PEPTIDE TRANSPORTER 1; PROTEIN; QA 1B PROTEIN; SIGNAL PEPTIDE; T LYMPHOCYTE RECEPTOR; TAPASIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; ENDOPLASMIC RETICULUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE;

EID: 4644312290     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.6.3707     Document Type: Article

References (65)

1. Pamer, E., and P. Cresswell. 1998. Mechanisms of MHC class I-restricted antigen processing. Annu. Rev. Immunol. 16:323.
2. Van Kaer, L. 2002. Major histocompatibility complex class I-restricted antigen processing and presentation. Tissue Antigens 60:1.
3. Paulsson, K. M., and P. Wang. 2004. Quality control of MHC class I maturation. FASEB J. 18:31.
4. Spiliotis, E. T., H. Manley, M. Osorio, M. C. Zuniga, and M. Edidin. 2000. Selective export of MHC class I molecules from the ER after their dissociation from TAP. Immunity 13:841.
5. 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.
6. Mayer, W. E., and J. Klein. 2001. Is tapasin a modified MHC class I molecule? Immunogenetics 53:719.
7. 2-microglobulin complexes associate with TAP transporters before peptide binding. Nature 368:864.
8. 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.
9. 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.
10. Grandea, A. G. I., and L. Van Kaer. 2001. Tapasin: and ER chaperone that controls MHC class I assembly with peptide. Trends Immunol. 22:194.
11. Garbi, N., P. Tan, F. Momburg, and G. J. Hammerling. 2001. Role of tapasin in MHC class I antigen presentation in vivo. Adv. Exp. Med. Biol. 495:71.
12. Antoniou, A. N., S. J. Powis, and T. Elliott. 2003. Assembly and export of MHC class I peptide ligands. Curr. Opin. Immunol. 15:75.
13. Momburg, F., and P. Tan. 2002. Tapasin-the keystone of the loading complex optimizing peptide binding by MHC class I molecules in the endoplasmic reticulum. Mol. Immunol. 39:217.
14. Androlewicz. M. J. 1999. The role of tapasin in MHC class I antigen assembly. Immunol. Res. 20:79.
15. 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.
16. Turnquist, H. R., J. L. Petersen, S. E. Vargas, M. M. McIlhaney, E. Bedows, W. E. Mayer, A. G. I. Grandea, L. Van Kaer, and J. C. Solheim. 2004. The Ig-like domain of lapasin influences intermolecular interactions. J. Immunol. 172:2976.
17. 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.
18. 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.
19. Li, S., K. M. Paulsson, S. Chen, H.-O. Sjogren, and P. Wang. 2000. Tapasin is required for efficient peptide binding to transporter associated with antigen processing. J. Biol. Chem. 275:1581.
20. Peh, C. A., N. Laham, Y. Burrows, Y. Zhu, and J. McCluskey. 2000. Distinct functions of tapasin revealed by polymorphism in MHC class I peptide loading. J. Immunol. 164:292.
21. 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.
22. d molecules share common tapasin dependencies as determined using a novel epitope tag. J. Immunol. 165:5656.
23. 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.
24. Barnden, M. J., A. W. Purcell, J. J. Gorman, and J. McCluskey. 2000. Tapasin-mediated retention and optimization of peptide ligands during the assembly of class I molecules. J. Immunol. 165:322.
25. Garbi, N., P. Tan, A. D. Diehl, B. J. Chambers, H. G. Ljunggren, F. Momburg, and G. J. Hammerling. 2000. Impaired immune responses and altered peptide repertoire in tapasin-deficient mice. Nat. Immunol. 1:234.
26. Paulsson, K. M., M. J. Kleijmeer, J. Griffith, M. Jevon, S. Chen, P. O. Anderson, H.-O. Sjogren, S. Li, and P. Wang. 2002. Association of tapasin and COPI provides a new mechanism for the retrograde transport of MHC class I molecules from the Golgi complex to the ER. J. Biol. Chem. 277:18266.
27. Sijts, A. J., and E. G. Pamer. 1997. Enhanced intracellular dissociation of major histocompatibility complex class I-associated peptides: a mechanism for optimizing the spectrum of cell surface-presented cytotoxic T lymphocyte epitopes. J. Exp. Med. 185:1403.
28. 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.
29. 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.
30. Wolf, P. R., and R. G. Cook. 1990. The TL region gene 37 encodes a Qa-1 antigen. J. Exp. Med. 172:1795.
31. Cotteril, L. A., H. J. Staus, M. M. Milrain, D. J. Pappin, D. Rahman, B. Canas, P. Chandler, A. Stackpoole, E. Simpsom, P. J. Robinson, and P. J. Dyson. 1997. Qa-1 interaction and T cell recognition of the Qa-1 determinant modifier peptide. Eur. J. Immunol. 27:2123.
32. Aldrich, C. J., A. DeCloux, A. S. Woods, R. J. Cotter, M. J. Soloski, and J. Forman. 1994. Identification of a Tap-dependent leader peptide recognized by alloreactive T cells specific for a class Ib antigen. Cell 79:649.
33. b. J. Immunol. 158:2183.
34. b. Immunity 9:413.
35. b. J. Immunol. 165:7025.
36. Lemberg, M. K., and B. Martoglio. 2002. Requirements for signal peptide peptidase-catalyzed intramembrane proteolysis. Mol. Cell 10:735.
37. d. Eur. J. Immunol. 12:159.
38. Aldrich, C. J., J. R. Rodgers, and R. R. Rich. 1988. Regulation of Qa-1 expression and determinant modification by an H-2D-linked gene, Qdm. Immunogenetics 28:334.
39. b peptide binding specificity and the capacity of CD94/NKG2A to discriminate between Qa-1-peptide complexes. J. Exp. Med. 192:613.
40. b molecule binds to a large subpopulation of murine NK cells. Eur. J. Immunol. 28:4356.
41. b. J. Exp. Med. 188:1841.
42. b. J. Exp. Med. 188:961.
43. Lo, W. F., A. S. Woods, A. DeCloux, R. J. Cotter, E. S. Metcalf, and M. J. Soloski. 2000. Molecular mimicry mediated by MHC class Ib molecules after infection with Gram-negative pathogens. Nat. Med. 6:215.
44. b as a key restricting element for Listeria-specific CTLs. J. Immunol. 159:2795.
45. + T cells restricted by the MHC class Ib molecule, Qa-1. Annu. Rev. Immunol. 18:185.
46. Tajima, A., T. Tanaka, T. Ebata, K. Takeda, A. Kawasaki, J. M. Kelly, P. K. Darcy, R. E. Vance, D. H. Raulet, K. Kinoshita, et al. 2003. Blastocyst MHC, a putative murine homologue of HLA-G, protects TAP-deficient tumor cells from natural killer cell-mediated rejection in vivo. J. Immunol. 171:1715.
47. Davies, A., S. Kalb, B. Liang, C. J. Aldrich, F. A. Lemonnier, H. Jiang, R. Cotter, and M. J. Soloski. 2003. A peptide from heat shock protein 60 is the dominant peptide bound to Qa-1 in the absence of the MHC class Ia leader sequence peptide Qdm. J. Immunol. 170:5027.
48. + T cells. Cell 71:1205.
49. Sullivan, B. A., P. Kraj, D. A. Weber, L. Ignatowicz, and P. E. Jensen. 2002. Positive selection of a Qa-1-restricted T cell receptor with specificity for insulin. Immunity 17:95.
50. Grandea, A. G. I., P. J. Lehner, P. Cresswell, and T. Spies. 1997. Regulation of MHC class I heterodimer stability and interaction with TAP by tapasin. Immunogenetics 46:260.
51. Hermel, E., C. Smith, and C. J. Aldrich. 2000. Allogeneic responses to the class Ib antigen Qa1: limited T-cell receptor Vα but not Vβ chain usage. J. Immunol. 51:600.
52. Singh, N., S. Hong, D. C. Scherer, I. Serizawa, N. Burdin, M. Kronenberg, Y. Koezuka, and L. Van Kaer. 1999. Cutting edge: activation of NK T cells by CD1d and α-galactosylceramide directs conventional T cells to the acquisition of a Th2 phenotype. J. Immunol. 163:2373.
53. Kambayashi, T., J. R. Kraft-Leavy, J. G. Dauner, B. A. Sullivan, O. Laur, and P. E. Jensen. 2004. The nonclassical MHC class I molecule Qa-1 forms unstable peptide complexes. J. Immunol. 172:1661.
54. Ljunggren, H. G., N. J. Stam, C. Ohlen, J. J. Neefjes, P. Hoglund, M. T. Heemels, J. Bastin, T. N. Schumacher, A. Townsend, K. Karre, and H. L. Ploegh. 1990. Empty MHC class I molecules come out in the cold. Nature 346:476.
55. Schumacher, T. N., M. T. Heemels, J. J. Neefjes, W. M. Kast, C. J. Melief, and H. L. Ploegh. 1990. Direct binding of peptide to empty MHC class I molecules on intact cells and in vitro. Cell 62:563.
56. Townsend, A., T. Elliott, V. Cerundolo, L. Foster, B. Barber, and A. Tse. 1990. Assembly of MHC class I molecules analyzed in vitro. Cell 62:285.
57. Wiertz, E. J., D. Tortorella, M. Bogyo, J. Yu, W. Mothes, T. R. Jones, T. A. Rapoport, and H. L. Ploegh. 1996. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384:432.
58. Hughes, E. A., C. Hammond, and P. Cresswell. 1997. Misfolded major histocompatibility complex class I heavy chains are translocated into the cytoplasm and degraded by the proteasome. Proc. Natl. Acad. Sci. USA 94:1896.
59. Ramirez, M. C., and L. J. Sigal. 2004. The multiple routes of MHC-1 cross-presentation. Trends Microbiol. 12:204.
60. Grandea, A. G., III, M. J. Androlewicz, R. S. Athwal, D. E. Geraghty, and T. Spies. 1995. Dependence of peptide binding by MHC class I molecules on their interaction with TAP. Science 270:105.
61. Park, B., and K. Ahn. 2003. An essential function of tapasin in quality control of HLA-G molecules. J. Biol. Chem. 278:14337.
62. Lybarger, L., Y. Y. L. Yu, T. Chun, C.-R. Wang, A. G. Grandea, 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.
63. Chun, T., A. G. Grandea, 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.
64. Braud, V. M., D. S. J. Allan, D. Wilson, and A. J. McMichael. 1997. TAP- and tapasin-dependent HLA-E surface expression correlates with the binding of an MHC class I leader peptide. Curr. Biol. 8:1.
65. Lee, N., and D. E. Geraghty. 2003. HLA-F surface expression of B cell and monocyte cell lines is partially independent from tapasin and completely independent from TAP. J. Immunol. 171:5264.